Troyer (2000)
Troyer (2000)
To cite this article: Angela K. Troyer (2000): Normative Data for Clustering and Switching on Verbal Fluency Tasks, Journal
of Clinical and Experimental Neuropsychology, 22:3, 370-378
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                                                                     Journal of Clinical and Experimental Neuropsychology                               1380-3395/00/2203-370$15.00
                                                                     2000, Vol. 22, No. 3, pp. 370-378                                                          © Swets & Zeitlinger
                                                                                                                       ABSTRACT
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                                                                         Normative data for clustering and switching on verbal fluency tasks are provided. Four hundred and eleven
                                                                         healthy adults between the ages of 18 and 91 were given tests of phonemic fluency (FAS or CFL) and
                                                                         semantic fluency (Animals and Supermarket). Raw scores were corrected for demographic (i.e., age, edu-
                                                                         cation, and sex) and test (i.e., fluency form) variables that were determined to make sizable contributions
                                                                         to fluency performance. These normative data should be useful for clinicians and researchers in determin-
                                                                         ing the nature of the fluency impairment in any given individual.
                                                                     Tests of verbal fluency or word-list generation            fluency, and is thought to be a relatively auto-
                                                                     are frequently used in clinical and experimental           matic process. Switching involves cognitive
                                                                     examinations of cognitive function. The most               flexibility in shifting from one subcategory to
                                                                     commonly used score from verbal fluency tests              another and is a relatively effortful process.
                                                                     is the total number of words generated. How-                   These components of fluency performance
                                                                     ever, this score provides little information about         are differentially affected by various neurologi-
                                                                     the cognitive processes underlying fluency per-            cal disorders. Clustering is related to temporal-
                                                                     formance and does not answer the question as to            lobe functioning, as indicated by impaired per-
                                                                     why a particular patient group or experimental             formance among patients with temporal lobec-
                                                                     manipulation is associated with reduced test per-          tomy for intractable epilepsy (Troyer, Mos-
                                                                     formance. Additional information is needed to              covitch, Winocur, Alexander, & Stuss, 1998)
                                                                     examine the behavioral components that deter-              and patients with Alzheimer’s disease (Troyer,
                                                                     mine fluency performance.                                  Moscovitch, Winocur, Leach, & Freedman,
                                                                        Optimal fluency performance involves gener-             1998). Clustering is unaffected by focal frontal
                                                                     ating words within a subcategory and, when a               lesions (Troyer, Moscovitch, Winocur, Alexan-
                                                                     subcategory is exhausted, switching to a new               der, et al., 1998). Switching, on the other hand,
                                                                     subcategory. These behavioral components were              is related to frontal functioning. That is, switch-
                                                                     identified (Bousfield & Sedgewick, 1944; Grue-             ing is specifically impaired among patients with
                                                                     newald & Lockhead, 1980) and operationalized               left dorsolateral and superior medial frontal-lobe
                                                                     as clustering and switching, respectively                  lesions (Troyer, Moscovitch, Winocur, Alexan-
                                                                     (Troyer, Moscovitch, & Winocur, 1997). Clus-               der, et al., 1998) and is decreased under condi-
                                                                     tering involves phonemic analysis on phonemic              tions of divided attention (Troyer et al., 1997),
                                                                     fluency and semantic categorization on semantic            an experimental model of frontal dysfunction
                                                                     *
                                                                      Thanks to Morris Moscovitch and Kathryn Stokes for conceptual input and comments on the manuscript; Jill
                                                                     B. Rich, Nicole D. Anderson, and Don Stuss for the provision of fluency protocols; Malcolm Binns for statistical
                                                                     assistance; and Katy Kamkar for assistance with scoring and data entry.
                                                                     Address correspondence to: A. Troyer, Psychology Department, Baycrest Centre for Geriatric Care, 3560
                                                                     Bathurst Street, Toronto, ON, M6A 2E1, Canada. E-mail: a.troyer@utoronto.ca.
