MINI REVIEW ARTICLE

HUMAN NEUROSCIENCE
published: 17 February 2014
doi: 10.3389/fnhum.2014.00073

Dissociable roles of the hippocampus and parietal cortex in

processing of coordinate and categorical spatial
information
Oliver Baumann 1 * and Jason B. Mattingley 1,2
1
Queensland Brain Institute, The University of Queensland, St. Lucia, QLD, Australia
2
School of Psychology, The University of Queensland, St. Lucia, QLD, Australia

Edited by: It is generally accepted that spatial relationships and spatial information are critically
R. Shayna Rosenbaum, York involved in the formation of cognitive maps. It remains unclear, however, which properties
University, Canada
of the world are explicitly encoded and how these properties might contribute to the
Reviewed by:
formation of such maps. It has been proposed that spatial relations are encoded either
Elisa Ciaramelli, Università di Bologna,
Italy categorically, such that the relative positions of objects are defined in prepositional terms;
Michael R. Hunsaker, MIND Institute, or as visual coordinates, such that the precise distances between objects are represented.
USA Emerging evidence from human and animal studies suggests that distinct neural circuits
*Correspondence: might underlie categorical and coordinate representations of object locations during active
Oliver Baumann, Queensland Brain
spatial navigation. Here we review evidence for the hypothesis that the hippocampal
Institute, The University of
Queensland, Building 79, St. Lucia, formation is crucial for encoding coordinate information, whereas the parietal cortex is
QLD 4072, Australia crucial for encoding categorical spatial information. Our short review provides a novel
e-mail: o.baumann@uq.edu.au view regarding the functions and potential interactions of these two regions during active
spatial navigation.

Keywords: categorical, coordinate, spatial, memory, navigation, fMRI, hippocampus, parietal

INTRODUCTION as a function of an animal’s location in space, but show little

As humans navigate they build up mental models of the physical dependence on the animal’s egocentric orientation during active
world, which are indispensable for finding one’s way in complex navigation (O’Keefe and Dostrovsky, 1971; Ekstrom et al., 2003).
environments and planning routes to distant locations. Previous
human and animal studies have suggested that mental models of CATEGORICAL VS. COORDINATE SPATIAL
spatial environments are not maintained as a unitary representa- REPRESENTATIONS
tion; instead, different aspects of space appear to be underpinned Another hypothesized dichotomy within spatial memory is the
by many different cognitive subsystems and brain regions (e.g., distinction between categorical and coordinate representations of
Bohbot et al., 2000; Epstein and Higgins, 2007; Zhang et al., space. Categorical spatial relationships capture general proper-
2012; Baumann and Mattingley, 2013). A prominent example ties of the spatial layout, referring to broad equivalence classes
of this representational fragmentation is the distinction between of spatial positions relative to reference stimuli (e.g., left/right,
egocentric and allocentric representations of object locations. The below/above, inside/outside). By contrast, coordinate spatial rela-
egocentric representational system is thought to provide tran- tionships refer to precise spatial locations, which can be expressed
sient action-oriented representations of the environment from in terms of metric units between locations (e.g., Object A is
the viewpoint of the navigator (for an overview see reviews by located 2.4 m from Object B). This distinction was originally
Klatzky, 1998; Burgess, 2006). Several lines of evidence indicate proposed by Kosslyn (Kosslyn, 1987; Kosslyn et al., 1989, 1992),
that egocentric representations are supported by the parietal lobe. based on neural network simulations that showed that it is com-
For example, lesions of the posterior parietal cortex are known putationally more efficient to represent categorical and coordi-
to disrupt patients’ ability to point to the locations of objects in nate spatial information separately. Kosslyn also made anatomic
the absence of visual input (Levine et al., 1985), and neurons in predictions, proposing that the left hemisphere is involved specif-
the intraparietal sulcus have been found to respond to visual and ically in processing categorical information, whereas the right
auditory targets in a body-centered fashion (Mullette-Gillman hemisphere is involved in processing coordinate information.
et al., 2005). In contrast, the allocentric system is thought to According to his original theory, such a hemispheric asymmetry
provide a comprehensive and enduring representation of the might have arisen for two reasons. First, the left hemisphere
environment that is accessible from any viewpoint (Klatzky, 1998; advantage for categorical processing could have emerged from
Burgess, 2006). In humans and rodents, the hippocampus has its pre-existing dominance for language, particularly with respect
been found to contain view-invariant cells that fire selectively to category formation, whereas the right hemisphere advantage

