Journal of Clinical and Experimental Neuropsychology

ISSN: 1380-3395 (Print) 1744-411X (Online) Journal homepage: https://www.tandfonline.com/loi/ncen20

Lexical, Semantic, and Action Verbal Fluency in

Parkinson's Disease with and without Dementia

Andrea L. Piatt , Julie A. Fields , Anthony M. Paolo , William C. Koller &

Alexander I. Tröster

To cite this article: Andrea L. Piatt , Julie A. Fields , Anthony M. Paolo , William C. Koller &
Alexander I. Tröster (1999) Lexical, Semantic, and Action Verbal Fluency in Parkinson's Disease
with and without Dementia, Journal of Clinical and Experimental Neuropsychology, 21:4, 435-443,
DOI: 10.1076/jcen.21.4.435.885

To link to this article: https://doi.org/10.1076/jcen.21.4.435.885

Published online: 09 Aug 2010.

Submit your article to this journal

Article views: 567

View related articles

Citing articles: 18 View citing articles

Full Terms & Conditions of access and use can be found at

https://www.tandfonline.com/action/journalInformation?journalCode=ncen20
Journal of Clinical and Experimental Neuropsychology 1380-3395/99/2104-435$15.00
1999, Vol. 21, No. 4, pp. 435-443 © Swets & Zeitlinger

Lexical, Semantic, and Action Verbal Fluency in Parkinson’s

Disease with and without Dementia*
Andrea L. Piatt, Julie A. Fields, Anthony M. Paolo, William C. Koller, and Alexander I. Tröster
Department of Neurology, University of Kansas Medical Center, Kansas City

ABSTRACT

Previous research suggests that lexical and semantic verbal fluency are differentially sensitive to the effects
of cortical and subcortical dementias, but little is known about action fluency performance in dementias.
The present study compared lexical, semantic, and action fluency in groups of patients with Parkinson’s
disease (PD) with and without dementia and an elderly control group. Findings revealed an interaction
between fluency type and subject group. Although the demented PD (PDD) group performed significantly
more poorly than their non-demented counterparts and normal controls on all three fluency tasks, a dispro-
portionate disparity in scores was noted on the action fluency task. The findings suggest that action fluency
may be particularly sensitive to PD-associated dementia and may be an early indicator of the conversion
from PD to PDD. As reported elsewhere, PD without dementia was not associated with significant impair-
ment on any of the fluency tasks.

Verbal fluency tasks have been frequently em-
ployed as indicators of semantic memory func-
tioning in cortical and subcortical dementias.
Prior research suggests that lexical and semantic
verbal fluency tasks are differentially sensitive
to the effects of cortical (e.g., Alzheimer’s dis-
ease [AD]) and subcortical (e.g., Huntington’s
disease [HD], and Parkinson’s disease [PD])
dementias (Barr & Brandt, 1996; Monsch et al.,
1992). Whereas letter fluency is disproportio-
nately impaired in HD, semantic fluency is di-
minished to a greater extent than letter fluency
in AD (Butters, Granholm, Salmon, Grant, &
Wolfe, 1987). This finding is consistent with the
putative cognitive demands of the verbal fluency
tasks, and the most prominent locus of neuropa-
thology in HD and AD. Butters et al. (1987) pro-
posed that letter fluency places greater demands
on the initiation and maintenance of systematic
retrieval strategies than does semantic fluency.
Thus, letter fluency tasks might be reasonably
expected to be more sensitive to HD and
frontostriatal pathology than semantic fluency
tasks. Given the critical importance of the tem-
poral lobes in semantic fluency (Fink & Ran-
dolph, 1998), and the early involvement of the
temporal lobes by AD, it is not surprising that
AD, even early in its course, is associated with
semantic fluency deficits (e.g., Hodges, Salmon,
& Butters, 1990; Martin & Fedio, 1983; Tröster,
Salmon, McCullough, & Butters, 1989).
It has been proposed that many of the cogni-
tive deficits observed in PD reflect difficulties
with the initiation and execution of internally
guided information processing strategies which
are related to cortico-striatal-thalamo-cortical
loop pathophysiology (Taylor & Saint-Cyr,
1995; Tröster & Fields, 1995). Consequently
one might expect the pattern of verbal fluency
deficits in PD to parallel those observed in HD.
To date, however, findings of verbal fluency
deficit patterns in PD have been inconsistent.

