Kristjansson 2009
Kristjansson 2009
                                                                                                                  P
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                          frequent occurrence in both men and women,41 and patients                                                       mobility comes at the expense of its me-
                                                                                                                                                                                                                                          chanical stability.7,22 The highly developed
                                                                                                                          with neck pain are the second largest group (after patients with
                                                                                                                                                                                                                                          proprioceptive system provides neuro-
                                                                                                                          low back pain) attending physical therapy and chiropractic                                                      muscular control to the mobile cervical
                                                                                                                  clinics for relief of their symptoms.2 Further research shows that                                                      spine and allows efficient utilization of
Copyright © 2009 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
                                                                                                                  about one third of patients diagnosed with whiplash-associated                                                          the vital organs in the head42 via unique
                                                                                                                  disorder (WAD) (a variety of clinical manifestations due to bony or                                                     connections to the vestibular and visual
                                                                                                                                                                                                                                          systems.22,77,80,87,109 This may explain why
                                                                                                                  soft tissue neck injuries following an               an ineffective treatment. Preventing a                             the cervical spine is an extremely vulner-
                                                                                                                  acceleration-deceleration energy                         portion of patients with neck pain                             able structure, especially where trauma
                                                                                                                  transfer sustained from a mo-                             to enter the chronic phase of their                           is involved (eg, whiplash injury), and is a
                                                                                                                  tor vehicle accident119) only gain                        condition represents a great chal-                            source of a plethora of symptoms that do
                                                                                                                                                           SUPPLEMENTAL
                                                                                                                  short-term relief by conven-              VIDEO ONLINE    lenge for clinicians.                                         not arise from any other musculoskeletal
                                                                                                                  tional musculoskeletal interven-                             The cervical spine, especially                             region of the body.58
Journal of Orthopaedic & Sports Physical Therapy®
                                                                                                                  tions,12,82,123 which, by definition, are               the upper cervical spine, is the most                                Disturbances to the afferent input
                                                                                                                                                                                                                                          from the cervical region in those with
                                                                                                                   T SYNOPSIS: The term sensorimotor describes               might be an important factor in the maintenance,             neck pain may be a possible cause of
                                                                                                                   all the afferent, efferent, and central integration       recurrence, or progression of various symptoms in            symptoms such as dizziness, unsteadi-
                                                                                                                   and processing components involved in maintain-           some patients with neck pain. In these cases, more           ness, and visual disturbances, as well as
                                                                                                                   ing stability in the postural control system through      specific and novel treatment methods are needed               signs of altered postural stability, cervical
                                                                                                                   intrinsic motor-control properties. The scope of          which progressively address neck position and                proprioception, and head and eye move-
                                                                                                                   this paper is to highlight the sensorimotor deficits       movement sense, as well as cervicogenic oculomo-             ment control. Conventional approaches
                                                                                                                   that can arise from altered cervical afferent             tor disturbances, postural stability, and cervico-           to management may be sufficient for pa-
                                                                                                                   input. From a clinical orthopaedic perspective,           genic dizziness. In this commentary we review the
                                                                                                                                                                                                                                          tients with neck pain with minimal sen-
                                                                                                                   the peripheral mechanoreceptors are the most              most relevant theoretical and practical knowledge
                                                                                                                   important in functional joint stability; but in the       on this matter and implications for clinical assess-
                                                                                                                                                                                                                                          sorimotor proprioceptive disturbances.
                                                                                                                   cervical region they are also important for postural      ment and management, and we propose future                   However, clinical experience and research
                                                                                                                   stability, as well as head and eye movement               directions for research.                                     indicates that significant sensorimotor
                                                                                                                   control. Consequently, conventional musculosk-                                                                         proprioceptive disturbances in the cervi-
                                                                                                                                                                             TB;L;BE<;L?:;D9;0 Level 5. J Orthop Sports
                                                                                                                   eletal intervention approaches may be sufficient                                                                       cal spine might be an important factor in
                                                                                                                                                                             Phys Ther 2009;39(5):364-377. doi:10.2519/
                                                                                                                   only for patients with neck pain and minimal                                                                           the maintenance, recurrence, or progres-
                                                                                                                                                                             jospt.2009.2834
                                                                                                                   sensorimotor proprioceptive disturbances. Clinical
                                                                                                                                                                                                                                          sion of various symptoms in patients with
                                                                                                                   experience and research indicates that significant         TA;OMEH:I0 cervical, head, postural stability,
                                                                                                                   sensorimotor cervical proprioceptive disturbances         proprioception, sensorimotor                                 neck pain.52,122 Thus, addressing these
                                                                                                                                                                                                                                          deficits is likely to be an important step
                                                                                                                   1
                                                                                                                     Physical Therapist and Researcher, Faculty of Medicine, The University of Iceland, Reykjavik, Iceland. 2 Physical Therapist and Researcher/Lecturer, Neck pain and Whiplash
                                                                                                                   Research Unit, Division of Physiotherapy, University of Queensland, Australia. Address correspondence to Eythor Kristjansson, Skipholt 50c, IS-105 Reykjavik, Iceland. E-mail:
                                                                                                                   eythork@simnet.is
                                                                                                                  364 | may 2009 | volume 39 | number 5 | journal of orthopaedic & sports physical therapy
                                                                                                                  towards better management of some pa-                                                         
                                                                                                                  tients with neck pain.                                                                      
                                                                                                                      The scope of this paper is to high-                                      	                                                                 
                                                                                                                  light the sensorimotor deficits that can                                                                                                           
                                                                                                                  arise from altered cervical afferent input.
                                                                                                                  While the cervical spine should always                                     	
                                                                                                                  be considered in the differential diagno-
                                                                                                                  sis of dizziness and unsteadiness, as well
                                                                                                                  as visual disturbances, other potential
                                                                                                                  causes, such as peripheral or central ves-
                                                                                                                                                                                                                               CNS integration
                                                                                                                  tibular pathology and pathology in the                                 
                                                                                                                  central nervous system (CNS) along with
                                                                                                                  vertebrobasilar insufficiency, must also
                                                                                                                  be considered and excluded.57 The mere
                                                                                                                                                                                     
                                                                                                                  combination of dizziness and neck pain
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                                                                                      
                                                                                                                                                                                                                                                
                                                                                                                  should not be interpreted as necessar-                                  
                                                                                                                                                                                                                                                  
                                                                                                                  ily indicating the neck to be the source                           
                                                                                                                  of the dizziness.64 Dizziness and visual
                                                                                                                                                                                                                                                                  
                                                                                                                  disturbances as a consequence of altered                                                             
                                                                                                                  afferent input from the cervical spine                                                           
Copyright © 2009 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
                                                                                                                  CNS or vestibular system pathologies.31,134      ments.56 <?=KH;' provides an overview of                    don organs, fine tune the muscle spindle
                                                                                                                  Nevertheless, the presence of CNS signs          the subsystems in the postural control                       information, predominantly by reflex ef-
                                                                                                                  in the absence of a diagnosis or other ex-       system. The somatosensory, vestibular,                       fects on the H-motoneurones.116
                                                                                                                  planation should be considered a red flag         and visual systems are the subsystems                           The dense network of mechanorecep-
                                                                                                                  and the physical therapist should imme-          that provide sensory input to the postural                   tors in the soft tissues in this region not
                                                                                                                  diately refer the patient to a physician for     control system.                                              only controls multiple degrees of freedom
                                                                                                                  further workup.                                  The Somatosensory Subsystem This                             of movements about each of its joints but,
                                                                                                                                                                   system encompasses all of the mecha-                         more importantly, gives the CNS infor-
                                                                                                                  J^[9[hl_YWbIf_d[WdZj^[FeijkhWb             noreceptive information arising from                         mation about the orientation of the head
                                                                                                                  9edjhebIoij[c                                   the periphery43 which leads to the per-                      with respect to the rest of the body via
                                                                                                                  The postural control system includes all         ception of pain, temperature, touch, and                     direct neurophysiological connections to
                                                                                                                  the sensorimotor and musculoskeletal             proprioception.110 The proprioceptive                        the vestibular and visual systems. Soma-
                                                                                                                  components involved in the control of            system of the cervical spine, in particular,                 tosensory information from the cervical
                                                                                                                  2 important behavioral goals: postural           is extremely well developed, as reflected                     region is the only region that has this
                                                                                                                  orientation and postural equilibrium.            by an abundance of mechanoreceptors,                         direct access to the sense of balance and
                                                                                                                  Postural orientation is the relative posi-       especially from the H-muscle spindles                        sense of sight.23,57
                                                                                                                  tioning of the body segments with respect        in the deep segmental upper cervical                         The Vestibular Subsystem This system is
                                                                                                                  to each other and to the environment,            muscles.73,76,122 The H-muscle spindle sys-                  specially designed to maintain adequate
                                                                                                                  whereas postural equilibrium is the state        tem serves as the final common pathway                        postural tone in the muscles of the trunk
                                                                                                                  in which all the forces acting on the body       for the regulation of the muscle stiffness                   and extremities to provide overall bal-
                                                                                                                  tend to keep the body in a desired posi-         required for various neuromuscular per-                      ance during posture and locomotion.
                                                                                                                  tion and orientation (static equilibrium)        formances.116 Muscle spindle afferents                       Neck, eye, trunk, and limb muscle reflex-
                                                                                                                  or to move in a controlled way (dynamic          appear particularly important, as they                       es evolved to meet these requirements.