                                                                     Accepted for publication: October 19, 1999.
                                                                                                           NORMATIVE FLUENCY DATA                                         371
                                                                     (Moscovitch, 1994). Decreased switching is also      were required either to: (a) obtain scores of 25 or
                                                                     seen in patient groups with frontal dysfunction      higher on the Mini Mental Status Examination
                                                                     in the context of additional brain dysfunction,      (Folstein, Folstein, & McHugh, 1975), or (b) score
                                                                                                                          within the normal range on an episodic memory
                                                                     including Parkinson’s disease (Tröster et al.,
                                                                                                                          test (Anderson, Craik, & Naveh-Benjamin, 1998).
                                                                     1998; Troyer, Moscovitch, Winocur, Leach, et
                                                                     al., 1998), Huntington’s disease (Rich, Troyer,      Fluency Tasks
                                                                     Bylsma, & Brandt, 1999), multiple sclerosis           All testing was conducted in English. Each partic-
                                                                     (Tröster et al., 1998), and schizophrenia (Robert    ipant was administered three trials of a phonemic
                                                                     et al., 1998).                                       fluency task and one or two trials of a semantic
                                                                        Overall, research with these patient groups       fluency task. For phonemic fluency, participants
                                                                                                                          were given either the letters F, A, and S (n = 257)
                                                                     has consistently shown distinctions between pa-      or C, F, and L (n = 154). Consistent with standard
                                                                     tient groups with predominant temporal versus        instructions (e.g., Spreen & Strauss, 1998), partici-
                                                                     frontal dysfunction. Some inconsistencies have
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                                                                     ency, only phonemic clusters were counted, and on       sex-specific and age-specific names of the same
                                                                     semantic fluency, only semantic clusters were           animal species were considered to be the same ani-
                                                                     counted. The size of the cluster was counted begin-     mal (e.g., hen and rooster, cat and kitten). In order
                                                                     ning with the second word in each cluster. The          to provide consistency between the semantic flu-
                                                                     mean cluster size was calculated by summing the         ency tasks, on supermarket fluency, no credit was
                                                                     size of each cluster and dividing by the number of      given for subcategory labels (e.g., fruits) if spe-
                                                                     clusters. Switches were calculated as the number        cific exemplars were also given (e.g., apple, ba-
                                                                     of transitions between clusters, including single       nana).
                                                                     words. The number of switches, therefore, is the            On phonemic fluency, scores from the three tri-
                                                                     same as the number of clusters minus the number         als (i.e., F, A, and S, or C, F, and L) were com-
                                                                     of trials administered (e.g., three trials on phone-    bined into a single score for each participant. Simi-
                                                                     mic fluency and two trials on semantic fluency).        larly, on semantic fluency, scores on the two trials
                                                                        For several reasons, the raw number of switches      (i.e., Animals and Supermarket) were combined
                                                                     was chosen as the switching index rather than the       into a single variable. The benefit of these com-
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                                                                     number of switches corrected for number of words        bined scores is that they are based on a higher
                                                                     generated. Conceptually, the raw number of swit-        number of responses and are thus presumed to be
                                                                     ches is the behavior of interest, as it indicates the   more valid and reliable measures of fluency abil-
                                                                     number of times an individual can generate a new        ity. Because a large number of participants re-
                                                                     cluster of responses. This is similar to the raw in-    ceived animal but not supermarket fluency, animal
                                                                     dex used for the number of words generated.             scores alone were also retained.
