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Neuropsychologia 37 (1999) 1499±1503

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Note

Action (verb naming) ¯uency as an executive function measure:


convergent and divergent evidence of validity
Andrea L. Piatt 1, Julie A. Fields, Anthony M. Paolo, Alexander I. TroÈster*
Department of Neurology, University of Kansas Medical Center, 3901 Rainbow Blvd, Kansas City, KS 66160±7314, USA
Received 2 June 1998; received in revised form 26 February 1999; accepted 2 March 1999

Abstract

Numerous studies have demonstrated dissociable neuroanatomic underpinnings for the retrieval of grammatical classes of
words such as nouns and verbs. Whereas retrieval of common and proper nouns is primarily mediated by posterior and anterior
temporal regions, respectively, verb retrieval is primarily mediated by frontal regions. The majority of studies evaluating verb
production have utilized tasks requiring subjects to name a graphically depicted action (i.e. action naming), leaving tests of verb
generation in the absence of prompting stimuli (i.e. action ¯uency) largely unexamined. In a recent study, Piatt, Fields, Paolo,
Koller and TroÈster (in press) found that an action ¯uency task discriminated demented Parkinson's disease (PD) patients from
non-demented PD patients and healthy control subjects, whereas lexical and categorical ¯uency tasks did not. These authors
suggested that action ¯uency was sensitive to the fronto±striatal pathophysiology associated with PD dementia, and thus, that
action ¯uency might serve as an indicator of executive functioning. This study was undertaken to evaluate the construct validity
of action ¯uency as an executive function measure in a group of healthy elderly control subjects. Findings revealed modest to
moderate relationships between action ¯uency and several putative executive measures. Action ¯uency was unrelated to indices
of semantic and episodic memory. Results support the construct validity of action ¯uency as an executive function measure and
suggest that this task may provide some unique information not tapped by traditional executive function tasks. # 1999 Elsevier
Science Ltd. All rights reserved.

Keywords: Verbal ¯uency; Executive functioning; Neuropsychological assessment

Numerous studies have demonstrated dissociable frontal and posterior lesions. For example, in a study
neuroanatomic underpinnings for the retrieval of involving patients with aphasia syndromes suggestive
grammatical classes of words such as nouns and verbs. of neuroanatomical dysfunction in frontal (agrammatic
An accumulation of evidence supports the contention aphasics) and temporal (anomic aphasics) regions,
that common and proper nouns are represented in pos- Miceli et al. [15] found that agrammatic aphasics
terior and anterior temporal regions, respectively, demonstrated notable de®cits in verb production,
whereas verb retrieval is strongly mediated by frontal despite preservation of noun retrieval. In contrast, the
neural circuits [1,3,5±9,11,14,15,19]. Evidence for the anomic aphasic subjects demonstrated greater diculty
prominent role of the frontal lobes in verb retrieval with noun retrieval in comparison to verb production.
comes predominantly from studies comparing noun Similar ®ndings were reported by Damasio and Tranel
and verb retrieval in patients with known or suspected [7] who found that patients with frontal lobe injury
demonstrated notable diculty with verb but not noun
retrieval. In contrast, patients with posterior lesions
* Corresponding author. Tel.: +1-913-588-7187; fax: 1-913-588- demonstrated the opposite pattern of preserved verb
6965.
E-mail address: atroster@kumc.edu (A.I. TroÈster)
retrieval in the presence of poor noun generation.
1
Present address Department of Psychiatry and Human Behavior, Based on this double-dissociation, Damasio and
Brown University School of Medicine Tranel asserted that verb naming is mediated by the

0028-3932/99/$ - see front matter # 1999 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 2 8 - 3 9 3 2 ( 9 9 ) 0 0 0 6 6 - 4
1500 A.L. Piatt et al. / Neuropsychologia 37 (1999) 1499±1503