*
Andrea L. Piatt is now at Department of Psychiatry and Human Behavior, Brown University School of Medi-
cine, Providence, RI.
Address correspondence to: Alexander I. Tröster, Department of Neurology, University of Kansas Medical
Center, 3901 Rainbow Boulevard, Kansas City, KS 66160-7314, USA. E-mail: atroster@kumc.edu
Accepted for publication: February 17, 1999.
436 ANDREA L. PIATT ET AL.
Inconsistent results of studies evaluating lexical
and semantic fluency in patients with PD might
reflect differential difficulty of fluency tasks
(see Azuma et al., 1997) and varying or un-
known severity of general cognitive decline
among patient samples. For example, Gurd and
Ward (1989) identified both lexical and seman-
tic fluency deficits in a sample of PD patients,
but no information regarding the overall level of
cognitive functioning of the subjects was pro-
vided. Similarly, Matison, Mayeux, Rosen and
Fahn (1982) reported categorical verbal fluency
deficits, but preserved letter fluency in their
sample of PD patients. However, while they
state that their subjects were not demented based
on clinical and examination data, they appar-
ently did not employ a formal measure of overall
cognitive status. As such, the actual mental sta-
tus of their subjects is unclear. Based on studies
that have identified a relationship between men-
tal status and verbal fluency in both AD and PD
patients (Appell, Kertesz, & Fisman, 1982;
Azuma et al., 1997; Martin & Fedio, 1983),
evaluation of mental status is central to verbal
fluency studies with these populations.
Even among studies employing samples free
of significant cognitive decline, findings are still
notably inconsistent. Some studies have reported
no lexical or semantic fluency deficits among
cognitively intact PD subjects relative to control
subjects (Beatty & Monson, 1989; Hanley,
Dewick, Davies, Playfer, & Turnbull, 1990;
Tröster et al., 1998), whereas others have identi-
fied deficits in both lexical and semantic fluency
in PD subjects (Bayles, Trosset, Tomoeda,
Montgomery, & Wilson, 1993; Flowers, Robert-
son, & Sheridan, 1996). Still others have identi-
fied deficient semantic fluency but preserved
lexical fluency (Auriacombe et al., 1993; Beatty
& Monson, 1989; Raskin, Sliwinski, & Borod,
1992). It might be that PD patients’ retrieval
difficulties, when present, can affect both lexical
and semantic fluency tasks (e.g., Randolph,
Braun, Goldberg, & Chase, 1993).
Despite the volume of research on lexical and
semantic fluency in PD, action fluency (i.e., the
spontaneous production of verbs) has not been
examined in this population, and no studies have
compared action fluency with lexical and/or cat-
egorical fluency in Parkinson’s disease or other
diseases associated with fronto-subcortical neu-
ropathology such as Huntington’s disease. This
seems somewhat surprising given both the
known fronto-striatal pathophysiology of Par-
kinson’s disease and clinical evidence suggest-
ing a relationship between verb retrieval and
frontal lobe functioning.
Although imaging studies reveal the widely
distributed nature of neural networks involved in
verbal fluency, during the past two decades, re-
searchers have suggested that noun and verb
retrieval abilities are mediated by different (al-
though perhaps overlapping) neuroanatomical
circuits, with verb retrieval being most strongly
mediated by prefrontal networks and noun re-
trieval being based predominantly within tempo-
ral-parietal neural circuitry (Caramazza &
Hillis, 1991; Damasio & Tranel, 1993; McCar-
thy & Warrington, 1985; Miceli, Silveri, Villa,
& Caramazza, 1984; Zingeser & Berndt, 1990).
According to Grossman (1998), verb naming
deficits may reflect underlying executive system
dysfunction that undermines the ability to men-
tally coordinate and manipulate the diverse
range of information that may be associated with
a verb, a hypothesis borne out in the literature.
For example, based on lesion data from four
subjects, Damasio and Tranel (1993) concluded
that patients with frontal lobe injury demonstrate
notable difficulty with verb production, but re-
trieve nouns at normal levels. In contrast, pa-
tients with more posterior lesions demonstrated
the opposite pattern of preserved verb retrieval
in the presence of poor noun generation. Based
on this double-dissociation, they asserted that
verb retrieval is mediated by the frontal regions,
whereas noun retrieval is mediated by the domi-
nant, anterior temporal lobe. Similarly, in a
study involving patients with aphasia syndromes
suggestive of neuroanatomical dysfunction in
frontal (agrammatic aphasics) and temporal
(anomic aphasics) regions, Miceli et al. (1984)
found that agrammatic aphasics demonstrated
notable deficits in verb production, despite pres-
ervation of noun retrieval. In contrast, the
anomic aphasic subjects demonstrated greater
difficulty with noun retrieval in comparison to