                                                                                                                                                                 journal of orthopaedic & sports physical therapy | volume 39 | number 5 | may 2009 | 365
                                                                                                                                                        [   CLINICAL COMMENTARY                                     ]
                                                                                                                  The specialized mechanoreceptors in the        where vestibular, ocular, and proprio-          and head movement illusions,69,79,126 and
                                                                                                                  semicircular canals are sensitized during      ceptive information is integrated.129 The       has been shown to influence postural
                                                                                                                  changes in rate of motion; that is, angu-      CCN also has important connections to           stability and the velocity and direction
                                                                                                                  lar velocity, and the specialized mecha-       the VNC.94 This allows the postural con-        of gait and running.9,18,79 Even wearing a
                                                                                                                  noreceptors in the otolith systems of the      trol system to quickly receive information      restrictive brace (hard collar) for 5 days
                                                                                                                  utricular and saccular maculae provide         about the position and movement of the          or being exposed to sustained isometric
                                                                                                                  information about the position and veloc-      head in relation to the body and to inte-       neck muscle contraction has been dem-
                                                                                                                  ity of the head relative to the direction of   grate cervical information with that from       onstrated to lead to altered eye move-
                                                                                                                  the forces of gravity.50 Sensory informa-      the labyrinths and eyes so that different       ment control, increased postural sway,
                                                                                                                  tion from the vestibular system converges      information from the subsystems can be          and disturbed head-neck awareness in
                                                                                                                  in all nuclei comprising the vestibular        compared and equalized.                         healthy persons.21,39,66,98,113,114,140
                                                                                                                  nuclear complex (VNC) via the vestibular       Reflex Pathways Close connections be-                The upper cervical region has an
                                                                                                                  nerve and in the cerebellum.95                 tween the cervical somatosensory, vestibular,   abundance of muscle spindle receptors
                                                                                                                  The Visual Subsystem Vision plays a            and visual systems are also demonstrated in     and greater contributions to reflex ac-
                                                                                                                  dominant role in the guidance of move-         a number of reflexes influencing head ori-        tivity and connections to the visual and
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                  ments and this is reflected by the fact         entation, postural stability, and eye move-     vestibular systems when compared to the
                                                                                                                  that when somatosensory inputs and vi-         ment control.89,102 The cervicocollic reflex,    lower cervical spine.77,80,93,94 This might
                                                                                                                  sion disagree, it is usually the visual ver-   the cervico-ocular reflex, and the tonic neck    suggest that patients with neck pain with
                                                                                                                  sion of events that prevails.121 The visual    reflex are generated by cervical afferents       upper cervical complaints have greater
                                                                                                                  postural system consists of 3 different eye    and work in conjunction with other ves-         potential for balance and visual distur-
Copyright © 2009 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
                                                                                                                  movement systems: the smooth pursuit           tibular and visual reflexes for coordinated      bances than those with complaints from
                                                                                                                  system, the saccadic system, and the op-       stability of posture, as well as head and       the lower cervical spine.128
                                                                                                                  tokinetic system.129 The smooth pursuit        eye movement control. The cervicocollic             In patients with neck pain, there are
                                                                                                                  system stabilizes images of smoothly           reflex works with the vestibulocollic reflex      several mechanisms that could disturb
                                                                                                                  moving targets on the fovea by slow eye        to activate neck muscles and protect the        cervical afferent activity. Sensitivity of
                                                                                                                  movements. The saccadic system, on the         cervical spine against overrotation.102,103     the receptors can be affected by chemi-
                                                                                                                  other hand, is responsible for rapid, small    The cervico-ocular reflex works with the         cal changes brought about by ischemic
                                                                                                                  movements of both eyes simultaneously          vestibulo-ocular and optokinetic reflexes        or inflammatory events,127 as well as re-
                                                                                                                  in changing a point of fixation. The op-        to control the extraocular muscles, creat-      flex joint inhibition of the muscle spin-
Journal of Orthopaedic & Sports Physical Therapy®
                                                                                                                  tokinetic system stabilizes images on the      ing clear vision with head movement. The        dles.86,127,142 Pain at many levels of the
                                                                                                                  entire retina whenever the entire visual       tonic neck reflex maintains a stable pos-        CNS can change muscle spindle sensi-
                                                                                                                  field is moving (eg, when walking).129          ture via alteration in limb muscle activity     tivity and alter the cortical representa-
                                                                                                                                                                 when the body moves with respect to the         tion and modulation of cervical afferent
                                                                                                                  H[b[lWdjD[khef^oi_ebe]_YWb9edd[Yj_edi        head and is integrated with the vestibu-        input.34,78,127 Psychosocial distress also
                                                                                                                  There are many direct neurophysiological       lospinal reflex.145                              has the potential to alter muscle spindle
                                                                                                                  connections between these 3 subsystems                                                         activity via activation of the sympathetic
                                                                                                                  and from the cervical region to the pos-       JH7DIB7J?D=H;B;L7DJ                           nervous system.101 Functional impair-
                                                                                                                  tural control system, which provides fur-      H;I;7H9>?DJE9B?D?97B                         ment of the muscles, such as increased
                                                                                                                  ther evidence for the plausability of the      FH79J?9;                                        fatigability,28 and degenerative changes,
                                                                                                                  varied signs and symptoms that occur as                                                        such as fiber transformation,139 fatty in-
                                                                                                                  a consequence of disturbed cervical affer-                                                     filtration, and atrophy of the neck mus-
                                                                                                                                                                 T
                                                                                                                                                                       he importance of the above
                                                                                                                  ent input in those with neck pain.                   neurophysiological connections be-        cles,25,72,88 may alter their proprioceptive
                                                                                                                     Mechanoreceptor input from the                    tween the cervical spine structures       capabilities, joint mechanics, and muscle
                                                                                                                  uppermost cervical segments (Occiput-          and the vestibular and visual systems           spindle sensitivity, thus affecting cervical
                                                                                                                  Atlas, Atlas-Axis, Axis-C3), particularly      is demonstrated by the adverse effects          afferent input.20
                                                                                                                  from the upper cervical spine muscles,         on postural stability and eye and head              Sensorimotor control deficits such
                                                                                                                  has direct access to the VNC and the           movement control following artificial dis-       as disturbances to head-neck aware-
                                                                                                                  superior colliculus, a reflex centre for        turbance to cervical afferents in healthy       ness,45,73,81,107,136 neck movement control,74
                                                                                                                  coordination between vision and neck           human subjects. For example, stimula-           postural stability,1,84,90,112,118,135,138 and oc-
                                                                                                                  movement.17 It also converges in the           tion of the muscle spindle afferents, via       ulomotor control53,124,129,134 can present in
                                                                                                                  central cervical nucleus (CCN),94 which        neck muscle vibration induces eye posi-         patients with idiopathic neck pain and
                                                                                                                  serves as a pathway to the cerebellum          tion changes, visual illusory movements,        in those not specifically complaining of
                                                                                                                  366 | may 2009 | volume 39 | number 5 | journal of orthopaedic & sports physical therapy
                                                                                                                  dizziness, unsteadiness, or visual dis-             and then converted into degrees (angle         segmental support and control has been
                                                                                                                  turbances as symptoms.31,73,130 However,            = tan-1[error distance/90 cm]). Thus           demonstrated15,85 and clinical research
                                                                                                                  these sensorimotor control deficits have             an approximately 7.1-cm error distance         indicates that many patients with neck
                                                                                                                  been shown to be more pronounced in                 would translate to a meaningful error of       pain have inadequate support from these
                                                                                                                  patients with whiplash injury and those             4.5° (as long as the subject is sitting 90     muscles.26,29,62 Insufficiency in the pre-
                                                                                                                  with complaints of dizziness, unsteadi-             cm from the wall) and is called the joint      programmed activation of the cervical
                                                                                                                  ness, or visual disturbances.128,130,134,136        position error (JPE).107,111 JPE can be as-    muscles, altered motor control recruit-
                                                                                                                  Furthermore, there does not appear to be            sessed on return from all active cervical      ment patterns, and increased fatigabil-
                                                                                                                  a direct relationship between the impair-           movements. Errors of greater than 4.5°         ity have also been found in patients with
                                                                                                                  ments, such that an individual patient              are thought to suggest impairment in re-       neck pain.27,28 Further, the measured in-
                                                                                                                  may present with dysfunction in either 1            location accuracy of the head-neck.107,111     creased activation of the superficial cervi-
                                                                                                                  or several systems, and thus evaluation of          Patients might also demonstrate jerky or       cal musculature in those with neck pain
                                                                                                                  each area of sensorimotor control should            altered movement patterns, overshoot-          is thought to be a compensation for poor
                                                                                                                  be considered appropriate for all patients          ing of the position in order to gain more      passive or active segmental support.28,73
                                                                                                                  with neck pain.133                                  proprioceptive feedback for the task, or           These changes in muscle function
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                                                                      “searching” for the position. Occasionally     have potential to overload painful cervi-
                                                                                                                  :_ijkhX[Z>[WZ#D[Ya7mWh[d[ii                       patients will also experience a reproduc-      cal structures and affect cervical move-
                                                                                                                  Clinical Research Relocation tests that             tion of dizziness and/or unsteadiness          ment sense and control. This may cause
                                                                                                                  either relocate the natural head posture            with the task. A computerized method           uncertainty for the patient, automatically
                                                                                                                  or the head to a set point in range have            for assessing position sense in the clini-     leading to further increased muscle cocon-
Copyright © 2009 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
                                                                                                                  most commonly been used to verify poor              cal setting is currently being developed.      traction,36 diminishing range of motion
                                                                                                                  awareness of the head-neck region in pa-            The goal is to improve measurement ac-         for self-protection of the cervical spine
                                                                                                                  tients with neck pain to reflect impaired            curacy and to provide more sophisticated       movements. This could reduce the fre-
                                                                                                                  cervical position sense. These methods              feedback than the laser beam method,           quency and duration of muscle relaxation
                                                                                                                  address a patient’s ability to consciously          while ensuring that each patient can start     periods, causing release of inflammatory
                                                                                                                  indicate when a prespecified position                the treatment for improving head-neck          substances and promoting a vicious cy-
                                                                                                                  has been reproduced. Impairments have               awareness at his/her impairment level.         cle.6 Patients with chronic whiplash pres-
                                                                                                                  been demonstrated by these methods                                                                 ent as a difficult clinical condition as the
                                                                                                                  in subjects with neck pain of both idio-            :_ijkhX[ZD[YaCel[c[dj9edjheb                initial trauma can also compromise joint
Journal of Orthopaedic & Sports Physical Therapy®
                                                                                                                  pathic and traumatic origin (ie, whiplash           Clinical Research Despite many attempts        stability by permanent changes in tissue
                                                                                                                  injury).45,73,81,107,136 Patients who overshoot     to quantify intersegmental movements in        compliance or cause direct damage to
                                                                                                                  targets when position sense is measured             the spine and to describe the movements        the mechanoreceptors and their axons,
                                                                                                                  may have disordered cervicocollic reflex             qualitatively, no method has yet been vali-    because they have lower tensile strength
                                                                                                                  inhibition.103                                      dated to reliably detect minor segmental       than the surrounding collagen fibers.73,87
                                                                                                                  Clinical Presentation Patients with neck            instabilities in the cervical spine.35 Minor       Recently a computerized method to
                                                                                                                  pain seem to have a poor awareness of               segmental instabilities or segmental hyper-    measure accuracy of head and neck move-
                                                                                                                  their head-neck posture, and some in-               mobilities, therefore, remain an intensely     ment called “the Fly” was developed.74 It
                                                                                                                  deed complain about “a wobbling head,”75            controversial topic, as there is no con-       measures the patient’s ability to correct
                                                                                                                  which may be resultant of impaired cervi-           sensus about its precise definition.3,100,125   cervical spine movements on a moment-
                                                                                                                  cal position sense.                                 Nevertheless, early spinal degenerative        to-moment basis, while moving the head-
                                                                                                                  Clinical Assessment Cervical position               change has been recognized as a potential      neck. This method has demonstrated
                                                                                                                  sense can be assessed clinically by using a         physiological basis for minor segmental        impaired head-neck movement accuracy
                                                                                                                  laser pointer mounted onto a lightweight            instabilities,19 and, recently, segmental      in patients with a history of whiplash in-
                                                                                                                  headband. Patients are asked to focus on            hypermobility was demonstrated in the          jury when compared to controls.74
                                                                                                                  the natural resting head position for a few         lower cervical spine in some women with        Clinical Presentation Subjective com-
                                                                                                                  seconds, sitting 90 cm away from a wall.            chronic whiplash.76 In these individuals,      plaints of a painful stiff neck are often ac-
                                                                                                                  With the eyes closed, they actively move            management directed towards the sta-           companied by associated complaints like
                                                                                                                  the head and then try to come back to               bilizing musculature and optimal neuro-        “my neck movements feel jerky,” “intense
                                                                                                                  the resting position as accurately as pos-          muscular control of movement is thought        tiredness in the back of the neck,” and
                                                                                                                  sible. The difference between the starting          to be particularly important.                  “the head feels heavy.”75 Clinicians often
                                                                                                                  and resting position of the laser beam on               The importance of the deep stabiliz-       suspect these patients to have disturbed
                                                                                                                  the wall can be measured in centimeters             ing musculature of the neck for spinal         neck movement control as a consequence
                                                                                                                                                                    journal of orthopaedic & sports physical therapy | volume 39 | number 5 | may 2009 | 367
                                                                                                                                                          [   CLINICAL COMMENTARY                                             ]
                                                                                                                  of the aforementioned clinical research          the vestibular system, has the potential                dem stance position has also been seen
                                                                                                                  findings.                                         to disturb an intact vestibular subsys-                 in those with neck pain when compared
                                                                                                                  Clinical Assessment In the Fly,74 the            tem.32,55,93,95 This makes the patient—in               to asymptomatic individuals.31,90,135,138 Re-
                                                                                                                  patient sits in front of a computer with         this case a patient with neck pain and                  cently, it has been suggested that cervical
                                                                                                                  sensors on the head, which accurately            faulty neck mechanoreceptor input—less                  muscle fatigue may be an important con-
                                                                                                                  measure the positions and movements of           able to utilize internal vestibular orient-             tributing factor to altered postural stabil-
                                                                                                                  the head-neck in space. Two cursors are          ing information to resolve inaccurate in-               ity in those with neck pain.120 One study
                                                                                                                  visible on the computer screen: 1 cursor         formation from the somatosensory and                    has demonstrated a correlation between
                                                                                                                  is black, indicating the movements of the        visual subsystems.112 This is in accordance             fatty infiltration of the suboccipital mus-
                                                                                                                  head-neck, and the other cursor is blue,         with the “sensory mismatch” theory,                     cles and balance deficits,88 and further
                                                                                                                  derived from the Fly software program.           which holds that sensations of dizziness                research into this hypothesis is currently
                                                                                                                  At the very beginning of the test, both          and unsteadiness arise because of a con-                underway.