frontal regions, whereas noun retrieval is mediated by dysfunction that undermines the ability to mentally
the dominant, anterior temporal lobe. In a recent coordinate and manipulate the diverse range of infor-
study by Cappa et al. [2], similar dissociations were mation that may be associated with a verb. Although
observed among patients with Alzheimer's disease there is ample evidence to support the contention that
(AD) and fronto±temporal dementia (FTD). the retrieval of verbs re¯ects executive functioning, and
Speci®cally, Cappa et al. reported that both the AD possibly a unique aspect of executive functioning, these
and the FTD subjects exhibited inferior object and hypotheses have not been directly evaluated in non-
action naming relative to normal controls. However, clinical populations. Moreover, investigations of verb
the patients with FTD, relative to patients with AD, retrieval employing a ¯uency-based task are extremely
performed signi®cantly better on the object naming rare. The absence of both ¯uency-based methods of
test. Cappa et al. interpreted these ®ndings as assessing verb retrieval and the use of such measures
suggesting that the retrieval de®ciencies noted in the as indicators of frontal lobe and/or executive function-
AD subjects re¯ect more general loss of semantic in- ing is surprising given the notably wide use of lexical
formation, whereas the dissociation between object ¯uency as an executive function test.
and action naming observed in patients with FTD This study was undertaken to evaluate the construct
underscores the importance of the frontal lobes in the validity of an action ¯uency task as a measure of
retrieval of verbs. In a similar vein, Williamson et al. executive functioning in a sample of healthy elderly
[18] reported that patients with AD performed signi®- subjects. Given the prominent role ascribed to the
cantly more poorly on object than action naming, even frontal lobes in verb retrieval, it was hypothesized that
once word-frequency e€ects were controlled for. action ¯uency would be signi®cantly related to puta-
Although these and other studies [1,3,5,6,8,11,14,19] tive measures of executive functioning (convergent val-
support the hypothesized di€erential neuroanatomic idity), but not signi®cantly related to measures tapping
substrates of noun and verb retrieval, functional ima- semantic and episodic memory (divergent validity).
ging (PET) studies have suggested a more widely dis- However, based on evidence that verb retrieval
tributed representation of verb retrieval including involves neural circuits distinct from those involved in
heavy reliance on the dominant temporal and parietal traditional executive function tasks, we anticipated
regions [17]. only modest relationships between action ¯uency and
To date, the assessment of verb retrieval abilities has the executive function measures.
been generally limited to action naming tasks that
require subjects to identify the verb associated with a
graphically depicted image, similar to the action nam- 1. Method
ing subtest of the Boston Diagnostic Aphasia
Examination (BDAE) [10], see also Refs. 1.1. Participants
[1,3,11,14,15,19]. In contrast, the ability to generate
verbs in the absence of prompting stimuli (i.e. action Participants consisted of 67 healthy elderly control
verbal ¯uency) had been virtually unexamined until subjects recruited as caregivers of patients enrolled in
recently. In a study assessing the utility of an action studies at the Neurodegenerative Disease Research
¯uency task (rather than action naming) as an indi- Center at the University of Kansas Medical Center.
cator of frontal±subcortical pathophysiology, Piatt et Forty-two (63%) of the participants were female.
al. [16] found that action ¯uency, but not lexical or Sixty-four (96%) of the subjects were right-handed.
semantic ¯uency scores, discriminated patients with Additional sample characteristics are presented in
Parkinson's disease (PD) and dementia from non- Table 1. All subjects were free of histories of neuro-
demented PD and healthy elderly control groups. logic disease or injury, psychiatric illness including
Based on their ®ndings, Piatt et al. concluded that substance abuse or dependence, or self-reported
action ¯uency was particularly sensitive to the fronto± speci®c developmental disorders. All subjects under-
striatal pathophysiology of PD with dementia, went comprehensive interviews, neuropsychological
suggesting that action ¯uency may have utility as an testing, and neurologic examinations.
indicator of frontal lobe functioning in clinical popu-
lations. 1.2. Materials and procedures
Findings across clinical populations and assessment
methods (i.e. task) suggest that verb retrieval abilities As part of a larger test battery, subjects were admi-
re¯ect the underlying integrity of frontal lobe neural nistered the Dementia Rating Scale (DRS), Wisconsin
circuitry, and can be considered to re¯ect the cognitive Card Sorting Test (WCST), Trail Making Tests
construct of executive function. In a recent report, (Trails), Boston Naming Test (BNT), California
Grossman [12] discussed the hypothesis that verb Verbal Learning Test (CVLT), and the Wechsler
retrieval de®cits re¯ect underlying executive system Memory ScaleÐRevised (WMS-R), all in standard
A.L. Piatt et al. / Neuropsychologia 37 (1999) 1499±1503 1501

Table 1 total time to complete Trails B all served as measures


Demographic characteristics and Neuropsychological Test
of executive functioning.
Performance (Mean, SD, and Range)