Frontiers in Human Neuroscience www.frontiersin.org February 2014 | Volume 8 | Article 73 | 1

Baumann and Mattingley Spatial relation coding during navigation

for coordinate processing could have arisen from its fundamental neural circuits underlying the encoding of categorical and coor-
role in spatial navigation (Kosslyn, 1987; Kosslyn et al., 1989). dinate spatial relations during active navigation. Rats were first
In this context, however, it is important to mention that the left familiarized with a geometric object configuration on top of a
hemisphere advantage for categorical processing has also been round board (see Figure 1B). Subsequently, either the categorical
observed in monkeys (Jason et al., 1984; Vogels et al., 1994) or coordinate relationship between the geometric objects was
and pigeons (Yamazaki et al., 2007), implying that language is altered (e.g., via a left-right transposition or distance change),
not the only factor that aids category formation. An alternative and the rats’ exploration behavior was recorded and assessed
explanation for the hemispheric asymmetry is that it might arise as an indicator of their spatial knowledge (see Figure 1C). Rats
from a difference in the receptive field properties of neurons naturally familiarize themselves with their environment via initial
in the two hemispheres (Kosslyn et al., 1992; Jacobs et al., exploration (habituation, Poucet, 1993), and if a change in the
1994; Chabris and Kosslyn, 1998). According to this account, environment occurs they typically spend substantially more time
the right hemisphere has a bias to encode outputs from neurons re-exploring the environment (dishabituation, Save et al., 1992).
with relatively large receptive fields, whereas the left hemisphere The ratio of the total time spent exploring the displaced objects
has a bias for neurons with relatively small receptive fields. and the total time spent exploring the non-displaced objects
The assumption is that non-overlapping receptive fields divide can be used as an indicator of the reliability of the underlying
space into simple categorical relations, whereas large, overlap- spatial representation. For example, if a rat spends a significant
ping receptive fields support the encoding of precise coordinate amount of time re-exploring two objects that have undergone a
relations. This hypothesis is corroborated by the observation that categorical transformation, but fails to respond to a coordinate
the left hemisphere is biased to process signals from the parvo- transformation, it can be presumed that the rat has a compro-
cellular visual pathway, whereas the right hemisphere is biased to mised ability to encode coordinate relations, whereas its ability to
process signals from the magnocellular visual pathway (Kosslyn encode categorical relations is unimpaired. Using this approach,
et al., 1992; Roth and Hellige, 1998; Hellige and Cumberland, Goodrich-Hunsaker et al. (2005) discovered that rats with dorsal
2001). hippocampal lesions displayed deficits in coordinate spatial learn-
ing tasks, but behaved normally in categorical tasks. On the other
DISTINCT NEURAL NETWORKS UNDERLIE ENCODING OF hand, rats with parietal lesions showed significant impairments in
CATEGORICAL AND COORDINATE SPATIAL RELATIONS categorical spatial memory tasks but not in coordinate tasks.
Despite the uncertainty regarding a theoretical explanation, Thus, whereas the human literature has suggested a hemi-
several human studies have provided experimental evidence for spheric specialization (left vs. right) for the encoding of cate-