                                                                                                                  cursors match each other in the middle           flict between the converging input from                  Clinical Presentation Cervical induced
                                                                                                                  of the screen. Then the blue cursor starts       the different sensory subsystems and the                dizziness is characterized by subjective
                                                                                                                  to move, tracing slow and unpredictable          expected sensory patterns.10                            complaints of unsteadiness, insecurity,
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                  movement patterns of short duration.                Clinical research and experience indi-               and lightheadedness.58,64 Some patients
                                                                                                                  The patient is instructed to follow the Fly      cates that some patients with neck pain                 also complain about a feeling of spinning,
                                                                                                                  with the black cursor by moving the head-        do not seem to be aware that they have                  but this is more like a feeling of “spinning
                                                                                                                  neck as accurately as possible. The devia-       standing balance disturbances until their               in the head” rather than spinning of the
                                                                                                                  tion or amplitude accuracy between the           standing balance is challenged.11,74 A pos-             patient or the surroundings, as in typical
Copyright © 2009 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
                                                                                                                  2 cursors is continuously recorded dur-          sible explanation is that the symptoms                  vertigo of vestibular origin.58 Often cervi-
                                                                                                                  ing 3 randomly ordered test sequences.74         of cervicogenic dizziness may abate once                cal dizziness presents as a tipsy state as
                                                                                                                  The Fly method has recently been revised         the CNS has adapted to the altered neu-                 a consequence of “noise” in the postural
                                                                                                                  and can be used to grade the deficits of          rophysiological inputs, even though the                 control system and may be accompanied
                                                                                                                  movement control in patients with neck           underlying dysfunction remains.16 It is                 by nausea. It is rarely described as strong
                                                                                                                  pain much more accurately than the prior         hypothesized that the vestibular and the                attacks of dizziness or vertigo.136
                                                                                                                  Fly method, and, consequently, a treat-          somatosensory subsystems may compen-                        The subjective complaints are often
                                                                                                                  ment can be prescribed that starts at each       sate for the balance disturbances by in-                more pronounced early in the morn-
                                                                                                                  patient’s impairment level. Hitherto, the        creasing the muscle stiffness in the body               ing when the neck is stiff and late in the
Journal of Orthopaedic & Sports Physical Therapy®
                                                                                                                  laser method (as used for joint position         as a whole,11 which may also explain the                afternoon as the patient becomes tired.
                                                                                                                  sense) has been used by some therapists          unrelenting hyperactivity in the muscu-                 Quick movements of the cervical spine,
                                                                                                                  to trace an intricate pattern such as a          lature in some patients with neck pain.24               especially in the transverse plane but also
                                                                                                                  figure-of-eight placed on the wall 90 cm          This may serve as one explanation for                   in the sagittal plane, most commonly pro-
                                                                                                                  in front of the patient. A subjective clini-     why some patients with WAD develop                      voke these symptoms; but they may also
                                                                                                                  cal judgment can be made based on the            fibromyalgia.13,14 It is, therefore, impor-              occur when watching moving objects94 or
                                                                                                                  patient’s ability to trace the pattern ac-       tant to screen patients with neck pain for              walking in the dark.
                                                                                                                  curately and smoothly.                           balance disturbances, even in the absence               Clinical Assessment Karlberg et al65
                                                                                                                                                                   of subjective complaints about balance                  proposed a scientific method to measure
                                                                                                                  :_ijkhX[ZFeijkhWbIjWX_b_jo0:_pp_d[ii         problems.                                               cervical-related balance disturbances
                                                                                                                  WdZ%ehKdij[WZ_d[ii                                 Several studies have demonstrated dis-               in individuals with acute neck pain, but
                                                                                                                  Clinical Research Cervical induced bal-          turbed postural stability in patients with              this method has not yet been validated to
                                                                                                                  ance disturbances can be caused by sever-        neck pain,1,31,67,68,84,90,104,118,135,138 especially   measure more longstanding cervicogenic
                                                                                                                  al different pathophysiological processes,       in those with neck pain from whiplash                   balance disturbances where compensa-
                                                                                                                  including irritation of the sympathetic          injury and those complaining of dizzi-                  tory mechanisms might be present. A
                                                                                                                  vertebral plexus, vertebrobasilar insuf-         ness.31,135 Most of the research has been               clinical diagnosis of cervical-induced diz-
                                                                                                                  ficiency, and sensorimotor disturbanc-            conducted with respect to static stand-                 ziness and/or unsteadiness is, therefore,
                                                                                                                  es from the cervical spine structures.4          ing balance where an increase in postural               a diagnosis of exclusion of other possible
                                                                                                                  Emerging evidence draws attention to the         sway or rigidity is noted even in simple                causes.65 However, research suggests
                                                                                                                  last explanation.74,84,136,141 Altered sensory   tests of standing comfortably on a firm                  that balance disturbances in neck pain
                                                                                                                  input, especially mediated via the direct        surface with eyes closed. An increased                  present differently than those with a ves-
                                                                                                                  neurophysiological connections between           rate of failure to maintain stability for               tibular disorder, in whom balance distur-
                                                                                                                  the upper cervical spine structures and          30 seconds in the more challenging tan-                 bances appear to be easily noticeable on
                                                                                                                  368 | may 2009 | volume 39 | number 5 | journal of orthopaedic & sports physical therapy
                                                                                                                  difficult tests, such as narrow stance on          steps completed on and off a 7.5-cm step                 will have further implications for the con-
                                                                                                                  a foam surface, when compared to those             in 15 seconds for each limb.                             trol of neck posture and movement, and,
                                                                                                                  with whiplash, who showed more subtle                 Thus clinicians should consider such                  again, could contribute to a vicious cycle
                                                                                                                  deficits in all tests.65,137 At present, clini-     dynamic tests particularly for patients                  of altered cervical afferent input and al-
                                                                                                                  cal tests of postural stability are not use-       with neck pain complaining of dizziness,                 tered sensorimotor control.5
                                                                                                                  ful to differentiate between a vestibular          unsteadiness, or loss of balance. Norma-                     The smooth pursuit neck torsion test
                                                                                                                  or neck etiology of balance disturbances.          tive values for these tests are generally                developed by Tjell et al129 is considered
                                                                                                                  But, as mentioned, the clinical presen-            provided for elders (65-80 years of age;                 to be specific for detecting eye move-
                                                                                                                  tation of these 2 conditions is different.         DGI score, 21/24; timed 10-meter walk                    ment disturbances due to altered cervi-
                                                                                                                  Nevertheless, balance in comfortable               with head turns, 15 steps in 8 seconds;                  cal afferent input. This test measures the
                                                                                                                  and narrow stance with the eyes open               and the step test, 14-15 steps).63,104 How-              difference in smooth pursuit eye move-
                                                                                                                  and closed should be assessed with the             ever, a recent study looked at a younger                 ment control with the head and trunk in
                                                                                                                  patient standing on a firm surface then             group of subjects between 43 and 57                      a neutral position, compared to when the
                                                                                                                  a soft surface, such as a piece of 10-cm-          years of age.83 Normative values provid-                 trunk and neck are rotated relative to the
                                                                                                                  thick dense foam. Inability to maintain            ed in this study were a DGI score of 23                  stationary head.130 A decrease in velocity
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                  stance for 30 seconds, noticeably large            to 24, a timed 10-meter walk with head                   gain of smooth pursuit eye movements
                                                                                                                  increases in sway, slower responses to             turns of 15 steps in 8 seconds, and a step               when the head is in a relatively torsioned
                                                                                                                  correct sway, or rigidity to prevent sway          test of 21 steps.83 Further research into                (rotated) position, when compared to
                                                                                                                  are considered abnormal responses. The             younger subjects (less than 40 years of                  the neutral position, is only seen in those
                                                                                                                  patient’s ability to maintain tandem and           age) is required.                                        with neck pain (ie, not in those with ves-
Copyright © 2009 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
                                                                                                                  single-leg stance on a firm surface with                                                                     tibular or CNS disorders) and is most evi-
                                                                                                                  eyes open and closed for up to 30 seconds          EYkbecejeh:_ijkhXWdY[i                                  dent in those with whiplash and in those
                                                                                                                  can also be assessed; although care in in-         Clinical Research Deficits in oculomotor                  complaining of dizziness.129,130,134
                                                                                                                  terpretation of the results in these more          control, such as decreased smooth pur-                       Recently, a pilot trial of case studies
                                                                                                                  difficult tests is needed in older individu-       suit velocity gain, altered velocity and la-             of individuals with whiplash reporting
                                                                                                                  als, where the ability to maintain tandem          tency of saccadic eye movements, and an                  visual disturbances indicated deficits in
                                                                                                                  stance can be impaired in normal adults            increased gain of the cervico-ocular re-                 head-eye coordination when compared
                                                                                                                  above the age of 45 years.31,138                   flex have been seen in patients with neck                 to control subjects.40 Specifically, a de-
                                                                                                                      To date, little research has been con-         pain.38,47,53,70,91,124,129,130,134,141 In people with   creased range of head movement during
Journal of Orthopaedic & Sports Physical Therapy®
                                                                                                                  ducted to determine any changes to func-           vestibular disorders and in the elderly, an              gaze fixation, a decreased head velocity
                                                                                                                  tional or dynamic balance in individuals           increased gain of the cervico-ocular reflex               during tasks involving head-eye coordi-
                                                                                                                  with neck pain; however, disturbances              is considered a compensation response                    nation, and compensatory head move-
                                                                                                                  to the velocity and direction of gait and          to a decrease in vestibulo-ocular gain. 92               ments during isolated eye rotation were
                                                                                                                  running have been seen in response to              However, a compensatory decrease in                      noted that suggest disturbances in gaze
                                                                                                                  neck muscle vibration in asymptomatic              the vestibulo-ocular gain has not been                   stability and head-eye coordination in
                                                                                                                  control subjects,9,18 and, recently, older         seen in those with an increased cervico-                 some of those with whiplash.40
                                                                                                                  patients (65-80 years of age) with neck            ocular gain secondary to whiplash, and                   Clinical Presentation Patients with neck