verb production. In a recent study of patients
 VERBAL FLUENCY IN PARKINSON’S DISEASE
with Alzheimer’s disease, and presumably pre-
dominant parietal-temporal pathology, William-
son et al. (1998) found that object naming was
more severely impaired than action naming,
even once the effect of word frequency was con-
trolled for. Although these and other studies
(Caramazza & Hillis, 1991; Daniele, Giustolisi,
Silveri, Colosimo, & Gainotti, 1994; McCarthy
& Warrington, 1985; Zingeser & Berndt, 1990)
support the hypothesized differential neuroana-
tomic substrates of noun and verb retrieval, this
dissociation is not always supported by func-
tional imaging (PET) studies. While some PET
studies have suggested that verb fluency relies
heavily on the dominant temporal and parietal
regions (see Warburton et al., 1996), others im-
plicate the left prefrontal cortex, particularly the
dorsolateral aspect, in action word naming
(Martin, Haxby, Lalonde, Wiggs, & Unger-
leider, 1995).
Given that frontal regions might be critically
involved in action fluency, and given the fronto-
striatal pathophysiology of PD, the present study
was undertaken to compare lexical, semantic,
and action fluency abilities in PD patients with
and without dementia. Based on the fronto-sub-
cortical pathophysiology of PD, it was antici-
pated that action fluency, if indeed heavily reli-
ant on the integrity of frontal lobe circuitry,
would be diminished in the PD patients relative
to age- and education-matched peers. Further, it
was hypothesized that action fluency would
demonstrate greater sensitivity to PD than either
semantic or lexical fluency tasks, particularly as
the disease progressed.
METHOD
Participants
Subjects consisted of 59 healthy elderly control
subjects (NC), 57 Parkinson’s disease patients
without dementia (PDND), and 20 Parkinson’s
disease patients with dementia (PDD). Seventy-
five subjects (55%) were male, whereas 61 sub-
jects (45%) were female. All subjects were re-
cruited as patients or caregivers enrolled in studies
at the Neurodegenerative Disease Research Center
at the University of Kansas Medical Center. Con-
trol subjects were free of histories of neurologic
437
disease/injury and psychiatric illness. Parkinson’s
disease was diagnosed by a staff neurologist on the
basis of two of three cardinal signs (bradykinesia,
rigidity, and tremor) and levo-dopa responsive-
ness. Dementia in PD was defined on the basis of
impairment in at least two of four cognitive do-
mains (language, memory, executive function,
visuoperceptual function). Impairment in a given
domain was defined by a score below age-appro-
priate cutoff or the fifth percentile on at least one
of two tests of that cognitive domain. To minimize
inclusion of patients with concomitant Alzheimer’s
and Parkinson’s disease or Lewy body variant of
Alzheimer’s disease, motor symptoms had to pre-
cede any cognitive deficit in PD patients with de-
mentia. Further, as indicated in Table 1, the PDND
subjects performed significantly better on mea-
sures of overall cognitive functioning, learning and
memory, and visual confrontation naming, sup-
porting the cognitive distinction between the two
groups of subjects. All PD patients were taking
anti-Parkinsonian medications at the time of test-
ing. Patients with motor fluctuations were tested
while in their ‘‘on state’’. All PD patients were
free of other neurologic disorder and major psychi-
atric illness, excepting mild depression which is
common in PD. None of the participants had histo-
ries of significant head injury with loss of con-
sciousness, substance abuse or dependence, or
self-reported specific developmental disorders. All
subjects underwent comprehensive interviews,
neuropsychological testing, and neurologic exami-
nations.
The three groups were matched for age and edu-
cation. Additionally, the NC and PDND groups
were matched for total Dementia Rating Scale
(DRS; Mattis, 1988) score.
Materials and Procedures
As part of a larger test battery, subjects were ad-
ministered the DRS (Mattis, 1988) in standard
fashion. The Controlled Oral Word Association
Test (FAS; Spreen & Benton, 1969, 1977) was also
standardly administered. Since the FAS task was
based on a 3-min word generation period, the total
score for this task was divided by three in order to
compare raw production scores across the three
fluency tasks. The Animal Naming task from the
Boston Diagnostic Aphasia Examination (BDAE;
Goodglass & Kaplan, 1987) was utilized to evalu-
ate semantic fluency. This task required subjects to
orally generate the names of as many different ani-
mals as they could in a 60-s period. The total score
for this task was the total number of correct items
produced. Instructions for the Action Fluency task
were as follows: ‘‘I’d like you to tell me as many
 438
Table 1. Demographic Data and Test Results.