                                                                     Knowing the percent of the words generated that
                                                                     were correct does not provide as much information
                                                                     as knowing the raw number of words generated            RESULTS
                                                                     (e.g., 90% could indicate 9 out of 10 or 36 out of
                                                                     40). As well, because switching is thought to deter-
                                                                     mine, in part, the number of words generated            Raw total mean scores obtained by the entire
                                                                     (Troyer et al., 1997), correcting switches for total    sample were 42.5 (SD = 11.7) for FAS and CFL,
                                                                     words generated would be tantamount to correct-         19.5 (SD = 5.3) for Animals, and 22.9 (SD =
                                                                     ing a cause for its effect. Another reason that raw     5.8) for Supermarket fluency. These scores are
                                                                     switches were used is because previous experience       consistent with previously published scores
                                                                     has indicated that a corrected switching score does
                                                                                                                             (e.g., Bolla, Lindgren, Bonaccorsy, & Bleecker,
                                                                     not produce meaningful information. No patient
                                                                     groups, including those with mild to moderate de-       1990; Kozora & Cullum, 1995; Spreen &
                                                                     mentia, have been found to be impaired in compar-       Strauss, 1998).
                                                                     ison to controls on a corrected switching score,           To determine the contributions of demo-
                                                                     despite large group impairments on other fluency        graphic and administrative factors to fluency
                                                                     measures (Troyer, 1997; Tröster et al., 1998).          performance, a series of regression equations
                                                                        Importantly, repetitions and intrusions were         was performed using age, education, sex, and
                                                                     included in calculations of cluster size and swit-
                                                                     ches because they provide information about the
                                                                                                                             phonemic-fluency test form (i.e., CFL or FAS)
                                                                     ongoing strategy. Any protocol on which the ex-         to predict cluster size, switches, and total words
                                                                     aminer failed to record repetitions or intrusions in    generated on the fluency tasks. Effect sizes (i.e.,
                                                                     the order in which they were generated was dis-         f; Cohen, 1988) based on the partial regression
                                                                     carded from the analyses (six protocols). This was      coefficients (Bs) were calculated to determine
                                                                     considered to be important because, otherwise,          which variables made meaningful contributions
                                                                     both clustering and switching would be under-           to fluency scores. According to Cohen (1988), fs
                                                                     reported in patient populations in which perse-
                                                                     verations are frequent.                                 of .10, .25, .40 correspond to small, medium,
                                                                        Repetitions and intrusions were excluded from        and large effect sizes, respectively.
                                                                     the number of correct words generated. On phone-
                                                                     mic fluency, consistent with the instructions given     Age
                                                                     to participants, proper names and repetitions of the    Age showed a small effect size as a predictor of
                                                                     same word with a different ending were also ex-         switching on phonemic fluency, B = 0.04, t =
                                                                     cluded. On animal fluency, no credit was given for
                                                                                                                             –2.05, p = .041, f = .10, and a large effect size as
                                                                     subcategory labels (e.g., bird) if specific exemplars
                                                                     were also given (e.g., robin, canary). In addition,     a predictor of switching on semantic fluency, B
                                                                                                             NORMATIVE FLUENCY DATA                                        373
                                                                     increasing age was associated with slightly             Generally, age, education, and fluency form (but
                                                                     larger cluster sizes and with reduced switches          not sex) were important predictors of fluency
                                                                     and words generated.                                    performance. Thus, regression analyses were
                                                                                                                             performed that included only these three predic-
                                                                     Education                                               tor variables. Corrections were then determined
                                                                     Number of years of formal education showed              by the B’s, and these corrections were applied to
                                                                     minimal to small effect sizes as a predictor of         the original scores in order to calculate norma-
                                                                     clustering on phonemic fluency, B = 0.015, t =          tive test data. The corrections are presented at
                                                                     3.34, p = .001, f = .17, semantic fluency, B =          the top of Table 1. Age and education correc-
                                                                     0.012, t = 0.75, p = .454, f = .06, and animal flu-     tions were applied for each year of age or formal
                                                                     ency, B = 0.024, t = 2.31, p = .021, f = .12. Edu-      education, respectively, and form corrections
                                                                     cation had a small effect size as a predictor of        were applied for FAS. Percentiles were then cal-
                                                                     switching on phonemic, B = 0.39, t = 2.53, p =          culated based on the actual distribution of the
                                                                     .012, f = .13, semantic, B = 0.25, t = 1.67, p =        corrected scores (e.g., 16% of participants in our
                                                                     .097, f = .14, and animal fluency, B = 0.17, t =        sample obtained scores at the 16th percentile or
                                                                     3.49, p = .001, f = .17. Education showed the           less). This method was chosen because some
                                                                     largest effect size (small to medium) as a predic-      score distributions (i.e., cluster size) were
                                                                     tor of total number of words generated, includ-         slightly skewed. Means, standard deviations,
                                                                     ing phonemic, B = 1.06, t = 5.06, p < .001, f =         and percentiles for the corrected scores are pre-
                                                                     .25, semantic, B = 0.74, t = 2.80, p = .006, f =        sented in the Table.