                                                                                                                  pain demonstrated significant differ-               this imbalance between the reflexes has                   pain sometimes complain about symp-
                                                                                                                  ences in the dynamic gait index (DGI),             been suggested as a potential cause of                   toms relating to the visual system such
                                                                                                                  timed 10-meter walk with head turns,               disturbances to the visual system.92 There               as blurred vision, reduced visual field,
                                                                                                                  and the step test, when compared to                is also some evidence that eye movement                  grey spots appearing in the visual field,
                                                                                                                  elders without neck pain.63,104 The DGI            dysfunction may be associated with a                     temporary blinding, photophobia, and
                                                                                                                  rates the control of 8 functional mobil-           poorer prognosis in those with a whiplash                disordered fusion.57,143 These visual dis-
                                                                                                                  ity tasks that include walking at comfort-         injury.52,53 Altered cervical somatosensory              turbances may explain reading problems
                                                                                                                  able and changing speeds, walking with             input is thought to adversely influence eye               reported by some patients with neck
                                                                                                                  horizontal and vertical head movements,            movement control. Further, there is also                 pain.37 Diplopia, which is common in pa-
                                                                                                                  walking, pivot turning, stepping over              some evidence that normal reflexive neck                  tients with vertebrobasilar insufficiency,
                                                                                                                  and around an object, and walking up               muscle activity seen during eye move-                    is rare in somatic neck dysfunctions. If
                                                                                                                  and down stairs.144 The timed 10-meter             ments in individuals without neck pain                   patients with neck pain report double
                                                                                                                  walk with head turns48 measures the time           is altered with respect to timing in those               vision, it is most often not true diplopia
                                                                                                                  and number of steps taken to complete              with neck pain.5 Abnormal neck muscle                    but rather the contours of an object that
                                                                                                                  the task.8 The step test54 is the number of        activity associated with eye movement                    become unclear.57
                                                                                                                                                                   journal of orthopaedic & sports physical therapy | volume 39 | number 5 | may 2009 | 369
                                                                                                                                                        [   CLINICAL COMMENTARY                                   ]
                                                                                                                  Clinical Assessment While we are just          the patient having the available rotation     between the cervical somatosensory, ves-
                                                                                                                  starting to develop clinical assessment        range of motion and ability to perform        tibular, and visual systems, and second-
                                                                                                                  methods, it is currently suggested that        the task accurately when not fixating the      ary adaptive changes in the sensorimotor
                                                                                                                  the clinical examination of oculomotor         patient’s gaze, patients with neck pain       control system need also to be consid-
                                                                                                                  control in those with neck pain should         often40 are unable to keep focus or move      ered. This is of the utmost importance to
                                                                                                                  include a qualitative analysis of eye follow   the head as far or as quickly or smoothly     understand for the optimal management
                                                                                                                  (smooth pursuit) while keeping the head        as asymptomatic individuals (45°). They       of patients with neck pain, as secondary
                                                                                                                  still (comparing neck neutral to neck tor-     may also deviate into cervical lateral flex-   disturbances in the vestibular and visual
                                                                                                                  sion), head movement while maintaining         ion. Reproduction of dizziness and/or         systems can occur via plasticity in the
                                                                                                                  focus on an object (gaze stability), head      blurred vision may occur. This is similar     CNS.115 Therefore, a combined approach
                                                                                                                  and eye movement coordination, and             to the dynamic visual acuity test used for    is likely to best address the perpetuation
                                                                                                                  quick movements of the eyes to refocus         those with vestibular disorders; however,     of a vicious cycle of events where second-
                                                                                                                  (saccades).                                    head movement is performed actively and       ary adaptive changes in the sensorimotor
                                                                                                                      Clinical assessment of eye movement        slowly rather than passively and quickly.     control system could lead to altered cervi-
                                                                                                                  in those with neck pain can be conducted       This approach is better suited to cervical-   cal muscle function and joint mechanics
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                  by assessing the quality of eye movements      related gaze disorders, as the cervical af-   further altering cervical afferent input.
                                                                                                                  and eye movement control, as well as any       ferents are stimulated at lower movement
                                                                                                                  reproduction of symptoms during the            frequencies compared to fast movements        7ZZh[ii_d]7bj[h[Z9[hl_YWb7÷[h[dj
                                                                                                                  tests described below. Such tests are not      that stimulate the vestibular afferents.49    ?dfkj
                                                                                                                  exclusive to, nor can specifically differen-        Saccadic Eye Movement The patient         Physical therapy interventions such as
Copyright © 2009 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
                                                                                                                  tiate, those with cervical disorders and       quickly moves the eyes to fix his/her gaze     pain management, manipulative therapy,
                                                                                                                  are often used in those with vestibular or     between several targets. The targets are      active range-of-motion exercises, and ex-
                                                                                                                  CNS disorders; although some tests have        placed in several different movement          ercises to improve neuromuscular control
                                                                                                                  been modified in an attempt to bias a cer-      directions. Inability to fixate on target,     will all be important in reducing possible
                                                                                                                  vical component to the testing.                overshooting the target, and taking more      causes of altered afferent cervical input
                                                                                                                      Smooth Pursuit The patient is asked        than 2 eye movements to reach the tar-        and subsequent disturbances to senso-
                                                                                                                  to accurately and smoothly follow a            get might indicate a poor performance.        rimotor control. Some physical interven-
                                                                                                                  slow-moving target with his/her eyes,          Again reproduction of dizziness and or        tions have been shown to improve aspects
                                                                                                                  while keeping the head still. The target is    blurred vision may also occur.                of sensorimotor deficits. For example,
Journal of Orthopaedic & Sports Physical Therapy®
                                                                                                                  moved from side to side. Quick saccadic            Eye-Head Coordination The patient         manipulative therapy has been shown
                                                                                                                  eye movements to catch up to the target        first moves the eyes to a point to focus       to improve joint position sense and diz-
                                                                                                                  rather than smooth eye movement, espe-         and then, while maintaining focus, moves      ziness46,99,105,106; specific neuromuscular
                                                                                                                  cially during midrange eye movement,           the head to that point. This can be per-      control training60 has improved cervi-
                                                                                                                  are an indication of impairment in the         formed to the left and right, and up and      cal position sense; and cervical muscle
                                                                                                                  task.134 Reproduction of dizziness and         down. Asymptomatic individuals are able       endurance training has been suggested
                                                                                                                  blurred vision may also occur. Deteriora-      to perform isolated eye and head move-        to improve balance.120 Acupuncture has
                                                                                                                  tion of eye follow (increase in catch-up       ments and maintain focus. Often, pa-          also been demonstrated to improve cer-
                                                                                                                  saccades), when the patient’s trunk is         tients with neck pain are unable to keep      vical joint position sense, vertigo,46 and
                                                                                                                  subsequently turned to 45° (in either di-      their head still while their eyes move or     standing balance. 30 However, clinical
                                                                                                                  rection), while the head is kept still, sug-   lose focus during the head movements.40       experience suggests that this alone may
                                                                                                                  gests a cervical afferent component to the     Eye and head movements to follow a            not be sufficient nor the most efficient
                                                                                                                  deficits as seen on the smooth-pursuit          trunk or an arm movement can also be          way of addressing all of the sensorimotor
                                                                                                                  neck torsion test.129 If a poor performance    assessed.                                     deficits.56
                                                                                                                  is noted when the head is in neutral, and
                                                                                                                  is unchanged by adding neck torsion by         9B?D?97BC7D7=;C;DJ                           7ZZh[ii_d]I[YedZWho7ZWfj_l[9^Wd][i
                                                                                                                  rotating the trunk 45°, this would imply                                                     _dj^[I[dieh_cejeh9edjhebIoij[c
                                                                                                                  a CNS disorder.                                                                              Addressing any secondary effects on the
                                                                                                                                                                 E
                                                                                                                                                                       vidence to date would suggest
                                                                                                                      Gaze Stability The patient is asked to           that management of disturbed sen-       visual and vestibular systems will also be
                                                                                                                  focus on a point directly in front of him/           sorimotor control due to cervical so-   important in the management of senso-
                                                                                                                  her and maintain visual focus as the pa-       matosensory dysfunction might need to         rimotor control disturbances in those with
                                                                                                                  tient actively moves the head into rota-       address the local causes of abnormal cer-     neck pain.33,51 This is where a tailored ap-
                                                                                                                  tion and flexion and extension. Despite         vical afferent input. The important links     proach to sensorimotor control becomes
                                                                                                                  370 | may 2009 | volume 39 | number 5 | journal of orthopaedic & sports physical therapy
                                                                                                                  important. There is evidence that specific                           coordination, and gaze stability60,108,124                        improved neck pain and disability and
                                                                                                                  treatment programs that have trained                                have resulted in improvements not only                            range of motion.108 Recently, a vestibular
                                                                                                                  cervical joint position sense, eye-neck                             in sensorimotor impairments but also                              rehabilitation program improved balance
                                                                                                                                                                                                                                                        and dizziness in patients with whiplash
                                                                                                                                                           Example Exercise Program for                                                                 injury.44 Again, it is unknown whether
                                                                                                                         J78B;'                                                                                                                        such an approach provided in isolation is
                                                                                                                                                        Cervicogenic Dizziness/Unsteadiness 97
                                                                                                                                                                                                                                                        able to address all of the deficits or is the
                                                                                                                   1. Oculomotor exercises standing on an unstable surface (foam)                                                                       most efficient approach.