NC PDND PDD F(2,135)

(n = 59) (n = 57) (n = 20)

M (SD) M (SD) M (SD)

Age 72.86 (7.51) 70.30 (6.64) 73.90 (6.36) 2.27
Education 14.40 (2.14) 14.45 (2.96) 14.25 (3.24) 0.04
DRS Total (/144) 137.20 (6.31) 135.91 (6.40) 116.25 (14.48) 52.38***a
FAS (words/min) 12.05 (3.54) 11.78 (3.96) 7.47 (3.92) 11.82***a
Animal Naming (words/min) 17.49 (4.61) 17.12 (4.44) 10.85 (5.15) 16.95***a
Action Fluency (words/min) 15.14 (4.33) 14.28 (5.14) 7.30 (3.36) 22.48***a
CVLT Total (/80) 41.61 (11.02) 29.95 (9.48) 30.74***b
CVLT Long-delay Free Recall (/16) 8.42 (3.83) 3.21 (2.07) 31.84***b
CVLT Recognition Hits (/16) 14.12 (1.60) 13.95 (1.96) 0.15
24.56***b

ANDREA L. PIATT ET AL.

Boston Naming Test (/60) 55.37 (3.73) 49.21 (6.87)

Note. NC = normal controls; PDND = Parkinson’s disease without dementia; PDD = Parkinson’s disease with dementia; DRS = Dementia Rating Scale; FAS =
Controlled Oral Word Association Test; CVLT = California Verbal Learning Test.
a
PDD < PDND = NC.
b
PDD < PDND
***p .001
 VERBAL FLUENCY IN PARKINSON’S DISEASE
different things as you can think of that people do.
I don’t want you to use the same word with differ-
ent endings, like eat, eating, eaten. Also, just give
me single words such as eat, or smell, rather than a
sentence. Can you give me an example of some-
thing that people do?’’ (Any verb response is ac-
ceptable) If the response is acceptable: ‘‘That’s the
idea. Now in one minute, tell me as many different
things as you can think of that people do.’’ The
score for this task was the total number of items
correctly produced in a 60-s period. In addition,
Parkinson’s disease patients (demented and non-
demented) were administered the California Ver-
bal Learning Test (CVLT; Delis, Kramer, Kaplan,
& Ober, 1987) and the Boston Naming Test (BNT;
Kaplan, Goodglass, & Weintraub, 1983) in the
standard manner.
RESULTS
Sample characteristics and scores (mean and
standard deviation) for the three verbal fluency
measures for each subject group are presented in
Table 1. Additionally, data regarding episodic
memory and visual confrontation naming for the
two Parkinson’s disease groups are presented in
Table 1. To determine whether gender influ-
enced any of the verbal fluency scores or inter-
acted with group membership, a two-way
MANOVA with group membership (NC,
PDND, and PDD) and gender serving as inde-
pendent variables and the three verbal fluency
tasks serving as dependent measures was con-
ducted. Results indicated no significant main
effect for gender [F(1,130) = 1.49, p = .23] and
no interaction between gender and group mem-
bership [F(2, 130) = .42, p = .66]. As such, data
for men and women were combined for all sub-
sequent analyses. To assess the differential diffi-
culty of the three fluency tasks and possible dif-
ferences among subject group’s performances
on the three fluency tasks, a 3 (fluency task) × 3
(group) Multivariate Analysis of Variance was
conducted with group membership (NC, PDND,
PDD) serving as the between subjects factor and
fluency task serving as the within subjects fac-
tor. Results revealed a significant between
groups effect, F(2,133) = 24.71, p < .01. Follow-
up comparisons using Tukey’s HSD test indi-
cated that the PDD group performed signifi-
439
cantly (p < .00) more poorly on all three fluency
measures relative to the NC and PDND group.
The NC and PDND groups did not differ on any
of the fluency tests (see Table 1). Within sub-
jects analyses revealed a significant main effect
for fluency task, F(2,132) = 74.84, p < .01, as
well as a significant group by fluency task inter-
action, F(4,262) = 2.81, p < .05. Paired-sample
t-tests revealed that, overall, the semantic flu-
ency task was easier than the action fluency task