                                                                     .23, and animal fluency, B = 0.51, t = 6.12, p <           Percentiles for individual raw scores can be
                                                                     .001, f = .31. Higher levels of education were          obtained by adding any relevant corrections and
                                                                     always associated with better fluency perfor-           looking up the corresponding corrected score.
                                                                     mance.                                                  Consider, for example, a hypothetical 50-year-
                                                                                                                             old woman with 13 years of education. If she
                                                                     Sex                                                     produced a cluster size of 0.35 on FAS, her cor-
                                                                     Sex showed a minimal effect size as a predictor         rected score would be calculated as 0.35 +
                                                                     of every phonemic, semantic, or animal fluency          50(–.001) + 13 (–0.015) + 0.094 = 0.20. This
                                                                     variable, t’s = 0.08 to 1.25, p’s = .21 to .94, f’s =   places her at approximately the 50th percentile.
                                                                     .00 to .06, with the exception of a small effect        If this same individual generated a total of 35
                                                                     size on total number of words generated on se-          words on semantic fluency, her corrected score
                                                                     mantic fluency, B = –2.32, t = –1.55, p = .123, f       would be 35 + 50(0.23) + 13 (–0.74) = 36.8,
                                                                     = .13.                                                  which places her between the 5th and 16th per-
                                                                                                                             centiles.
                                                                     374                                             ANGELA K. TROYER
Table 1. Corrections, Demographically Corrected Descriptive Data, and Percentiles for Fluency Scores.
                                                                     Age (years)            –0.001      +0.05    +0.04       –0.001     +0.11      +0.23      –0.002   +0.05       +0.09
                                                                     Education (years)      –0.015      –0.38    –1.06       –0.012      –0.25      –0.74     –0.023    –0.17       –0.51
                                                                     Form (FAS)             +0.094      –2.67    –2.18      NA          NA         NA        NA        NA          NA
                                                                     Mean                    0.24       23.9      28.6        0.94      23.4       46.9        0.75          9.8   18.1
                                                                     SD                      0.23        8.2      11.1        0.47       4.4        7.9        0.57          2.7    4.6
                                                                     1st percentile         –0.16        6.6       4.3        0.24      13.4       28.3       –0.24      3.9        8.3
                                                                     5th percentile         –0.06       10.2      11.4        0.40      16.2       34.4        0.01      5.8       10.9
                                                                     16th percentile         0.01       15.6      17.0        0.60      18.9       39.4        0.23      7.3       13.5
                                                                     25th percentile         0.08       18.7      20.6        0.66      20.5       40.7        0.40      7.9       14.9
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                                                                     50th percentile         0.19       23.3      28.7        0.91      22.7       46.3        0.64      9.6       17.9
                                                                     75th percentile         0.35       29.7      36.6        1.18      26.5       52.5        1.12     11.6       21.2
                                                                     84th percentile         0.44       32.3      39.3        1.44      27.5       56.6        1.39     12.4       22.8
                                                                     95th percentile         0.73       37.6      47.6        2.02      31.3       60.7        1.89     14.7       26.7
                                                                     99th percentile         0.97       43.2      57.4        2.37      34.0       62.4        2.43     16.7       29.3
                                                                     cation was associated with more switches and         centile) fluency. This pattern is not consistent
                                                                     more words generated on animal fluency. In this      with Alzheimer’s disease, and instead implicates
                                                                     case, more frequent switching presumably re-         frontal dysfunction, perhaps related to vascular
                                                                     sulted in more words generated. Thus, both clus-     or frontal dementia. Indeed, vascular dementia
                                                                     tering and switching are necessary to account for    was the most likely diagnosis for LS, given her
                                                                     variations in the number of words generated.         history (stable impairment over the last year)
                                                                         The usefulness of these fluency scores in as-    and brain imaging (periventricular white matter
                                                                     sessment and diagnosis can be demonstrated           changes on CT). Thus, an examination of clus-
                                                                     with the following sample patient profiles. SR is    tering and switching scores may be useful in
                                                                     a 56-year-old woman with a university-level          discriminating between different causes of cog-
                                                                     education and a one- to two-year history of          nitive impairment.