the hypothesized separation of coordinate and categorical repre- gorical and coordinate spatial relations, the rodent data imply a
sentations of space. Evidence has come from three main sources: structural specialization (parietal cortex vs. hippocampus). It is
(1) visual half-field studies in healthy participants; (2) neu- important to note, however, that the relevant human studies have
roimaging investigations; and (3) behavioral studies in patients employed almost exclusively static, two-dimensional stimulus
with brain lesions. The proposed hemispheric lateralization effect arrays, whereas the rodent studies have used three-dimensional
has been most consistently observed in the parietal cortex (cf. mazes and arenas that the animal is required to learn through
Jager and Postma, 2003), but has also been detected in frontal active exploration. A possible explanation for the apparent dis-
areas (Slotnick and Moo, 2006; van der Ham et al., 2009). It is crepancy between the human and rodent research, therefore, is
important to add, however, that the evidence for hemispheric that the two species process categorical and coordinate informa-
specialization originates almost exclusively from experiments in tion differently, or that the discrepancy is due to the different
which human participants are asked to encode and recall visual paradigms used in people and rats.
stimuli within static, two-dimensional displays (cf. Jager and We recently investigated this question by using fMRI to mon-
Postma, 2003). A classic example is the seminal study by Kosslyn itor brain activity while human participants actively navigated
et al., 1989; see Figure 1A) in which participants either judged a three-dimensional virtual arena, which was similar to those
whether a dot was on or off the contour of a line drawing of employed in rodent research (Baumann et al., 2012). The virtual
a nonsense shape (the categorical task), or whether the dot was arena consisted of an infinite plane and contained just two geo-
within 2 mm of the contour (the metric task). Later studies repli- metric objects, with one serving as a landmark and the other as
cated the hemispheric specialization effect using more realistic a target. The landmark was a cylinder rendered in four different
stimuli, such as meaningful objects (Saneyoshi et al., 2006) and colors, virtually dividing the arena into four quadrants, and the
natural scenes (van der Ham et al., 2011). These studies, however, target was a small yellow pyramid (see Figure 2A). On every trial,
did not examine whether the distinction between coordinate the participants were required to locate and navigate to the target
and categorical representations would also apply to the encoding object using a hand-held joystick. In the categorical condition,
of three-dimensional spatial environments, in which individuals participants were instructed to remember the quadrant in which
must build up a representation based upon continually changing the target object was located, as defined by the color-code of
visual inputs obtained from a first-person perspective. the central landmark. By contrast, in the coordinate condition
Initial evidence for separate coordinate and categorical rep- participants were instructed to remember the distance between
resentations of three-dimensional spatial environments was the target object and the landmark, irrespective of the quadrant
obtained in animals. Goodrich-Hunsaker et al. (2005) employed in which the target was located. After a brief maintenance period
a novelty-detection task in brain-lesioned rats to investigate the participants re-entered the virtual environment, but the target