[t(135) = 6.99, p < .01], which in turn was easier
than the letter fluency task [t(135) = 6.74, p <
.01]. Of note, however, is a significant interac-
tion effect (see Fig. 1). Specifically, the action
fluency task was slightly more difficult than the
letter fluency task for the PDD group. Although
the PDD group performed more poorly on all
three fluency measures relative to the NC and
PDND group (see Table 1), the action fluency
task was differentially more difficult for the
PDD group than either the lexical or semantic
fluency tasks relative to the NC and PDND
groups.
To evaluate whether or not the apparent diffi-
culty of action fluency in the PDD group simply
reflects sensitivity to dementia rather than to
fronto-subcortical compromise, a Pearson prod-
uct moment correlation was computed for DRS
scores. Since the DRS partly is comprised of a
semantic fluency task (supermarket fluency), the
raw supermarket fluency scores were subtracted
from the total DRS scores for this analysis. The
findings indicated a marginally significant rela-
tionship between lexical verbal fluency and DRS
scores (r = .43, p = .06) and a trend toward a
significant relationship between semantic verbal
fluency and DRS scores (r = .40, p = .08). No
significant or marginal relationship was ob-
served between action fluency scores and DRS
scores (r = .34, p = .14).
DISCUSSION
As hypothesized, there was a significant interac-
tion between the type of fluency task utilized
and diagnostic group. Although the PDD group
performed significantly more poorly on all three
of the verbal fluency measures relative to their
440 ANDREA L. PIATT ET AL.
Fig. 1. Interaction between fluency type and subject group: Mean number of words produced.
non-demented counterparts and normal control
subjects, action fluency was differentially more
difficult for the PDD subjects than for the other
two subject groups. As Figure 1 indicates, action
fluency was not the most difficult task for the
NC and PDND subjects, arguing against the pos-
sibility that the action fluency impairment in
PDD simply reflects greater task difficulty in
general. Given the lack of association between
action fluency scores and DRS scores within the
PDD group, action fluency appears to be sensi-
tive to the progressive fronto-subcortical dys-
function of Parkinson’s disease rather than to
overall severity of cognitive impairment in gen-
eral. Given the presence of marginal and trend
relationships between lexical and semantic flu-
ency scores and DRS performance (minus super-
market fluency scores) in the PDD sample, these
fluency tasks may be sensitive to the overall
cognitive decline in PD, but not necessarily spe-
cific to the frontostriatal pathophysiology of PD.
This hypothesis is consistent with the findings
of Tröster et al. (1998) who identified a signifi-
cant relationship between lexical and semantic
fluency and severity of dementia in Parkinson’s
disease patients.
Consistent with other reports (Beatty &
Monson, 1989; Hanley et al., 1990), the PDND
group did not differ from an age and education
matched control group on any of the fluency
tasks, suggesting that action fluency is not sensi-
tive to the early pathophysiological changes of
PD. Given that differences in fluency perfor-
mance between PDND and PDD are most appar-
ent on the action fluency task, there is sugges-
tion that action fluency may be an early indica-
tor of the conversion from PD to PD with asso-
ciated dementia. As the present study employed
a cross-sectional design this possibility could
not be directly assessed, and future studies uti-
lizing longitudinal approaches will be needed to
address this issue adequately. However, the po-
tential utility of verbal fluency tasks in detecting