Mean (SD) Range 1.4. Memory and language measures

Age 71.39 (6.45) 57±84 The following measures of episodic memory were
Education 14.96 (2.31) 12±20 included: The number of words recalled on CVLT
Dementia Rating Scale total (/144) 139.37 (4.05) 128±144
Action ¯uency (words/min) 16.75 (4.73) 8±30 trials one through ®ve and the WMS-R Logical
Dementia Rating Scale I/P (/37) 36.49 (1.30) 31±37 Memory (WMS-R LM) immediate recall raw score.
Dementia Rating Scale CNC (/39) 37.45 (2.36) 30±39 The BNT total correct score was used as a measure of
Trails B (total time) 83.00 (33.32) 37±218 semantic memory.
WCST-Categories (/6) 4.77 (2.13) 0±6
WCST-Conceptual Responses (%) 66.15 (24.34) 5±91
WCST-Perseverative Responses 15.98 (14.56) 3±65
WCST-Perseverative Errors 14.26 (11.94) 3±51
Boston Naming Test (/60) 57.09 (3.34) 36±60
CVLT total (/80) 50.91 (10.45) 24±70 2. Results
WMS-R Logical Memory Immediate (/50) 27.15 (5.53) 10±36

Table 1 presents the means and standard deviations


fashion. Detailed descriptions of these tests are pre- for action ¯uency and the various neuropsychological
sented in Lezak [13]. Instructions for the Action measures. Because not all variables were normally dis-
Fluency task were as follows: I'd like you to tell me as tributed, nonparametric Spearman's rho correlations
many di€erent things as you can think of that people do. were utilized for relational analyses, with attendant
I don't want you to use the same word with di€erent results depicted in Table 2. As indicated, there is a sig-
endings, like eat, eating, eaten. Also, just give me single ni®cant positive relationship between education and
words such as eat, or smell, rather than a sentence. Can action ¯uency scores, whereas age is unrelated to
you give me an example of something that people do? If action ¯uency scores. Modest negative correlations
the response was acceptable participants were further were noted between action ¯uency performance and
instructed: That's the idea. Now in one minute, tell me Trails B, WCST±PR, and WCST±PE scores, whereas
as many di€erent things as you can think of that people moderate positive correlations were noted between
do. If the subject had diculty understanding the task, action ¯uency and WCST±CR and WCST±Categories.
the words `verb' or `action' were used for clari®cation. A modest positive correlation between action ¯uency
The score for this task was the total number of unique scores and DRS±CNC scores was observed, but no
words produced in 60 s. Given the marked similarity signi®cant relationship was found between the DRS±I/
in method (monomethod) used in the assessment of P scores and action ¯uency, despite a signi®cant re-
action, lexical and semantic ¯uency, the latter two lationship between DRS±I/P scores and Trails B and
were not included in the present study. Although re- WCST±PE. In order to further clarify the relationships
lationships between the three ¯uency measures may between action ¯uency and the executive measures, a
have been identi®ed, whether such relationships would step-wise multiple regression analysis was conducted
have re¯ected similarity of underlying traits or simply with six executive measures (the four WCST scores,
comparability of methodology would have been quite two DRS scores, and Trails B) and education serving
dicult to ascertain with any degree of certainty. As as predictor variables and action ¯uency serving as the
such, a multi-trait/multi-method approach was utilized criterion variable. Results yielded a signi®cant re-
in this study. gression equation that accounted for slightly more
than 28% of the variance in action ¯uency scores
(adjusted R 2=0.28), F (3,61)=9.47, P < 0.001.
1.3. Executive function measures WCST±PR was the ®rst variable to enter the equation,
accounting for approximately 15% of the variance in
In order to provide an adequate representation of action ¯uency scores (R 2=0.145), followed by edu-
executive function abilities, several scores from various cation which accounted for an additional 11% of the
measures were included. Speci®cally, the Initiation/ variance in action ¯uency scores (R 2 change=0.106),
Perseveration and Conceptualization subtest scores while DRS±I/P was the last variable to enter the
from the DRS (DRS±I/P and DRS±CNC), the Percent equation, accounting for another 5% of variance (R 2
Conceptual Level Responses (WCST±CR), change=0.053). The assumptions of multiple re-
Perseverative Responses (WCST±PR), Perseverative gression were met as indicated by observation of stan-
Errors (WCST±PE) and Categories Completed dardized residual plots and by results of a Durbin±
(WCST±Categories) scores from the WCST, and the Watson test that indicated independence of errors.
1502 A.L. Piatt et al. / Neuropsychologia 37 (1999) 1499±1503

3. Discussion

Education DRS±I/P DRS±CNC Trails B WCST±PR WCST±PE WCST±CR WCST±Categories CVLT total WMS-R LM BNT total

1.0
As hypothesized, action ¯uency was signi®cantly,
but moderately, related to several putative executive
function measures. Although no signi®cant relation-
ship was observed between action ¯uency and DRS±I/

0.18
P scores, this may have re¯ected a marked restriction

1.0
of range in DRS±I/P scores (60 of the 67 subjects
obtained scores of 36 or 37/37). However, the signi®-
cant relationships between DRS±I/P scores and Trails

0.37b
0.25a
B and WCST±PE argue against this explanation.