Frontiers in Human Neuroscience www.frontiersin.org February 2014 | Volume 8 | Article 73 | 2

Baumann and Mattingley Spatial relation coding during navigation

FIGURE 1 | (A) Example of the stimuli used in the experiment by Kosslyn (2005). Shown is the geometric configuration of colored objects on top of
et al. (1989). The stimuli were amorphous outline figures with a large dot a round board. (C) After rats habituated to the environment, either a
located 0, 1 or 10 mm from the border of the figure. Participants in the categorical or coordinate transformation was applied (in this illustration, a
coordinate task were asked to judge whether the dot was within 2 mm categorical transformation via a left-right transposition of the green and
of the contour of the blob, whereas participants in the categorical task red landmarks is shown). Subsequent assessment of the rats’
were asked to judge whether the dot was on or off the contour. (B) re-exploration behavior served as an indicator of the precision of their
Illustration of the spatial environments used by Goodrich-Hunsaker et al. internal representation of the layout.

object was now absent. In the coordinate condition participants target object in the retrieval phase. Other human imaging studies
were required to navigate back to the remembered distance of have implicated the human hippocampus even more explicitly
the target object from the cylindrical landmark, ignoring the in the encoding of distance information. Morgan et al. (2011)
quadrant, whereas in the categorical condition participants were recorded brain activity using fMRI while university students were
required to navigate back to the remembered sector of the target’s shown images of landmarks from a familiar college campus. They
location, irrespective their distance from the central landmark. To found that activity in the hippocampus scaled with the distances
determine whether distinct neural substrates are responsible for between landmarks. More specifically, the hippocampal response
the encoding of categorical and coordinate aspects of spatial envi- to each landmark was dependent on the real-world distance
ronments, encoding-related fMRI activity was compared using a between that landmark and the landmark shown on the preceding
simple subtraction approach. The results revealed a hemispheric trial. This distance-related effect was observed in the absence of
as well as structural dissociation for categorical vs. coordinate any explicit navigational task—participants were simply asked to
memory encoding. In line with previous studies in humans, think about the identity of each landmark—suggesting that this
the categorical condition led to predominantly left hemispheric process operates automatically. Further evidence for a hippocam-
activity, whereas the coordinate condition activated primarily the pal role in distance coding comes from a recent imaging study by
right hemisphere. Moreover, in line with the relevant rodent liter- Viard et al. (2011), in which participants were asked to indicate
ature, categorical encoding led to stronger activity in the parietal the shortest egocentric distance to a target location from varying
cortex, whereas coordinate encoding led to stronger activity in the locations in a virtual environment. The hippocampus showed a
hippocampus (see Figures 2B–D). very robust increase in activation with goal proximity, in line with
its hypothesized role in encoding coordinate properties of the
spatial environment.
HIPPOCAMPAL AND PARIETAL CONTRIBUTIONS TO While crucial for the encoding of coordinate spatial relations,
SPATIAL-RELATION CODING lesion data in rodents suggest that categorical spatial relations can
The notion that the hippocampus underlies the encoding of be encoded in the absence of an intact hippocampus (Goodrich-
coordinate spatial relations is in line with earlier human imaging Hunsaker et al., 2005). Lesions of the parietal lobe, however, have
studies, which showed that the hippocampus is typically active been found to cause severe deficits in rodents during such tasks,
whenever spatial associations have to be formed in a way that suggesting an important role for this structure in the encoding
allows for absolute metric accuracy during navigation. A recent of categorical spatial relations. In humans, the posterior parietal
example is an fMRI study in which we observed a close rela- cortex has long been known to play a pivotal role in the short-
tionship between hippocampal activity and metric accuracy in term maintenance of spatial information (for a meta-analysis, see
a memory-guided navigation task (Baumann et al., 2010). We Wager et al., 2003). However, several lines of evidence also point to
measured neural responses as participants learned the location a more specific role of this structure in categorical spatial informa-
of a single target object relative to a small set of landmarks. tion processing. Early evidence came from clinical reports, which
Following a delay, the target was removed and participants were suggested that lesions of the posterior parietal lobe can lead to
required to navigate back to its original position. We found that left-right (Laeng, 1994) or inside-outside confusion for locations
greater activity in the right hippocampus during object-location in space (Robertson et al., 1997). In a later study, Ciaramelli
encoding predicted higher metric accuracy in locating the hidden et al. (2010) reported that patients with lesions in the posterior

Frontiers in Human Neuroscience www.frontiersin.org February 2014 | Volume 8 | Article 73 | 3

Baumann and Mattingley Spatial relation coding during navigation

FIGURE 2 | (A) Schematic of the virtual environment used in the experiment environments and differed only in the instructions to the participants (i.e.,
by Baumann et al. (2012). The blue and green side of the reference landmark coordinate task: “Remember the distance”; categorical task: “Remember the
is shown. The target is shown in yellow, with a virtual “beacon” projecting sector”). (B) Rendered image of left hemisphere showing corresponding
vertically from its apex. Participants were required to actively navigate the fMRI data. (C) Axial view. (D) Sagittal view. There was greater left posterior
arena and to encode either the distance of the target relative to the landmark parietal activity during the encoding of categorical spatial relations, and
(coordinate task), or the sector in which the target object was located greater right hippocampal activity during the encoding of coordinate spatial
(categorical task). The two task conditions employed visually identical virtual relations.