dementia in PD is supported by Jacobs et al.’s
(1995) and Mahieux et al.’s (1998) longitudinal
findings indicating that verbal fluency tasks are
 VERBAL FLUENCY IN PARKINSON’S DISEASE
significantly and independently associated with
incident dementia.
Overall, the current findings support earlier
studies that have linked verb generation abilities
to neuroanatomic underpinnings that are distinct
(but perhaps overlapping) from those mediating
retrieval of lexical and semantic information
(Caramazza & Hillis, 1991; Damasio & Tranel,
1993; McCarthy & Warrington, 1985; Miceli et
al., 1984; Zingeser & Berndt, 1990). We con-
tend that diminished action verbal fluency, per-
haps to a greater extent than lexical and seman-
tic fluency impairments, reflect the frontostriatal
neuropathology and/or neurochemical deteriora-
tion known to occur with the progression of Par-
kinson’s disease (Braak & Braak, 1990; Forno,
1992, 1996; Kopin & Markea, 1988). This hy-
pothesis is consistent with recent literature indi-
cating that such frontal lobe functions as work-
ing memory decline with disease progression
(see Owen, Sahakian, & Robbins, 1998). Indirect
support that action fluency might be mediated
predominantly by frontal regions comes from
the observation that action fluency was not sig-
nificantly related to dementia severity in PDD,
yet recent neuropathologic evidence indicates
that dementia severity in PD, even in the absen-
ce of Alzheimer’s disease pathology at autopsy,
might be related to hippocampal pathology
(Churchyard & Lees, 1997). Consequently, se-
mantic and letter fluency might be more strongly
related to dementia severity by virtue of relying
on temporal circuits to a greater extent than ac-
tion fluency. Action fluency, on the other hand,
may be less dependent on these temporal cir-
cuits. One might speculate that as the well
known frontal-subcortical pathophysiology in
PD reaches a certain threshold (but shortly be-
fore overt dementia is clinically apparent), more
pronounced action than letter or semantic flu-
ency impairments become observable. As de-
mentia becomes clinically evident, and perhaps
temporal/hippocampal pathologic load increa-
ses, letter and semantic fluency deficits increase.
It must be noted that this interpretation is com-
plicated by the fact that the neuropathology of
PD dementia is heterogeneous. Although up to
35% of cases of PD with dementia have Alzhei-
mer’s disease pathology, dementia can be ob-
441
served in the absence of Alzheimer’s disease
pathology, and even in the absence of cortical
pathology (for review, see Tröster, Fields, &
Koller, in press). It remains to be established
whether verbal fluency tasks are differentially
affected in neuropathologically distinct cases of
Parkinson’s disease dementia. Nonetheless, the
current findings suggest that action fluency
might be useful in detecting dementia in the ear-
liest stages in PD patients, at least as a group.
Additional research with other clinical popula-
tions (e.g., HD, frontal lesions) will be neces-
sary to further support the clinical utility of ac-
tion fluency as an indicator of frontal lobe func-
tioning.
REFERENCES
Appell, J., Kertesz, A., & Fisman, M. (1982). A study
of language functioning in Alzheimer’s patients.
Brain and Language, 17, 73-91.
Auriacombe, S., Grossman, M., Carvell, S., Stern, M.
B., & Hurtig, H. I. (1993). Verbal fluency deficits
in Parkinson’s disease. Neuropsychology, 7, 182-
192.
Azuma, T., Bayles, K.A., Cruz, R.F., Tomoeda, C.K.,
Wood, J.A., McGeagh, A., & Montgomery, E.B.
(1997). Comparing the difficulty of letter, seman-
tic, and name fluency tasks for normal elderly and
patients with Parkinson’s disease. Neuropsychol-
ogy, 11, 488-497.
Barr, A., & Brandt, J. (1996). Word-list generation