                                                                                                                     ;o[cel[c[djim_j^j^[^[WZijWj_edWho"j^[fWj_[djcel[ij^[[o[iX[jm[[d(XbWYaZeji"'cWfWhj"edj^[mWbb
                                                                                                                     J^[[o[i\ebbemWjWh][jcel_d]i_Z[jei_Z[WdZkfWdZZemd"m_j^j^[^[WZijWj_edWho                                          ?dYehfehWj_d]CWdkWbJ^[hWfo%
                                                                                                                   ($ ;o[#d[YaYeehZ_dWj_ed[n[hY_i[iijWdZ_d]edWdkdijWXb[ikh\WY[\eWc                                                           ;n[hY_i[iWdZJW_beh[ZI[dieh_cejeh
                                                                                                                                                                                                                                                        9edjheb7ffheWY^[i
                                                                                                                     J^[fWj_[djcel[ij^[[o[iÓhijjeWjWh][jWdZj^[dj^[^[WZ"[dikh_d]j^[[o[iWh[a[fj\eYki[Zedj^[jWh][j$
                                                                                                                        The movements are rotations to the left and right, respectively                                                                 Intertwining manual therapy/exercises
                                                                                                                     J^[fWj_[djÓn[ij^[]Wp[edWXbWYaZejedj^[mWbb"Wj'cZ_ijWdY["WdZcel[ij^[^[WZ_dj^[jhWdil[hi[fbWd[              approaches with tailored sensorimotor
                                                                                                                        (rotation left and right) and in the sagittal plane (up and down)                                                               control programs would seem an ap-
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                                                                                  journal of orthopaedic & sports physical therapy | volume 39 | number 5 | may 2009 | 371
                                                                                                                                                                    [      CLINICAL COMMENTARY                                                       ]
                                                                                                                                                                                                                                                  of different exercises are required. Exer-
                                                                                                                                                       Examples of Tasks and Progressions
                                                                                                                                                                                                                                                  cises should be performed at a speed and
                                                                                                                         J78B;)                        to Improve Sensorimotor Control
                                                                                                                                                                                                                                                  range of movement that allow the patient
                                                                                                                                                               in Neck Disorders
                                                                                                                                                                                                                                                  to perform with precision and continuous
                                                                                                                   7_c                 JWia                                         Fhe]h[ii_ed                                                   correction, gradually increasing speed
                                                                                                                   Cervical position   With laser on headband for feedback,          ;o[iYbei[Z"Y^[Ya[o[ief[d                              and range as able. Exercises should also
                                                                                                                     sense                relocate back to neutral head posi-        H[beYWj[jefe_dji_dhWd][fbWY[ZedmWbb"[o[i       be performed in a position where preci-
                                                                                                                                          tion from all head movements with             closed, check eyes open
                                                                                                                                          eyes open                                  ?dYh[Wi[if[[Z
                                                                                                                                                                                                                                                  sion is paramount, progressing to more
                                                                                                                                                                                     F[h\ehc_dijWdZ_d]                                       difficult positions, such as tandem stance,
                                                                                                                                                                                     F[h\ehcedkdijWXb[ikh\WY[                               on soft surface, etc.
                                                                                                                   Cervical movement   With laser mounted on headband                ?dYh[Wi[if[[Z                                                The observed individuality in senso-
                                                                                                                     sense                practice tracing over a pattern placed     Ceh[Z_øYkbjWdZ_djh_YWj[fWjj[hd
                                                                                                                                          on the wall, eyes open                     IcWbbÓd[hcel[c[dji
                                                                                                                                                                                                                                                  rimotor disturbances in patients with
                                                                                                                                                                                                                                                  neck pain suggests that it may be im-
                                                                                                                   Eye follow          Sitting in a neutral neck position,           I_jm_j^d[Ya_dh[bWj_l[d[Yajehi_edfei_j_ed
                                                                                                                                           keeping the head still and the hands      ;o[ikfWdZZemd">fWjj[hd                               portant to develop specific rehabilitation
                                                                                                                                           in the laps. Moving the laser light       ?dYh[Wi[if[[Z                                            programs for specific dysfunctions and to
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                                         therapist passively moves the                   check if gaze was maintained                             neck pain to another.71 Good skills in
                                                                                                                                         patients trunk and/or the head/neck         9^Wd][j^[XWYa]hekdZe\j^[jWh][j"fbW_d"ijh_f[i"
                                                                                                                                       Maintain gaze on a dot placed on the             checks                                                    clinical examination and clinical reason-
                                                                                                                                         wall or ceiling as patient actively         9^Wd][\eYkife_djjemehZiehWXki_d[iiYWhZ            ing are, therefore, mandatory for effective
                                                                                                                                         moves the head/neck in all directions       ?dYh[Wi[if[[Z
                                                                                                                                                                                     ?dYh[Wi[hWd][e\cej_ed
                                                                                                                                                                                                                                                  management.
                                                                                                                                                                                     Fhe]h[ii\hecbo_d]jei_jj_d]jeijWdZ_d]
                                                                                                                                                                                     F[h\ehcedkdijWXb[ikh\WY[                               If[Y_ÓY;n[hY_i[i\ehKi[_dj^[JW_beh[Z
                                                                                                                   Eye-head            Move eyes to a new focus point and            7Yj_l[bocel[^[WZWdZ[o[ije][j^[hiWc[Z_h[Yj_ed       I[dieh_cejehFhe]hWc
                                                                                                                      coordination       then move head in the same direc-           Cel[[o[ied[Z_h[Yj_edWdZ^[WZeffei_j[Z_h[Yj_ed
                                                                                                                                         tion and return to neutral                  Cel[[o[iWdZ^[WZje][j^[hm^[df[h_f^[hWbl_i_ed      Neck Proprioception New advances in
                                                                                                                                                                                        restricted                                                physical therapy indicate that principles
Journal of Orthopaedic & Sports Physical Therapy®
                                                                                                                  372 | may 2009 | volume 39 | number 5 | journal of orthopaedic & sports physical therapy
                                                                                                                  task. The task can be progressed by ask-        The oculomotor exercises performed
                                                                                                                  ing the patient to relocate the head posi-      while moving the head can be imple-
                                                                                                                  tion to different points throughout the         mented at the same time as retraining
                                                                                                                  range of motion (eg, left rotation 20°,         cervical movement sense. Patients with
                                                                                                                  40°, and 60°) rather than the neutral           severe neck pain may benefit by start-
                                                                                                                  head position. Performing these activi-         ing the treatment regime by just moving
                                                                                                                  ties in more challenging standing posi-         the eyes with the head stationary so as to
                                                                                                                  tions can also be used as a progression         avoid symptom exacerbation.
                                                                                                                  for the exercises.                                  Smooth pursuit can be practiced by
                                                                                                                      Cervical movement sense can be im-          following a moving target with the eyes as
                                                                                                                  proved by moving the head, thus mov-            accurately as possible, while keeping the
                                                                                                                  ing the laser, to trace patterns placed on      head still. Performing this task in neck
                                                                                                                  a wall such as a figure-of-eight pattern.        torsion positions will also be important
                                                                                                                  Patients can practice performing the            to bias the cervical influence on the eyes.
                                                                                                                                                                                                                  <?=KH;($The balance exercises are combined with
                                                                                                                  task as accurately as possible, keeping             Gaze stability can be practiced by fo-
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                  accurately as possible.                         cus point. The patient can also move the        This is important, as patients with neck
                                                                                                                      More sophisticated computerized ver-        trunk, or the therapist can passively move      pain may react with compensatory in-
                                                                                                                  sions of retraining of neck propriocep-         the trunk, while the patient maintains fo-      creased muscle activity in the neck and
                                                                                                                  tion, both position sense and movement          cus on the point ahead. These tasks can be      other regions to achieve stabilization.
                                                                                                                  sense, are currently being developed and        progressed by altering the focus point (a       This is ordinarly not a problem for pa-
                                                                                                                  designed to enhance treatment progres-          word or group of words, such as a business      tients with dizziness of noncervical ori-
                                                                                                                  sion, with graduated levels of difficulty       card), the background behind the focus          gins; but for the patient with neck pain,
                                                                                                                  built into the programs. The training of        point (stripes or checks), the speed and        such training may be harmful, as it leads
                                                                                                                  neck position sense is aimed at better          range of the movement, restricting the pe-      to augmented neck muscle tension in al-
Journal of Orthopaedic & Sports Physical Therapy®
                                                                                                                  perception of body posture, dissociation        ripheral vision (wearing goggles blackened      ready tensed neck muscles and a vicious
                                                                                                                  between body parts, and better aware-           out at the sides), and/or by altering the po-   circle of increased muscle activity and
                                                                                                                  ness of the body’s position in space, es-       sition the patient is in to perform the task    pain and altered cervical afferent input
                                                                                                                  pecially improvement of the patients’           (eg, standing instead of sitting).              may develop, further exacerbating the
                                                                                                                  awareness of the head-neck and shoul-               Eye-head coordination can be prac-          cervicogenic dizziness.128
                                                                                                                  der girdle posture, and is dependent on         ticed as it is assessed, with attention to          Attempts at sustaining static stand-
                                                                                                                  proprioceptive, visual, auditory, and ves-      correctly isolate eye and head movement         ing balance for up to 30 seconds can be
                                                                                                                  tibular cues. In the training of movement       and perform accurate cervical move-             practiced according to the extent of im-
                                                                                                                  sense by the new Fly Exercise Program           ment. These tasks can be progressed by          pairment found on the initial assessment.
                                                                                                                  the patient begins to use additional de-        using the eyes to follow arm and trunk          Progressions can be made by altering the
                                                                                                                  grees of freedom by moving the cervical         movements. Saccades can be practiced by         stance position, closing the eyes, and/or
                                                                                                                  spine in larger ranges of movements and         quickly moving the eyes from one point          altering the support surface, such as us-
                                                                                                                  performing unpredictable, incrementally         to another and refocusing. Again, these         ing a soft surface or an unstable surface
                                                                                                                  difficult movement patterns at different        tasks can be progressed by altering the         such as a wobble board.
                                                                                                                  velocities.                                     speed and range of the movement, re-                Functional and more dynamic tasks,
                                                                                                                  Oculomotor Tasks Exercises to improve           stricting the peripheral vision (wearing        such as walking with head turns to the
                                                                                                                  oculomotor control can be divided into          goggles blackened-out at the sides), and/       left and right or up and down while
                                                                                                                  exercises performed with the head sta-          or by altering the position the patient is      maintaining the direction and velocity
                                                                                                                  tionary and while the head is moving.           in to perform the task (eg, standing in-        of walking, can also be incorporated de-
                                                                                                                  The exercises with the head stationary          stead of sitting).                              pending on the level of impairment. This
                                                                                                                  can be implemented at the same time as          Postural Stability Generally, dizziness         can be progressed by varying the walking
                                                                                                                  the exercises for improving head-neck           is provoked with balance training. How-         surface and speed of the activity, as well
                                                                                                                  awareness and cervical position sense.          ever, care and slow progression without         as the walking task (J78B;'"<?=KH;(.
                                                                                                                                                                journal of orthopaedic & sports physical therapy | volume 39 | number 5 | may 2009 | 373
                                                                                                                                                                                         [     CLINICAL COMMENTARY                                                  ]
                                                                                                                                                                                                                                                                 especially important for patients with
                                                                                                                                                                                                               Postural stability-balance training               neck pain, as their aforementioned subtle
                                                                                                                                                                                                      General balance exercises/specific balance exercises        impairments may not be readily detected
                                                                                                                                                                                                                                          Integrating:           by clinical examination alone. It is impor-
                                                                                                                                                                                           Movement control exercises             Exercises for position sense   tant for clinicians to monitor the status
                                                                                                                                                                                                                                  Oculomotor exercises
                                                                                                                                                                                             With increasing complexity                                          of a patient with neck pain by objective
                                                                                                                     Progressive Interaction
                                                                                                                                                       Physical therapy/exercises including postural corrections and dissociation between body parts
                                                                                                                                                                                                                                                                                    H;<;H;D9;I
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                                               Start                                    Number of treatment sessions                                     End       '$ Alund M, Ledin T, Odkvist L, Larsson SE. Dy-
                                                                                                                                                                                                                                                                         namic posturography among patients with
                                                                                                                   <?=KH;)$Suggested treatment planning showing progressive interaction of treatment interventions.                                                    common neck disorders. A study of 15 cases
                                                                                                                                                                                                                                                                         with suspected cervical vertigo. J Vestib Res.
                                                                                                                                                                                                                                                                         1993;3:383-389.