                                                                     memory decline. A comparison of her demo-
                                                                     graphically-corrected fluency component scores
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                                                                     Lacy, M. A., Gore Jr., P. A., Pliskin, N. H., Henry, G.    Tröster, A. I., Fields, J. A., Testa, J. A., Paul, R. H.,
                                                                        K., Heilbronner, R. L., & Hamer, D. P. (1996).             Blanco, C. R., Hames, K. A., Salmon, D. P., &
                                                                        Verbal fluency task equivalence. The Clinical Neu-         Beatty, W. W. (1998). Cortical and subcortical in-
                                                                        ropsychologist, 10, 305-308.                               fluences on clustering and switching in the perfor-
                                                                     Mattis, S. (1988). Dementia Rating Scale. Odessa, FL:         mance of verbal fluency tasks. Neuropsychologia,
                                                                        Psychological Assessment Resources.                        36, 295-304.
                                                                     McKhann, G., Drachmann, D., Folstein, M., Katzman,         Tröster, A. I., Salmon, D. P., McCullough, D., & But-
                                                                        R., Price, D., & Stadlan, E. M. (1984). Clinical           ters, N. (1989). A comparison of the category flu-
                                                                        diagnosis of Alzheimer’s disese. Neurology, 34,            ency deficits associated with Alzheimer’s and
                                                                        939-944.                                                   Huntington’s disease. Brain and Language, 37,
                                                                     Moscovitch, M. (1994). Cognitive resources and dual-          500-513.
                                                                        task interference effects at retrieval in normal peo-   Troyer, A. K. (1997). [Alternate indices of verbal flu-
                                                                        ple: The role of the frontal lobes and medial tem-         ency clustering and switching]. Unpublished raw
                                                                        poral cortex. Neuropsychology, 8, 524-534.                 data.
                                                                     Rich, J. B., Troyer, A. K., Bylsma, F. W., & Brandt, J.    Troyer, A. K., Moscovitch, M., & Winocur, G.
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                                                                        (1999). Longitudinal analysis of phonemic cluster-         (1997). Clustering and switching as two compo-
                                                                        ing and switching during word list generation in           nents of verbal fluency: Evidence from younger
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                                                                        531.                                                       138-146.
                                                                     Robert, P. H., Lafont, V., Medecin, I., Berthet, L.,       Troyer, A. K., Moscovitch, M., Winocur, G., Alexan-
                                                                        Thauby, S., Baudu, C., & Darcourt, G. (1998).              der, M. P., & Stuss, D. (1998). Clustering and
                                                                        Clustering and switching strategies in verbal flu-         switching on verbal fluency: The effects of focal
                                                                        ency tasks: Comparison between schizophrenic and           frontal- and temporal-lobe lesions. Neuropsy-
                                                                        healthy subjects. Journal of the International Neu-        chologia, 36, 449-504.