deficits in dementia. Journal of Clinical and Ex-
perimental Neuropsychology, 18, 810-822.
Bayles, K.A., Trosset, M.W., Tomoeda, C.K., Mont-
gomery, E.B., & Wilson, J. (1993). Generative
naming in Parkinson’s disease patients. Journal of
Clinical and Experimental Neuropsychology, 15,
547-562.
Beatty, W.W., & Monson, N. (1989). Lexical process-
ing in Parkinson’s disease and multiple sclerosis.
Journal of Geriatric Psychiatry and Neurology, 2,
145-152.
Braak, H., & Braak, E. (1990). Cognitive impairment
in Parkinson’s disease: Amyloid plaques, neuro-
fibrillary tangles and neuropil threads in the cere-
bral cortex. Journal of Neural Transmission, 2, 45-
57.
Butters, N., Granholm, E., Salmon, D.P., Grant, I., &
Wolfe, J. (1987). Episodic and semantic memory:
A comparison of amnesic and demented patients.
Journal of Clinical and Experimental Neuropsy-
chology, 9, 479-497.
442 ANDREA L. PIATT ET AL.
Caramazza, A., & Hillis, A.E. (1991). Lexical organi-
zation of nouns and verbs in the brain. Nature, 349,
788-790.
Churchyard, A., & Lees, A.J. (1997). The relationship
between dementia and direct involvement of the
hippocampus and amygdala in Parkinson’s disease.
Neurology, 49, 1570-1576.
Cummings, J.L., & Benson, D.F. (1983). Dementia: A
clinical approach. Boston: Butterworths.
Damasio, A., & Tranel, D. (1993). Nouns and verbs
are retrieved with differently distributed neural
systems. Proceedings of the National Academy of
Science, USA, 90, 4957-4960.
Daniele, A., Giustolisi, L., Silveri, M.C., Colosimo,
C., & Gainotti, G. (1994). Evidence for a possible
neuroanatomical basis for lexical processing of
nouns and verbs. Neuropsychologia, 32, 1325-
1341.
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A.
(1987). The California Verbal Learning Test. New
York: Psychological Corporation.
Fink, J.W., & Randolph, C. (1998). Semantic memory
in neurodegenerative disease. In A.I. Tröster (Ed.),
Memory in neurodegenerative disease: Biological,
cognitive, and clinical perspectives (pp. 197-209).
Cambridge, UK: Cambridge University Press.
Flowers, K.A., Robertson, C., & Sheridan, M.R.
(1996). Some characteristics of word fluency in
Parkinson’s disease. Journal of Neurolinguistics, 9,
33-46.
Forno, L.S. (1992). Neuropathologic features of Par-
kinson’s, Huntington’s and Alzheimer’s diseases.
Annals of the New York Academy of Sciences, 648,
6-16.
Forno, L.S. (1996). Neuropathology of Parkinson’s
disease. Journal of Neuropathology and Experi-
mental Neurology, 55, 259-272.
Goodglass, H., & Kaplan, E. (1987). Boston Diagnos-
tic Aphasia Examination (2nd ed.). Philadelphia:
Lea & Febiger.
Grossman, M. (1998). Not all words are created equal:
Category-specific deficits in central nervous sys-
tem disease. Neurology, 50, 324-325.
Gurd, J., & Ward, C. (1989). Retrieval from semantic
and letter-initial categories in patients with Parkin-
son’s disease. Neuropsychologia, 27, 743-746.
Hanley, J.R., Dewick, H.C., Davies, A.D.M., Playfer,
J., & Turnbull, C. (1990). Verbal fluency in Par-
kinson’s disease. Neuropsychologia, 28, 737-741.
Hodges, J.R., Salmon, D.P., & Butters, N. (1990).
Differential impairment of semantic and episodic
memory in Alzheimer’s and Huntington’s disease:
A controlled prospective study. Journal of Neurol-
ogy, Neurosurgery and Psychiatry, 53, 1089-1095.
Jacobs, D.M., Marder, K., Côté, L.J., Sano, M., Stern,
Y., & Mayeux, R. (1995). Neuropsychological
characteristics of preclinical dementia in Parkin-
son’s disease. Neurology, 45, 1691-1696.
Kaplan, E., Goodglass, H., & Weintraub, S. (1983).
The Boston Naming Test. Philadelphia: Lea and
Febiger.
Kopin, I.J., & Markea, S.P. (1988). MPTP toxicity:
Implications for research in Parkinson’s disease.
Annual Review of Neuroscience, 11, 81-96.