parietal cortex show deficits in making landmark sequence (i.e., should benefit from an egocentric reference frame. In contrast,
categorical) judgments, but are unimpaired in distance and prox- the independence hypothesis states that reference frame processing
imity (i.e., coordinate) judgments. In recent years, a series of and spatial relation coding form independent dimensions, which
neuroimaging studies have provided additional evidence for a can be fully combined without showing selective facilitation.
role of the human parietal cortex in encoding categorical spatial Ruotolo et al. (2011) tested the interaction and independence
relations (cf. Jager and Postma, 2003). An interesting example is hypotheses in a behavioral experiment. Participants were asked to
a study by Amorapanth et al. (2010), which found that having judge the position of two vertical bars placed above and below a
participants direct their attention to categorical spatial relations horizontal bar, in relation either to their body midline (egocentric
between objects, as opposed to the identity of objects, resulted in reference frame) or to the center of the horizontal bar (allo-
greater activity in superior and inferior parietal cortices. Finally, centric reference frame). Moreover, they had to make distance
while most of the human findings have been based on static (coordinate) judgments or relative categorical judgments. Partic-
two-dimensional stimulus arrays, we recently demonstrated that ipants were more accurate in judging categorical than coordinate
the posterior parietal cortex is also engaged when categorical relations, and especially so in the allocentric condition. This
relations have to be encoded within dynamic, three-dimensional study supports the interaction hypothesis, suggesting that reference
environments (Baumann et al., 2012). frame processing and spatial relation coding are not completely
independent cognitive mechanisms. It is important to note, how-
REFERENCE FRAME PROCESSING VS. SPATIAL RELATION ever, that the effects observed in the study of Ruotolo et al. (2011)
CODING could be task-dependent. Previous studies have shown that static,
As mentioned above, another hypothesized dichotomy in spatial two-dimensional perceptual tasks might favor allocentric and
memory is the distinction between egocentric and allocentric categorical representations, whereas egocentric and coordinate
representations of object locations. Previous studies have indi- information could be more relevant in three-dimensional, action-
cated that allocentric representations are underpinned by the oriented tasks (cf. Schenk and McIntosh, 2010).
hippocampus, whereas egocentric representations rely on the To answer the question whether and how reference frame
parietal cortex (cf. Burgess, 2006). This raises the important processing and spatial relation coding interact, it will be nec-
question of how these findings might best be integrated with essary to determine the neural correlates of these cognitive
the observed role of the same brain structures in coordinate processes in one common experiment. Only by carefully con-
and categorical spatial relation coding. Jager and Postma (2003) trolling both allocentric/egocentric and categorical/coordinate
proposed two opposing hypotheses concerning this question. aspects of spatial navigation tasks will it be possible to accu-
The interaction hypothesis states that allocentric processing is rately discern their relative contributions to parietal and hip-
associated with categorical coding of spatial relations, whereas pocampal activation patterns. Based on current evidence, we
egocentric processing is closely linked to coordinate coding. The hypothesize that spatial relation coding and reference frame
logic behind this hypothesis is that allocentric representations processing are independent cognitive mechanisms that engage
provide an observer with a sense of “space constancy”, defined as different subregions of the hippocampus and posterior parietal
the awareness of relative, categorical locations of objects, which cortex. An allocentric-coordinate task should therefore be entirely
underlies an observer’s ability to recognize scenes. Coordinate hippocampal dependent, whereas an egocentric-categorical task
representations, on the other hand, are used for action-oriented, would be solely dependent on the parietal cortex. On the
body-centered tasks. The interaction hypothesis therefore predicts other hand, allocentric-categorical and egocentric-coordinate
that categorical spatial processing should be more efficient within navigation tasks should rely on both the hippocampus and the
an allocentric reference frame, whereas coordinate processing parietal cortex. Future experiments will be necessary to test these

Frontiers in Human Neuroscience www.frontiersin.org February 2014 | Volume 8 | Article 73 | 4