                                                                        ropsychological Society, 4, 539-546.                    Troyer, A. K., Moscovitch, M., Winocur, G., Leach,
                                                                     Spreen, O., & Strauss, E. (1998). A compendium of             L., & Freedman, M. (1998). Clustering and switch-
                                                                        neuropsychological tests: Administration, norms,           ing on verbal fluency tests in Alzheimer’s and Par-
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                                                                                                          NORMATIVE FLUENCY DATA                                        377
APPENDIX
                                                                     Phonemic fluency
                                                                     Clusters on phonemic fluency trials consisted of successively generated words which shared any of
                                                                     the following phonemic characteristics:
                                                                        First letters: words beginning with same first two letters, such as ‘‘arm’’ and ‘‘art’’
                                                                        Rhymes: words that rhyme, such as ‘‘sand’’ and ‘‘stand’’
                                                                        First and last sounds: words differing only by a vowel sound, regardless of the actual spelling,
                                                                     such as ‘‘sat,’’ ‘‘seat,’’ ‘‘soot,’’ ‘‘sight,’’ and ‘‘sought’’
                                                                        Homonyms: words with two or more different spellings, such as ‘‘some’’ and ‘‘sum,’’ as indicated
                                                                     by the participant
                                                                     Semantic fluency
                                                                     Clusters on semantic fluency trials consisted of successively generated words belonging to the same
                                                                     subcategories, as specified below. Commonly generated examples are listed for each subcategory,
                                                                     although listings are not exhaustive.
                                                                     Animals
                                                                        African animals: aardvark, antelope, buffalo, camel, chameleon, cheetah, chimpanzee, cobra,
                                                                     eland, elephant, gazelle, giraffe, gnu, gorilla, hippopotamus, hyena, impala, jackal, lemur, leopard,
                                                                     lion, manatee, mongoose, monkey, ostrich, panther, rhinoceros, tiger, wildebeest, warthog, zebra
                                                                        Australian animals: emu, kangaroo, kiwi, opossum, platypus, Tasmanian devil, wallaby, wombat
                                                                        Arctic/Far North animals: auk, caribou, musk ox, penguin, polar bear, reindeer, seal
                                                                        Farm animals: chicken, cow, donkey, ferret, goat, horse, mule, pig, sheep, turkey
                                                                        North America animals: badger, bear, beaver, bobcat, caribou, chipmunk, cougar, deer, elk, fox,
                                                                     moose, mountain lion, puma, rabbit, raccoon, skunk, squirrel, wolf
                                                                        Water animals: alligator, auk, beaver, crocodile, dolphin, fish, frog, lobster, manatee, muskrat,
                                                                     newt, octopus, otter, oyster, penguin, platypus, salamander, sea lion, seal, shark, toad, turtle, whale
                                                                        Beasts of burden: camel, donkey, horse, llama, ox
                                                                        Animals used for their fur: beaver, chinchilla, fox, mink, rabbit
                                                                        Pets: budgie, canary, cat, dog, gerbil, golden retriever, guinea pig, hamster, parrot, rabbit
                                                                        Birds: budgie, condor, eagle, finch, kiwi, macaw, parrot, parakeet, pelican, penguin, robin, toucan,
                                                                     woodpecker
                                                                        Bovine: bison, buffalo, cow, musk ox, yak
                                                                        Canine: coyote, dog, fox, hyena, jackal, wolf
                                                                        Deers: antelope, caribou, eland, elk, gazelle, gnu, impala, moose, reindeer, wildebeest
                                                                        Feline: bobcat, cat, cheetah, cougar, jaguar, leopard, lion, lynx, mountain lion, ocelot, panther,
                                                                     puma, tiger
                                                                     378                                        ANGELA K. TROYER
                                                                     Supermarket Items
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                                                                     Note. From ‘‘Clustering and switching as two components of verbal fluency: Evidence from younger
                                                                     and older healthy adults,’’ by A. K. Troyer, M. Moscovitch, & G. Winocur, 1997, Neuropsychology,
                                                                     11, p. 145-146. Copyright 1997 by the American Psychological Association. Adapted by permission
                                                                     of the publisher.