1.0
Another possibility is that the low correlation between
DRS±I/P and action ¯uency stems from the fact that
the DRS±I/P score is heavily in¯uenced by category
(semantic) verbal ¯uency (up to 20 of 37 points), and
action and semantic ¯uency tasks tap somewhat di€er-
0.42b
0.30a

0.01
ent retrieval processes (see [16]). Of the executive
1.0

measures, WCST±PR was the most predictive of


action ¯uency scores, whereas DRS±I/P scores
Spearman's rho correlation coecients between action ¯uency scores, demographic variables, and neuropsychological test scores

accounted for a small portion of variance in action ¯u-


0.78b
0.42b
0.39b
0.26a

ency scores not tapped by WCST±PR. As the remain-


1.0

ing executive measures failed to enter the regression


equation, it appears that they tapped redundant
ÿ0.95b
ÿ0.76b
ÿ0.35b
ÿ0.40b

aspects of executive functioning. Although action ¯u-


ÿ0.22
1.0

ency shares common variance with other executive


tests, it appears to also measure a component of execu-
tive functioning not measured, or measured to a lesser
0.99b
ÿ0.94b
ÿ0.73b

ÿ0.40b
ÿ0.35a

ÿ0.22

extent, by more traditional tasks. Such an hypothesis


1.0

is supported by the rather modest relationships


observed between action ¯uency and the executive
ÿ0.32b
0.25a
ÿ0.28a

ÿ0.31a
0.23

ÿ0.12
ÿ0.21

tests utilized in the present study. This ®nding is con-


1.0

sistent with the report of Piatt et al. [16] who found


action ¯uency to be uniquely sensitive and speci®c to
the advanced frontostriatal pathophysiology of
0.36b
0.30a
ÿ0.03
ÿ0.16
ÿ0.20

0.18
0.11
0.09

Parkinson's disease with associated dementia, while


1.0

lexical and semantic ¯uency were not.


It is important to note that action ¯uency scores
ÿ0.27a

ÿ0.25a

were not signi®cantly related to BNT or Logical


ÿ0.03

ÿ0.24

0.22
0.20
0.13
0.03
0.15
1.0

Memory scores, arguing against the likelihood that


retrieval of verbs re¯ects only aspects of more general
semantic retrieval or components of memory. In the
0.25a

0.29a
ÿ0.01
0.03
0.04
ÿ0.15
ÿ0.16
0.14

ÿ0.02

0.03

presence of signi®cant relationships between action ¯u-


1.0

ency and several executive function measures, the lack


of association between action ¯uency and the memory
0.38b
0.35b
0.35b
ÿ0.37b
ÿ0.35b
ÿ0.39b
ÿ0.38b
ÿ0.05
ÿ0.23
ÿ0.19

ÿ0.22
1.0
Action ¯uency Age

measures o€ers further support to the purported sensi-


tivity of action ¯uency as an executive function
measure. These ®ndings also are consistent with a
number of studies that have identi®ed single or
0.41b

ÿ0.37b
ÿ0.38b
0.39b
0.40b
0.26a
ÿ0.28a

double-dissociations between noun and verb retrieval


ÿ0.10

0.24

0.04
0.18
0.19
1.0

abilities implicating the anterior brain region in verb


retrieval [2,7,15].
WCST±Categories

Overall, results provide evidence for the convergent


Action Fluency

P < 0.05,.
P < 0.01.

and divergent validity of action ¯uency as an executive


WMS-R LM
CVLT total
WCST±CR
DRS±CNC

WCST±PR
WCST±PE
Education

function measure in healthy elderly subjects. These


DRS±I/P

Trails B
Table 2

®ndings, in combination with the previously reported


BNT
Age

a
b

ability of action ¯uency to discriminate groups with


A.L. Piatt et al. / Neuropsychologia 37 (1999) 1499±1503 1503

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