                                                                                                                        <?=KH;) provides a suggestion for the                                       lenged. The training of position sense, oc-
                                                                                                                                                                                                                                                                   ($ Anderson G. Epidemiology of spinal disorders.
Copyright © 2009 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
                                                                                                                  treatment planning for a patient with                                              ulomotor control, and movement sense                                In: Frymoyer J, ed. The Adult Spine. New York,
                                                                                                                  neck pain who, at the same time, has all                                           is integrated into the balance exercise                             NY: Raven Press; 1991:107-146.
                                                                                                                  the sensorimotor impairments that can                                              program to enhance modulation of the                          )$ Ashton-Miller J, Schultz A. Spine instability and
                                                                                                                                                                                                                                                                         segmental hypermobility biomechanics: a call
                                                                                                                  possibly be of cervicogenic origin. Physical                                       sensorimotor circuits in the CNS and to
                                                                                                                                                                                                                                                                         for definition and standard use of terms. Semin
                                                                                                                  therapy/exercises are performed through-                                           make the balance exercises progressively                            Spine Surg. 1991;3:136-148.
                                                                                                                  out the management to make favorable                                               more difficult.                                               *$8Wbe^H">WbcW]o_=$Disorders of the Vestibular
                                                                                                                  conditions for the sensorimotor training                                                                                                               System. New York, NY: Oxford University Press;
                                                                                                                  and to treat any compensatory reactions                                            <KJKH;:?H;9J?EDI                                                   1996.
                                                                                                                                                                                                                                                                   +$8[nWdZ[h9I"C[bbehH">eZ][iFM$;÷[Yje\
                                                                                                                  that may prevail after the sensorimotor                                                                                                                gaze direction on neck muscle activity during
Journal of Orthopaedic & Sports Physical Therapy®
                                                                                                                                                                                                     A
                                                                                                                                                                                                            lmost all research on assess-                                cervical rotation. Exp Brain Res. (&&+1',-0*((#
                                                                                                                  head-neck awareness, which requires                                                       ment and management of senso-                                *)($^jjf0%%Zn$Ze_$eh]%'&$'&&-%i&&(('#&&+#
                                                                                                                                                                                                                                                                         0048-4
                                                                                                                  normal range of motion, and oculomotor                                                    rimotor dysfunctions, including
                                                                                                                                                                                                                                                                   ,$ Björklund M. Effects of Repetitive Work on
                                                                                                                  disturbances are then addressed before                                             cervicogenic dizziness, has been aimed at                           Proprioception and of Stretching on Sensory
                                                                                                                  training of disturbed neck movement                                                patients with specific dysfunctions. In the                          Mechanisms: Implications for Work-Related
                                                                                                                  control. Normal oculomotor control is re-                                          clinical setting, pragmatic multimodal                              Neuromuscular Disorders [dissertation]. Umeå,
                                                                                                                                                                                                                                                                         Im[[Z[d0Kc[Kd_l[hi_jo1(&&*$
                                                                                                                  quired before training of disturbed neck                                           intervention approaches, including sen-
                                                                                                                                                                                                                                                                   -$ Bogduk N, Mercer S. Biomechanics of the cervi-
                                                                                                                  movement control, as the patient has to be                                         sorimotor training, will likely be needed                           cal spine. I: Normal kinematics. Clin Biomech
                                                                                                                  able to follow the target (the Fly) by mov-                                        to address the heterogeneity of presenta-                           (Bristol, Avon). (&&&1'+0,))#,*.$
                                                                                                                  ing the head, using vision to appreciate                                           tion of patients with neck pain; but there                    .$ Bohannon RW. Comfortable and maximum
                                                                                                                                                                                                                                                                         mWba_d]if[[Ze\WZkbjiW][Z(&#-/o[Whi0
                                                                                                                  the relative movements between the target                                          is currently only a limited but growing
                                                                                                                                                                                                                                                                         reference values and determinants. Age Ageing.
                                                                                                                  (the Fly) and the cursor on the head, which                                        amount of research on such an approach.                             '//-1(,0'+#'/$
                                                                                                                  follows the Fly on the computer screen.                                            Given that such pragmatic multimodal                          /$ Bove M, Courtine G, Schieppati M. Neck
                                                                                                                  The same applies if a laser pointer is used                                        research will be conducted in academia,                             muscle vibration and spatial orientation during
                                                                                                                                                                                                                                                                         stepping in place in humans. J Neurophysiol.
                                                                                                                  to treat disturbed neck movement control.                                          there is a need to bridge the gap between
                                                                                                                                                                                                                                                                         (&&(1..0(()(#((*'$^jjf0%%Zn$Ze_$eh]%'&$''+(%
                                                                                                                  Disturbed postural stability—dizziness                                             the theoretical body of knowledge about                             `d$&&'/.$(&&(
                                                                                                                  and/or unsteadiness, which may improve                                             neck pain and the practical utilization of                   '&$ Brandt T. Vertigo: Its Multisensory Syndromes.
                                                                                                                  by implementing the aforementioned ap-                                             that knowledge. There is, for example, a                            1st ed. London, UK: Springer-Verlag; 1991.
                                                                                                                                                                                                                                                                  ''$8hdijhc>"CWbc]h[d#Ebiied;"8[hd[aem#
                                                                                                                  proaches first, is addressed at a later stage                                       lack of simple measurement devices in
                                                                                                                                                                                                                                                                         Bergkvist M. Balance performance in patients
                                                                                                                  to minimize the commonly observed re-                                              the clinical setting that can accurately and                        with whiplas associated disorders and patients
                                                                                                                  actions of compensatory increased muscle                                           reliably measure disturbances of postural                           with prolonged musculoskeletal disorders. Ad-
                                                                                                                  activity in the neck and other regions to                                          stability, cervical position and movement                           vances in Physiother. (&&'1)0'(&#'(-$
                                                                                                                                                                                                                                                                  '($8h_iedH@">Whjb_d]B"F_Ya[jjM$7fheif[Yj_l[
                                                                                                                  achieve stabilization when balance is chal-                                        sense, and oculomotor function. This is
                                                                                                                  374 | may 2009 | volume 39 | number 5 | journal of orthopaedic & sports physical therapy
                                                                                                                         study of acceleration-extension injuries follow-       (-$<WbbW:"@kbb=">eZ][iFM$<[[Z\ehmWhZWYj_l_jo            1986;64:59-69.
                                                                                                                         ing rear-end motor vehicle collisions. J Musculo-             e\j^[Y[hl_YWbÔ[nehckiYb[iZkh_d]lebkdjWho       *)$ Guyton AC. Textbook of Medical Physiology. 8th
                                                                                                                         skeletal Pain. (&&&1.0/-#'')$                                 arm movements is delayed in chronic neck pain.               ed. Philadelphia, PA: W.B. Saunders Company;
                                                                                                                  ')$ Buskila D, Neumann L. The development of                        Exp Brain Res. (&&*1'+-0*)#*.$^jjf0%%Zn$Ze_$                1991.
                                                                                                                         widespread pain after injuries. J Musculoskeletal             eh]%'&$'&&-%i&&(('#&&)#'.'*#/                         **$>Wdiied;;"CWdiiedDE"H_d]iX[h]
                                                                                                                         Pain. (&&(1'&0(,'#(,-$                                 (.$ Falla DL. Unravelling the complexity of muscle                 A7">WaWdiied7$:_pp_d[iiWced]fW-
                                                                                                                  '*$ Buskila D, Neumann L, Vaisberg G, Alkalay D,                    impairment in chronic neck pain. Man Ther.                   tients with whiplash-associated disorder:
                                                                                                                         Wolfe F. Increased rates of fibromyalgia follow-               (&&*1/0'(+#'))$                                              a randomized controlled trial. J Rehabil
                                                                                                                         ing cervical spine injury. A controlled study of       (/$ Falla DL, Jull G, Dall’Alba P, Rainoldi A, Merletti            Med. (&&,1).0).-#)/&$^jjf0%%Zn$Ze_$
                                                                                                                         161 cases of traumatic injury. Arthritis Rheum.               R. An electromyographic analysis of the deep                 eh]%'&$'&.&%',+&'/-&,&&-,.//(
                                                                                                                         '//-1*&0**,#*+($                                              Y[hl_YWbÔ[nehckiYb[i_df[h\ehcWdY[e\YhWd-        *+$>[_aa_bW>"7ijhecF=$9[hl_YeY[f^Wb_Ya_d[i-
                                                                                                                  '+$ Cholewicki J, Panjabi MM, Khachatryan A.                        _eY[hl_YWbÔ[n_ed$Phys Ther. (&&)1.)0.//#/&,$               thetic sensibility in patients with whiplash injury.
                                                                                                                         IjWX_b_p_d]\kdYj_ede\jhkdaÔ[neh#[nj[dieh          )&$ Fattori B, Borsari C, Vannucci G, et al. Acupunc-              Scand J Rehabil Med.'//,1(.0'))#').$
                                                                                                                         muscles around a neutral spine posture. Spine.                ture treatment for balance disorders following        *,$>[_aa_bW>"@e^WdiiedC"M[dd]h[d8?$;÷[Yji
                                                                                                                         '//-1((0((&-#(('($                                            whiplash injury. Acupunct Electrother Res.                   of acupuncture, cervical manipulation and
                                                                                                                  ',$9b[dZWd_[bH$9[hl_YWbL[hj_]e$?d0>[hZcWdI"               '//,1('0(&-#('-$                                             NSAID therapy on dizziness and impaired head
                                                                                                                         ed. Vestibular Rehabilitation. Philadelphia, PA:       )'$ Field S, Treleaven J, Jull G. Standing balance: a              repositioning of suspected cervical origin: a
                                                                                                                         <$7$:Wl_i9e1(&&&0*/*#+&/$                                  comparison between idiopathic and whiplash-                  pilot study. Man Ther. (&&&1+0'+'#'+-$^jjf0%%
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                   '-$ Corneil BD, Olivier E, Munoz DP. Neck muscle                   induced neck pain. Man Ther. (&&.1')0'.)#'/'$               Zn$Ze_$eh]%'&$'&+*%cWj^$(&&&$&)+-
                                                                                                                         responses to stimulation of monkey superior                   ^jjf0%%Zn$Ze_$eh]%'&$'&',%`$cWj^$(&&,$'($&&+          *-$>[_aa_bW>L"M[dd]h[d8?$9[hl_YeY[f^Wb_Y
                                                                                                                         colliculus. I. Topography and manipulation             )($<_iY^[h7@">ko][dFB"<eb][h_d]>J"L[h^W][d               kinesthetic sensibility, active range of cervical
                                                                                                                         of stimulation parameters. J Neurophysiol.                    WI, Theunissen EJ. Vestibular hyperreactivity                motion, and oculomotor function in patients
                                                                                                                         (&&(1..0'/.&#'///$                                            and hyperventilation after whiplash injury. J                with whiplash injury. Arch Phys Med Rehabil.
                                                                                                                  '.$ Courtine G, Papaxanthis C, Laroche D, Pozzo                     Neurol Sci. '//+1')(0)+#*)$                                  1998;79:1089-1094.