Mahieux, F., Fenelon, G., Flahault, A., Manifacier,
M.J., Michelet, D., & Boller, F. (1998). Neuropsy-
chological prediction of dementia in Parkinson’s
disease. Journal of Neurology, Neurosurgery and
Psychiatry, 64, 178-183.
Martin, A., & Fedio, P. (1983). Word production and
comprehension in Alzheimer’s disease: The break-
down of semantic knowledge. Brain and Lan-
guage, 19, 124-141.
Martin, A., Haxby, J.V., Lalonde, F.M., Wiggs, C.L.,
& Ungerleider, L.G. (1995). Discrete cortical re-
gions associated with knowledge of color and
knowledge of action. Science, 270, 102-105.
Matison, R., Mayeux, R., Rosen, J., & Fahn, S.
(1982). ‘‘Tip-of-the-tongue’’ phenomenon in Par-
kinson’s disease. Neurology, 32, 567-570.
Mattis, S. (1988). Dementia Rating Scale. Odessa, FL:
Psychological Assessment Resources.
McCarthy, R.A., & Warrington, E.K. (1985). Cate-
gory-specificity in an agrammatic patient: The rel-
ative impairment of verb retrieval and comprehen-
sion. Neuropsychologia, 23, 709-727.
Miceli, G., Silveri, M.C., Villa, G., & Caramazza, A.
(1984). On the basis for the agrammatic’s diffi-
culty in producing verbs. Cortex, 20, 207-220.
Monsch, A.U., Bondi, M.W., Butters, N., Salmon,
D.P. Katzman, R., & Thal, L.J. (1992). Compari-
sons of verbal fluency tasks in the detection of de-
mentia of the Alzheimer type. Archives of Neurol-
ogy, 49, 1253-1258.
Owen, A.M., Sahakian, B.J., & Robbins, T.W. (1998).
The role of executive deficits in memory disorders
in neurodegenerative disease. In A.I. Tröster (Ed.),
Memory in neurodegenerative nisease: Biological,
cognitive, and clinical perspectives (pp. 157-171).
Cambridge, UK: Cambridge University Press.
Randolph, C., Braun, A.R., Goldberg, T., & Chase,
T.N. (1993). Semantic fluency in Alzheimer’s, Par-
kinson’s, and Huntington’s disease: Dissociation of
storage and retrieval failures. Neuropsychology, 7,
82-88.
Raskin, S., Sliwinski, M., & Borod, J. (1992). Cluster-
ing strategies on tasks of verbal fluency in Parkin-
son’s disease. Neuropsychologia, 30, 95-99.
Spreen, O., & Benton, A.L. (1969, 1977). Neurosen-
sory Center Comprehensive Examination for Apha-
sia (NCCEA). Victoria, Canada: University of Vic-
toria Neuropsychology Laboratory.
Taylor, A.E., & Saint-Cyr, J.A. (1995). The neuropsy-
chology of Parkinson’s disease. Brain and Cogni-
tion, 28, 281-296.
Tröster, A.I., & Fields, J.A. (1995). Frontal cognitive
function and memory in Parkinson’s disease: To-
 VERBAL FLUENCY IN PARKINSON’S DISEASE
ward a distinction between prospective and declar-
ative memory impairments? Behavioural Neurol-
ogy, 8, 59-74.
Tröster, A.I., Fields, J.A., & Koller, W.C. (in press).
Parkinson’s disease and parkinsonism. In C.E.
Coffey & J.L. Cummings (Eds.), Textbook of geri-
atric neuropsychiatry (2nd ed.). Washington, DC:
American Psychiatric Press.
Tröster, A.I., Fields, J.A., Testa, J.A., Paul, R.H.,
Blanco, C.R., Hames, K.A., Salmon, D.P., &
Beatty, W.W. (1998). Cortical and subcortical in-
fluences on clustering and switching in the perfor-
mance of verbal fluency tasks. Neuropsychologia,
36, 295-304.
443
Tröster, A.I., Salmon, D.P., McCullough, D., & But-
ters, N. (1989). A comparison of the category flu-
ency deficits associated with Alzheimer’s and
Huntington’s disease. Brain and Language, 37,
500-513.
Warburton, E., Wise, R.J.S., Price, C.J., Weiller, C.,
Hadar, U., Ramsay, S., & Frackowiak, R.S.J.
(1996). Noun and verb retrieval by normal sub-
jects: Studies with PET. Brain, 119, 159-179.
Williamson, D.J.G., Adair, J.C., Raymer, A.M., &
Heilman, K.M. (1998). Object and action naming
in Alzheimer’s disease. Cortex, 34, 601-610.
Zingeser, L.B., & Berndt, R.S. (1990). Retrieval of
nouns and verbs in agrammatism and anomia.
Brain and Language, 39, 14-32.