Baumann and Mattingley Spatial relation coding during navigation

predictions and to provide a more mechanistic understanding Ciaramelli, E., Rosenbaum, R. S., Solcz, S., Levine, B., and Moscovitch, M. (2010).
of the roles hippocampal and parietal structures play in spatial Mental space travel: damage to posterior parietal cortex prevents egocentric
navigation and reexperiencing of remote spatial memories. J. Exp. Psychol.
relation coding and reference frame processing.
Learn. Mem. Cogn. 36, 619–634. doi: 10.1037/a0019181
Ekstrom, A. D., Kahana, M. J., Caplan, J. B., Fields, T. A., Isham, E. A., Newman,
CONCLUSION E. L., et al. (2003). Cellular networks underlying human spatial navigation.
Nature 425, 184–188. doi: 10.1038/nature01964
There is considerable evidence for dissociable roles of the hip- Epstein, R. A., and Higgins, J. S. (2007). Differential parahippocampal and retros-
pocampus and parietal cortex in encoding of coordinate and plenial involvement in three types of visual scene recognition. Cereb. Cortex 17,
categorical spatial information in three-dimensional environ- 1680–1693. doi: 10.1093/cercor/bhl079
ments. Crucially, recent findings suggest that the neural networks Goodrich-Hunsaker, N. J., Hunsaker, M. R., and Kesner, R. P. (2005). Dissociating
that subserve categorical and coordinate encoding are different the role of the parietal cortex and dorsal hippocampus for spatial information
processing. Behav. Neurosci. 119, 1307–1315. doi: 10.1037/0735-7044.119.5.
from those commonly reported in studies involving static, two- 1307
dimensional stimulus arrays. Given the growing body of literature Hellige, J. B., and Cumberland, N. (2001). Categorical and coordinate spatial
suggesting a diversity of functions of hippocampal and parietal processing: more on contributions of the transient/magnocellular visual system.
subregions (e.g., Howard et al., 2013; Poppenk et al., 2013) it will Brain Cogn. 45, 155–163. doi: 10.1006/brcg.2000.1233
Howard, L. R., Kumaran, D., Ólafsdóttir, H. F., and Spiers, H. J. (2013). Dissociation
be necessary to characterize more precisely the neural foundations
between dorsal and ventral posterior parietal cortical responses to inciden-
of categorical and coordinate encoding of spatial environments. tal changes in natural scenes. PLoS One 8:e67988. doi: 10.1371/journal.pone.
The nature of the representations underlying human spatial 0067988
cognition is still the subject of intense debate (Burgess, 2006). Jacobs, R. A., and Kosslyn, S. M. (1994). Encoding shape and spatial relations: the
We believe the notion of distinct categorical and coordinate role of receptive field size in coordinating complementary representations. Cogn.
Sci. 18, 361–386.
representations of spatial environments constitutes an important
Jager, G., and Postma, A. (2003). On the hemispheric specialization for categorical
additional factor to be considered in building a comprehensive and coordinate spatial relations: a review of the current evidence. Neuropsycholo-
model of human and animal spatial navigation, and that it could gia 41, 504–515. doi: 10.1016/s0028-3932(02)00086-6
have important applications beyond the laboratory. It should be Jason, G. W., Cowey, A., and Weiskrantz, L. (1984). Hemispheric asymmetry for a
possible, for example, to develop more refined behavioral tests in visuospatial task in monkeys. Neuropsychologia 22, 777–784. doi: 10.1016/0028-
3932(84)90102-7
patients with topographical disorientation, by incorporating mea- Klatzky, R. L. (1998). “Allocentric and egocentric spatial representations: defini-
sures of categorical and coordinate spatial performance (Aguirre tions, distinctions and interconnections,” in Spatial Cognition. An Interdisci-
and D’Esposito, 1999). plinary Approach to Representing and Processing Spatial Knowledge, eds C. Freksa,
C. Habel and K. F. Wender (Berlin: Springer), 1–17.
Kosslyn, S. M. (1987). Seeing and imagining in the cerebral hemispheres: a
ACKNOWLEDGMENTS computational approach. Psychol. Rev. 94, 148–175.