                                                                                                                         T. Gait-dependent integration of neck muscle           ))$<_iY^[h7@"L[h^W][dM?">ko][dFB$M^_fbWi^         *.$>[hZcWdI$Vestibular Rehabilitation. (dZ[Z$
                                                                                                                         afferent input. Neuroreport$(&&)1'*0(),+#
Copyright © 2009 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
                                                                                                                         muscle isometric contractions. Exp Brain Res.                 terjoint coordination. Can J Physiol Pharmacol.              '/-)1'.0+'(#+)&$
                                                                                                                         (&&*1'+.0+.#,,$^jjf0%%Zn$Ze_$eh]%'&$'&&-%                    '//+1-)0(-)#(.*$                                      +($>_bZ_d]iied9"JeebWd[d=$EkjYec[W\j[hie\j#
                                                                                                                         i&&(('#&&*#'.-'#.                                      )-$ Gimse R, Bjorgen IA, Tjell C, Tyssedal JS, Bo K.               tissue injury of the cervical spine. A prospective
                                                                                                                  (($ Dutia MB. The muscles and joints of the neck:                   Reduced cognitive functions in a group of whip-              study of 93 car-accident victims. Acta Orthop
                                                                                                                         their specialisation and role in head movement.               lash patients with demonstrated disturbances in              Scand. 1990;61:357-359.
                                                                                                                         Prog Neurobiol. 1991;37:165-178.                              the posture control system. J Clin Exp Neurop-        +)$>_bZ_d]iied9"M[dd]h[d8?"8h_d]="JeebWd[d
                                                                                                                  ()$ Edney DP, Porter JD. Neck muscle afferent                       sychol. 1997;19:838-849.                                     G. Oculomotor problems after cervical spine
                                                                                                                         projections to the brainstem of the monkey:            ).$ Gimse R, Tjell C, Bjorgen IA, Saunte C. Dis-                   injury. Acta Orthop Scand. 1989;60:513-516.
                                                                                                                         implications for the neural control of gaze. J                turbed eye movements after whiplash due to            +*$>_bbA"8[hd^WhZj@"CY=Wdd7"CWbj[i[:"
                                                                                                                         Comp Neurol. '/.,1(+&0)./#)/.$^jjf0%%Zn$Ze_$                 injuries to the posture control system. J Clin Exp           Berkovits D. A new test of dynamic standing
                                                                                                                         eh]%'&$'&&(%Yd[$/&(+&&)''                                     Neuropsychol. 1996;18:178-186.                               balance for stroke patients: reliability, validity
                                                                                                                  (*$ Elert J, Kendall SA, Larsson B, Mansson B,               )/$=eii[b_d="HWiiekb_Wd>"8hemd?$;\-                       and comparison with healthy elderly. Physiother
                                                                                                                         Gerdle B. Chronic pain and difficulty in relaxing             fects of neck extensor muscles fatigue                       Can. '//,1*.0(+-#(,($
                                                                                                                         postural muscles in patients with fibromyalgia                 on balance. Clin Biomech (Bristol, Avon).             ++$>_dea_C$L[hj_]eZk[jem^_fbWi^_d`kho0Wd[k-
                                                                                                                         and chronic whiplash associated disorders. J                  (&&*1'/0*-)#*-/$^jjf0%%Zn$Ze_$eh]%'&$'&',%`$                rotological approach. Acta Otolaryngol Suppl.
                                                                                                                         H^[kcWjeb$(&&'1(.0'),'#'),.$                                 Yb_dX_ec[Y^$(&&*$&($&&'                                      '/.*1*'/0/#(/$
                                                                                                                  (+$ Elliott J, Jull G, Noteboom JT, Darnell R, Gal-          *&$=h_f>"@kbb="Jh[b[Wl[d@$>[WZ[o[Ye#ehZ_dW-      +,$>ehWa<"CWYf^[hied@$FeijkhWbeh_[djWj_edWdZ
                                                                                                                         loway G, Gibbon WW. Fatty infiltration in                       tion using simultaneous measurement of eye in               equilibrium. In: Rowell LB, Shepherd JT, eds.
                                                                                                                         the cervical extensor muscles in persistent                    head and head in space movements: potential                 Section 12, Exercise: Regulation and Integration
                                                                                                                         whiplash-associated disorders: a mag-                          for use in subjects with a whiplash injury. J Clin          of Multiple Systems. New York, NY: Oxford Uni-
                                                                                                                         netic resonance imaging analysis. Spine.                       Mon Computing. (&&/1()0)'#*&$                               l[hi_joFh[ii"?dY1'//,0(++#(/($
                                                                                                                         (&&,1)'0;.*-#.++$^jjf0%%Zn$Ze_$eh]%'&$'&/-%&'$        *'$=k[pC">_bZ_d]iied9"D_biiedC"JeebWd[d           +-$>bi[C$Ab_d_aZ[h\kdaj_ediijhkd][dZ[iaef\-
                                                                                                                         Xhi$&&&&(*&.*'$&-&+&$)*                                       G. The prevalence of neck pain: a population-                ][b[d]X[h[_Y^i$?d0>bi[C"D[k^kX[hMB"Meb÷
                                                                                                                  (,$ Falla D, Bilenkij G, Jull G. Patients with chronic              based study from northern Sweden. Acta Orthop                >:"[Zi$Der Kranio-Zervikale Übergang. Berlin,
                                                                                                                         neck pain demonstrate altered patterns of                     Scand. (&&(1-)0*++#*+/$                                      Germany: Springer; 1998:43-97.
                                                                                                                         muscle activation during performance of a func-        *($ Guitton D, Kearney RE, Wereley N, Peterson BW.          +.$>bi[C">ebpbC$QL[ij_Xkbeif_dWbh[WYj_edi_d
                                                                                                                         tional upper limb task. Spine$(&&*1(/0'*),#                  Visual, vestibular and voluntary contributions               cervicogenic disequilibrium. Cervicogenic imbal-
                                                                                                                         1440.                                                         to human head stabilization. Exp Brain Res.                  ance]. HNO$(&&&1*.0(/+#)&'$
                                                                                                                                                                             journal of orthopaedic & sports physical therapy | volume 39 | number 5 | may 2009 | 375
                                                                                                                                                                       [     CLINICAL COMMENTARY                                                 ]
                                                                                                                   +/$ Jull G, Falla D, Treleavan J, Sterling M, O’Leary S.            ent subject groups. Clin Rehabil. (&&)1'-0-,.#                   control and motion perception under terrestrial
                                                                                                                          A therapeutic exercise approach for cervical dis-             774.                                                             and microgravity conditions--a conceptual mod-
                                                                                                                          orders. In: Boyling JD, Jull G, eds. Grieve’s Modern   -*$Ah_ij`Wdiied;">WhZWhZejj_hB"7ickdZWhZejj_h                  el. Brain Res Brain Res Rev.'//.1(.0''.#')+$
                                                                                                                          Manual Therapy. The Vertebral Column. Edinburgh,              M, Gudmundsson K. A new clinical test for cervi-        /&$ Michaelson P, Michaelson M, Jaric S, Latash ML,
                                                                                                                          KA09^khY^_bbB_l_d]ijed[1(&&*0*+'#*,/$                      YeY[f^Wb_Ya_d[ij^[j_Yi[di_X_b_jo0Çj^[ÔoÈ$Arch               Sjolander P, Djupsjöbacka M. Vertical posture
                                                                                                                   ,&$@kbb="<WbbW:"Jh[b[Wl[d@">eZ][iF"L_Y[dp_de            Phys Med Rehabil. (&&*1.+0*/&#*/+$                               and head stability in patients with chronic neck
                                                                                                                          B. Retraining cervical joint position sense: the       -+$Ah_ij`Wdiied;"@ediied>$IocfjecY^WhWYj[h-                    pain. J Rehabil Med.(&&)1)+0((/#()+$
                                                                                                                          effect of two exercise regimes. J Orthop Res.                 istics in women with chronic WAD, grades I-II,        /'$ Montfoort I, Kelders WP, van der Geest JN, et al.
                                                                                                                          (&&-1(+0*&*#*'($^jjf0%%Zn$Ze_$eh]%'&$'&&(%                   and chronic insidious onset neck pain. J Whip-                   ?dj[hWYj_edX[jm[[deYkbWhijWX_b_pWj_edh[Ô[n[i
                                                                                                                          `eh$(&((&                                                     lash and Rel Disorders. (&&*1)0)#'-$                             in patients with whiplash injury. Invest Ophthal-
                                                                                                                   ,'$ Jull G, Sterling M, Falla D, Treleaven J, O’Leary S.     -,$ Kristjansson E, Leivseth G, Brinckmann P,                          mol Vis Sci. (&&,1*-0(..'#(..*$^jjf0%%Zn$Ze_$
                                                                                                                          Whiplash, Headache, and Neck Pain: Research-                  Frobin W. Increased sagittal plane segmental                     org/10.1167/iovs.05-1561
                                                                                                                          Based Directions for Physical Therapies. Edin-                motion in the lower cervical spine in women           /($Cedj\eehj?"LWd:[h=[[ij@D"Ib_`f[h>F":[
                                                                                                                          Xkh]^"KA0;bi[l_[h1(&&.$                                    with chronic whiplash-associated disorders,                      Zeeuw CI, Frens MA. Adaptation of the cervico-
                                                                                                                   ,($@kbb=7$:[[fY[hl_YWbÔ[nehckiYb[Zoi\kdYj_ed              grades I-II: a case-control study using a new                    WdZl[ij_Xkbe#eYkbWhh[Ô[n_dm^_fbWi^_d`kho
                                                                                                                          in whiplash. J Musculoskel Pain.(&&&1.0'*)#                  measurement protocol. Spine$(&&)1(.0(('+#                       patients. J Neurotrauma. (&&.1(+0,.-#,/)$
                                                                                                                          154.                                                          ((('$^jjf0%%Zn$Ze_$eh]%'&$'&/-%&'$                              ^jjf0%%Zn$Ze_$eh]%'&$'&./%d[k$(&&-$&)'*
                                                                                                                   ,)$AW`[mia_>"Feeb[;"Bem9^eoD$:e[i_Z_e-                    8HI$&&&&&./+(+$+/,.*$*/                               /)$D[k^kX[hMB$Q9^WhWYj[h_ij_Yie\j^[_d-
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                          pathic neck pain affect balance and mobility in        --$ Kulkarni V, Chandy MJ, Babu KS. Quantita-                          nervation of the head and neck]. Orthopäde.
                                                                                                                          community dwelling adults aged 65 and over?                   tive study of muscle spindles in suboccipital                    '//.1(-0-/*#.&'$
                                                                                                                          Aust J on Ageing.Q?dh[l_[mS$                                muscles of human foetuses. Neurol India.              /*$D[k^kX[hMB$:[hahWd_ep[hl_aWb[X[h]Wd]0[d-
                                                                                                                   ,*$ Karlberg M. The Neck and Human Balance: A                       (&&'1*/0)++#)+/$                                                 twicklung, gelenke, muskulatur und innervation.
                                                                                                                          Clinical and Experimental Approach to “Cervical        -.$ Le Pera D, Graven-Nielsen T, Valeriani M, et al.                   ?d0>bi[C"D[k^kX[hMB"Meb÷>:"[Zi$Der
                                                                                                                          Vertigo” [dissertation]. Lund, Sweden: University             Inhibition of motor system excitability at cortical              Kranio-Zervikale Übergang. Berlin, Germany:
                                                                                                                          >eif_jWbe\BkdZ1'//+$                                       and spinal level by tonic muscle pain. Clin Neu-                 Springer; 1998:11-31.