Oliver Baumann was supported by an Australian Research Coun- Kosslyn, S. M., Chabris, C. F., Marsolek, C. J., and Koenig, O. (1992). Categorical
cil Discovery Early Career Researcher Award (DE120100535). versus coordinate spatial relations: computational analyses and computer simu-
lations. J. Exp. Psychol. Hum. Percept. Perform. 18, 562–577. doi: 10.1037//0096-
Jason B. Mattingley was supported by an Australian Research 1523.18.2.562
Council Australian Laureate Fellowship (FL110100103). The Kosslyn, S. M., Koenig, O., Barret, A., Cave, C. B., Tang, J., and Gabrieli, J. D. E.
authors would also like to thank David Lloyd for creating (1989). Evidence for two types of spatial representations: hemispheric special-
Figure 1. ization for categorical and coordinate relations. J. Exp. Psychol. Hum. Percept.
Perform. 15, 723–735. doi: 10.1037/0096-1523.15.4.723
Laeng, B. (1994). Lateralization of categorical and coordinate spatial functions:
REFERENCES a study of unilateral stroke patients. J. Cogn. Neurosci. 6, 189–203. doi: 10.
Aguirre, G. K., and D’Esposito, M. (1999). Topographical disorientation: a 1162/jocn.1994.6.3.189
synthesis and taxonomy. Brain 122, 1613–1628. doi: 10.1093/brain/122.9. Levine, D. N., Warach, J., and Farah, M. J. (1985). Two visual systems in mental
1613 imagery: dissociation of ‘what’ and ‘where’ in imagery disorders due to bilateral
Amorapanth, P. X., Widick, P., and Chatterjee, A. (2010). The neural basis for spatial posterior cerebral lesions. Neurology 35, 1010–1018. doi: 10.1212/wnl.35.7.1010
relations. J. Cogn. Neurosci. 22, 1739–1753. doi: 10.1162/jocn.2009.21322 Morgan, L. K., MacEvoy, S. P., Aguirre, G. K., and Epstein, R. A. (2011). Distances
Baumann, O., Chan, E., and Mattingley, J. B. (2010). Dissociable neural circuits for between realworld locations are represented in the human hippocampus. J.
encoding and retrieval of object locations during active navigation in humans. Neurosci. 31, 1238–1245. doi: 10.1523/jneurosci.4667-10.2011
Neuroimage 49, 2816–2825. doi: 10.1016/j.neuroimage.2009.10.021 Mullette-Gillman, O. A., Cohen, Y. E., and Groh, J. M. (2005). Eye-centered,
Baumann, O., Chan, E., and Mattingley, J. B. (2012). Distinct neural networks head-centered and complex coding of visual and auditory targets in the
underlie encoding of categorical versus coordinate spatial relations during intraparietal sulcus. J. Neurophysiol. 94, 2331–2352. doi: 10.1152/jn.00021.
active navigation. Neuroimage 60, 1630–1637. doi: 10.1016/j.neuroimage.2012. 2005
01.089 O’Keefe, J., and Dostrovsky, J. (1971). The hippocampus as a spatial map. Prelimi-
Baumann, O., and Mattingley, J. B. (2013). Dissociable representations of environ- nary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175.
mental size and complexity in the human hippocampus. J. Neurosci. 33, 10526– doi: 10.1016/0006-8993(71)90358-1
10533. doi: 10.1523/jneurosci.0350-13.2013 Poppenk, J., Evensmoen, H. R., Moscovitch, M., and Nadel, L. (2013). Long-
Bohbot, V. D., Allen, J. J., and Nadel, L. (2000). Memory deficits characterized by axis specialization of the human hippocampus. Trends Cogn. Sci. 17, 230–240.
patterns of lesions to the hippocampus and parahippocampal cortex. Ann. N Y doi: 10.1016/j.tics.2013.03.005
Acad. Sci. 911, 355–368. doi: 10.1111/j.1749-6632.2000.tb06737.x Poucet, B. (1993). Spatial cognitive maps in animals: new hypotheses on their struc-
Burgess, N. (2006). Spatial memory: how egocentric and allocentric combine. ture and neural mechanisms. Psychol. Rev. 100, 163–182. doi: 10.1037/0033-
Trends Cogn. Sci. 10, 551–557. doi: 10.1016/j.tics.2006.10.005 295x.100.2.163
Chabris, C. F., and Kosslyn, S. M. (1998). How do the cerebral hemispheres Robertson, L., Treisman, A., Friedman-Hill, S., and Grabowecky, M. (1997). The
contribute to encoding spatial relations. Curr. Dir. Psychol. Sci. 7, 8–14. doi: 10. interaction of spatial and object pathways: evidence from Balint’s syndrome. J.
1111/1467-8721.ep11521809 Cogn. Neurosci. 9, 295–317. doi: 10.1162/jocn.1997.9.3.295

Frontiers in Human Neuroscience www.frontiersin.org February 2014 | Volume 8 | Article 73 | 5

Baumann and Mattingley Spatial relation coding during navigation

Roth, E. C., and Hellige, J. B. (1998). Spatial processing and hemispheric asym- Vogels, R., Saunders, R. C., and Orban, G. A. (1994). Hemispheric lateralization in
metry. Contributions of the transient/magnocellular visual system. J. Cogn. rhesus monkeys can be task-dependent. Neuropsychologia 32, 425–438. doi: 10.
Neurosci. 10, 472–484. doi: 10.1162/089892998562889 1016/0028-3932(94)90088-4
Ruotolo, F., van der Ham, I. J., Iachini, T., and Postma, A. (2011). The relationship Wager, T. D., and Smith, E. E. (2003). Neuroimaging studies of work-
between allocentric and egocentric frames of reference and categorical and ing memory: a meta analysis. Cogn. Affect. Behav. Neurosci. 3, 255–274.
coordinate spatial information processing. Q. J. Exp. Psychol. (Hove) 64, 1138– doi: 10.3758/cabn.3.4.255
1156. doi: 10.1080/17470218.2010.539700 Yamazaki, Y., Aust, U., Huber, L., Hausmann, M., and Gunturkun, O. (2007).
Saneyoshi, A., Kaminaga, T., and Michimata, C. (2006). Hemispheric processing Lateralized cognition: asymmetrical and complementary strategies of pigeons
of categorical/metric properties in object recognition. Neuroreport 17, 517–521. during discrimination of the “human concept”. Cognition 104, 315–344. doi: 10.
doi: 10.1097/01.wnr.0000209009.70975.4c 1016/j.cognition.2006.07.004
Save, E., Poucet, B., Foreman, N., and Buhot, M. C. (1992). Object exploration and Zhang, H., Copara, M., and Ekstrom, A. D. (2012). Differential recruitment
reactions to spatial and nonspatial changes in hooded rats following damage of brain networks following route and cartographic map learning of spatial
to parietal cortex or hippocampal formation. Behav. Neurosci. 106, 447–456. environments. PLoS One 7:e44886. doi: 10.1371/journal.pone.0044886
doi: 10.1037/0735-7044.106.3.447
Schenk, T., and McIntosh, R. D. (2010). Do we have independent visual Conflict of Interest Statement: The authors declare that the research was con-
streams for perception and action? Cogn. Neurosci. 1, 52–62. doi: 10. ducted in the absence of any commercial or financial relationships that could be
1080/17588920903388950 construed as a potential conflict of interest.
Slotnick, S. D., and Moo, L. R. (2006). Prefrontal cortex hemispheric specialization
for categorical and coordinate visual spatial memory. Neuropsychologia 44, Received: 27 November 2013; accepted 29 January 2014; published online: 17 February
1560–1568. doi: 10.1016/j.neuropsychologia.2006.01.018 2014.
van der Ham, I. J., Raemaekers, M., Van Wezel, R. J. A., Oleksiak, A., and Postma, Citation: Baumann O and Mattingley JB (2014) Dissociable roles of the hippocampus
A. (2009). Categorical and coordinate spatial relations in working memory: an and parietal cortex in processing of coordinate and categorical spatial information.
fMRI study. Brain Res. 1297, 70–79. doi: 10.1016/j.brainres.2009.07.088 Front. Hum. Neurosci. 8:73. doi: 10.3389/fnhum.2014.00073
van der Ham, I. J., Zandvoort, M. J., Frijns, C. J., Kappelle, L. J., and Postma, This article was submitted to the journal Frontiers in Human Neuroscience.
A. (2011). Hemispheric differences in spatial relation processing in a scene Copyright © 2014 Baumann and Mattingley. This is an open-access article distributed
perception task: a neuropsychological study. Neuropsychologia 49, 999–1005. under the terms of the Creative Commons Attribution License (CC BY). The use, dis-
doi: 10.1016/j.neuropsychologia.2011.02.024 tribution or reproduction in other forums is permitted, provided the original author(s)
Viard, A., Doeller, C. F., Hartley, T., Bird, C. M., and Burgess, N. (2011). Anterior or licensor are credited and that the original publication in this journal is cited, in
hippocampus and goal-directed spatial decision making. J. Neurosci. 31, 4613– accordance with accepted academic practice. No use, distribution or reproduction is
4621. doi: 10.1523/jneurosci.4640-10.2011 permitted which does not comply with these terms.

Frontiers in Human Neuroscience www.frontiersin.org February 2014 | Volume 8 | Article 73 | 6