                                                                                                                   ,+$ Karlberg M, Johansson R, Magnusson M, Frans-                    rophysiol. (&&'1''(0',))#',*'$                            /+$D[k^kX[hMB"8WdaekbI$:[hÇ^Wbij[_bÈZ[i
Copyright © 2009 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
                                                                                                                          with dizziness of suspected cervical origin. Arch             '//-1((0.,+#.,.$                                                 Approaches [thesis]. Reykjavik, Iceland: Univer-
                                                                                                                          Phys Med Rehabil. '//,1--0.-*#..($                     .($Bel[bbC;"=WbWiae9I$M^_fbWi^Z_iehZ[hiÆ                       i_joe\?Y[bWdZ1(&&,$
                                                                                                                   ,.$ Karlberg M, Persson L, Magnusson M. Impaired                    a review. Injury$(&&(1))0/-#'&'$                         /.$Em[di;<"@h$">[dZ[hied9D"=kZWlWbb_CH"
                                                                                                                          postural control in patients with cervico-             .)$ LowChoy NL, Johnson N, Treleaven J, Jull G,                        F_YaWh@=$>[WZh[fei_j_ed_d][hhehi_ddehcWb
                                                                                                                          brachial pain. Acta Otolaryngol Suppl.'//+1+(&              Panizza B, Brown-Rothwell D. Balance, mobil-                     student volunteers: a possible tool to assess the
                                                                                                                          Fj(0**&#**($                                                 ity and gaze stability deficits remain following                  neck’s neuromuscular system. Chiropr Osteo-
                                                                                                                   ,/$AWhdWj^>E"H[_Y^;"HehZ[d9"<[jj[hC":h_l[h              surgical removal of vestibular schwannoma                        pat. (&&,1'*0+$^jjf0%%Zn$Ze_$eh]%'&$''.,%'-*,#
                                                                                                                          J. The perception of body orientation after neck-             (acoustic neuroma): an observational study.                      1340-14-5
                                                                                                                          proprioceptive stimulation. Effects of time and               Aust J Physiother. (&&,1+(0(''#(',$                     //$ Palmgren PJ, Sandstrom PJ, Lundqvist FJ,
                                                                                                                          of visual cueing. Exp Brain Res. (&&(1'*)0)+&#         .*$CWZ[b[_d[F"Fh_[jp[b>"IlWhh[h>"7h[dZj#                      >[_aa_bW>$?cfhel[c[djW\j[hY^_hefhWYj_Y
                                                                                                                          )+.$^jjf0%%Zn$Ze_$eh]%'&$'&&-%i&&(('#&&'#                    Nielsen L. Quantitative posturography in altered                 care in cervicocephalic kinesthetic sensibility
                                                                                                                          &//,#(                                                        sensory conditions: a way to assess balance in-                  and subjective pain intensity in patients with
                                                                                                                   -&$ Kelders WP, Kleinrensink GJ, van der Geest JN,                  stability in patients with chronic whiplash injury.              nontraumatic chronic neck pain. J Manipulative
                                                                                                                          [jWb$J^[Y[hl_Ye#eYkbWhh[Ô[n_i_dYh[Wi[Z                 Arch Phys Med Rehabil. (&&*1.+0*)(#*).$                          Physiol Ther. (&&,1(/0'&&#'&,$^jjf0%%Zn$Ze_$
                                                                                                                          in whiplash injury patients. J Neurotrauma.            .+$ Mayoux-Benhamou MA, Revel M, Vallee C,                             eh]%'&$'&',%`$`cfj$(&&+$'($&&(
                                                                                                                          (&&+1((0'))#')-$^jjf0%%Zn$Ze_$eh]%'&$'&./%                   Roudier R, Barbet JP, Bargy F. Longus colli has         '&&$ Panjabi MM, Lydon C, Vasavada A, Grob D,
                                                                                                                          d[k$(&&+$(($'))                                               a postural function on cervical curvature. Surg                   Crisco JJ, 3rd, Dvorak J. On the understanding
                                                                                                                   -'$ Kristjansson E. The cervical spine and prop-                    Radiol Anat. 1994;16:367-371.                                     of clinical instability. Spine$'//*1'/0(,*(#(,+&$
                                                                                                                          rioception. In: Boyling JD, Jull G, eds. Grieve’s      .,$ McCrea DA. Spinal cord circuitry and motor              '&'$FWiiWjeh[C"HeWjjWI$?dÔk[dY[e\iocfWj^[j_Y
                                                                                                                          Modern Manual Therapy. London, UK: Churchill                  h[Ô[n[i$Exerc Sport Sci Rev. 1986;14:105-141.                   nervous system on sensorimotor function: whip-
                                                                                                                          B_l_d]ijed[1(&&*0(*)#(+,$                             .-$ McLain RF. Mechanoreceptor endings in human                        lash associated disorders (WAD) as a model.
                                                                                                                   -($ Kristjansson E. Reliability of ultrasonography                  cervical facet joints. Spine. 1994;19:495-501.                   Eur J Appl Physiol. (&&,1/.0*()#**/$^jjf0%%
                                                                                                                          for the cervical multifidus muscle in asymp-            ..$CYFWhjbWdZ@C"8heZ[khHH">Wbb]h[dH9$                         Zn$Ze_$eh]%'&$'&&-%i&&*('#&&,#&)'(#.
                                                                                                                          tomatic and symptomatic subjects. Man Ther.                   Chronic neck pain, standing balance, and                 '&($ Peterson BW. Current approaches and future
                                                                                                                          (&&*1/0.)#..$^jjf0%%Zn$Ze_$eh]%'&$'&',%I')+,#                suboccipital muscle atrophy--a pilot study. J                     directions to understanding control of head
                                                                                                                          689X(03)00059-6                                               Manipulative Physiol Ther. '//-1(&0(*#(/$                         movement. Prog Brain Res. (&&*1'*)0),/#).'$
                                                                                                                   -)$ Kristjansson E, Dall’Alba P, Jull G. A study of five      ./$ Mergner T, Rosemeier T. Interaction of vestibular,       '&)$F[j[hied8M"=ebZX[h]@"8_bejje="<kbb[h@>$
                                                                                                                          cervicocephalic relocation tests in three differ-             somatosensory and visual signals for postural                     9[hl_YeYebb_Yh[Ô[n0_jiZodWc_Yfhef[hj_[iWdZ
                                                                                                                  376 | may 2009 | volume 39 | number 5 | journal of orthopaedic & sports physical therapy
                                                                                                                                      _dj[hWYj_edm_j^l[ij_XkbWhh[Ô[n[i$J Neuro-                             postural stability during clinical balance tests                      lash. Man Ther. (&&,1''0//#'&,$^jjf0%%Zn$Ze_$
                                                                                                                                      physiol. 1985;54:90-109.                                                  in patients with chronic whiplash injury symp-                        eh]%'&$'&',%`$cWj^$(&&+$&*$&&)
                                                                                                                       '&*$Feeb[;"Jh[b[Wl[d@"@kbb=$J^[_dÔk[dY[e\                                   toms. Spine$(&&)1(.0'-(+#'-)*$^jjf0%%Zn$Ze_$                 ')*$ Treleaven J, Jull G, LowChoy N. Smooth pur-
                                                                                                                                      neck pain on balance and gait parameters                                  org/10.1097/01.BRS.0000083170.34304.A3                                 suit neck torsion test in whiplash-associated
                                                                                                                                      in community-dwelling elders. Man Ther.                      ''/$ Spitzer WO, Skovron ML, Salmi LR, et al. Sci-                                 disorders: relationship to self-reports of neck
                                                                                                                                      (&&.1')0)'-#)(*$^jjf0%%Zn$Ze_$eh]%'&$'&',%`$                             entific monograph of the Quebec Task Force                              pain and disability, dizziness and anxiety. J
                                                                                                                                      cWj^$(&&-$&($&&(                                                          on Whiplash-Associated Disorders: redefin-                              Rehabil Med. (&&+1)-0('/#(()$^jjf0%%Zn$Ze_$
                                                                                                                            '&+$ Reid SA, Rivett DA. Manual therapy treatment                                  _d]Çm^_fbWi^ÈWdZ_jicWdW][c[dj$Spine.                              eh]%'&$'&.&%',+&'/-&*'&&(*(//
                                                                                                                                      of cervicogenic dizziness: a systematic review.                           '//+1(&0'I#-)I$                                                 ')+$ Treleaven J, Jull G, Lowchoy N. Standing bal-
                                                                                                                                      Man Ther. (&&+1'&0*#')$                                       '(&$ Stapley PJ, Beretta MV, Dalla Toffola E, Schi-                              ance in persistent whiplash: a comparison
                                                                                                                             '&,$ Reid SA, Rivett DA, Katekar MG, Callister R.                                  eppati M. Neck muscle fatigue and postural                           between subjects with and without dizziness.
                                                                                                                                      Sustained natural apophyseal glides (SNAGs)                                control in patients with whiplash injury. Clin                       J Rehabil Med. (&&+1)-0((*#((/$^jjf0%%Zn$Ze_$
                                                                                                                                      are an effective treatment for cervicogenic                                Neurophysiol. (&&,1''-0,'&#,(($^jjf0%%Zn$Ze_$                       eh]%'&$'&.&%',+&'/-&+'&&(-/./
                                                                                                                                      dizziness. Man Ther. (&&.1')0)+-#),,$^jjf0%%                              eh]%'&$'&',%`$Yb_df^$(&&+$''$&&-                           '),$ Treleaven J, Jull G, Sterling M. Dizziness and un-
                                                                                                                                      Zn$Ze_$eh]%'&$'&',%`$cWj^$(&&-$&)$&&,                     '('$ Stein JF, Glickstein M. Role of the cerebellum                                   steadiness following whiplash injury: character-
                                                                                                                              '&-$ Revel M, Andre-Deshays C, Minguet M. Cervi-                                 in visual guidance of movement. Physiol Rev.                           istic features and relationship with cervical joint
                                                                                                                                     cocephalic kinesthetic sensibility in patients                             '//(1-(0/,-#'&'-$                                                      position error. J Rehabil Med. (&&)1)+0),#*)$
                                                                                                                                     with cervical pain. Arch Phys Med Rehabil.                  '(($ Sterling M, Jull G, Vicenzino B, Kenardy J,                     ')-$ Treleaven J, LowChoy N, Darnell R, Panizza B,
Downloaded from www.jospt.org at on September 8, 2015. For personal use only. No other uses without permission.
                                                                                                                                                                                                                                                                     @
                                                                                                                                     eh]%'&$'&',%`$cWj^$(&&,$'&$&&(                                       '))$ Treleaven J, Jull G, LowChoy N. The relationship
                                                                                                                  ''.$I`ijhec>"7bbkc@>"9Whf[dj[hC="7Za_d7B"                                         of cervical joint position error to balance and
                                                                                                                                                                                                                                                                                         CEH;?D<EHC7J?ED
                                                                                                                                     >ed[]][h<";jjb_dJ$JhkdaimWoc[Wikh[ie\                               eye movement disturbances in persistent whip-                                 WWW.JOSPT.ORG
journal of orthopaedic & sports physical therapy | volume 39 | number 5 | may 2009 | 377