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Verbal Fluency in Right Brain Damage: Dissociations Among Production Criteria and Duration

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This study aimed to verify dissociations in the performance of verbal fluency tasks with different production criteria and duration following vascular right-hemisphere damage. We tested the hypothesis that longer fluency tasks would be more sensitive in identifying deficits in the sample. The relationship between verbal fluency performance and sustained attention was also investigated. Forty adults with vascular right-hemisphere damage were assessed using verbal fluency tasks with three different production criteria (unconstrained, phonemic, and semantic fluencies from the Montreal Communication Evaluation Battery). Performance deficits in 1-min and 2-min fluency tasks were calculated (Zscore) and com-pared (chi-square).Results didnot suggest a difference in sensitivity between the task lengths in detecting cognitive impairment. However, double dissociations were found, highlighting the contribution of extended verbal fluency tasks to neuropsychological assessment. Analy-ses also showed that participants exhibited greater levels of impairment in the semantic flu-ency task. No relationship was identified between performance in sustained attention tasks and verbal fluency tasks, regardless of the latter’s duration. The combined use of longer and shorter fluency tasks in the assessment of patients with right brain damage may contribute to the identification of different executive function impairments in this sample.
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Applied Neuropsychology: Adult
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Verbal Fluency in Right Brain Damage: Dissociations
Among Production Criteria and Duration
Nicolle Zimmermann a , Laura Branco a , Bernadette Ska b , Emerson Leandro Gasparetto c ,
Yves Joanette d & Rochele Fonseca a
a Postgraduate Program in Psychology, Human Cognition, Pontifical Catholic University of Rio
Grande do Sul , Porto Alegre , Brazil
b Institut Universitaire de Gériatrie de Montréal, Université de Montréal , Montréal ,
Québec , Canada
c Radiology Department, Federal University of Rio de Janeiro , Rio de Janeiro , Brazil
d Faculté de Médecine and Institut Universitaire de Gériatrie de Montréal, Université de
Montréal , Montréal , Québec , Canada
Published online: 03 Oct 2013.
To cite this article: Nicolle Zimmermann , Laura Branco , Bernadette Ska , Emerson Leandro Gasparetto , Yves Joanette
& Rochele Fonseca , Applied Neuropsychology: Adult (2013): Verbal Fluency in Right Brain Damage: Dissociations Among
Production Criteria and Duration, Applied Neuropsychology: Adult
To link to this article: http://dx.doi.org/10.1080/09084282.2013.802693
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Verbal Fluency in Right Brain Damage: Dissociations
Among Production Criteria and Duration
Nicolle Zimmermann and Laura Branco
Postgraduate Program in Psychology, Human Cognition, Pontifical Catholic
University of Rio Grande do Sul, Porto Alegre, Brazil
Bernadette Ska
Institut Universitaire de Ge
´riatrie de Montre
´al, Universite
´de Montre
´al,
Montre
´al, Que
´bec, Canada
Emerson Leandro Gasparetto
Radiology Department, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
Yves Joanette
Faculte
´de Me
´decine and Institut Universitaire de Ge
´riatrie de Montre
´al,
Universite
´de Montre
´al, Montre
´al, Que
´bec, Canada
Rochele Fonseca
Postgraduate Program in Psychology, Human Cognition, Pontifical Catholic
University of Rio Grande do Sul, Porto Alegre, Brazil
This study aimed to verify dissociations in the performance of verbal fluency tasks with
different production criteria and duration following vascular right-hemisphere damage.
We tested the hypothesis that longer fluency tasks would be more sensitive in identifying
deficits in the sample. The relationship between verbal fluency performance and sustained
attention was also investigated. Forty adults with vascular right-hemisphere damage were
assessed using verbal fluency tasks with three different production criteria (unconstrained,
phonemic, and semantic fluencies from the Montreal Communication Evaluation Battery).
Performance deficits in 1-min and 2-min fluency tasks were calculated (Zscore) and com-
pared (chi-square). Results did not suggest a difference in sensitivity between the task lengths
in detecting cognitive impairment. However, double dissociations were found, highlighting
the contribution of extended verbal fluency tasks to neuropsychological assessment. Analy-
ses also showed that participants exhibited greater levels of impairment in the semantic flu-
ency task. No relationship was identified between performance in sustained attention tasks
and verbal fluency tasks, regardless of the latter’s duration. The combined use of longer and
shorter fluency tasks in the assessment of patients with right brain damage may contribute to
the identification of different executive function impairments in this sample.
Key words: cognitive processes, neuropsychological tests, right hemisphere, vascular brain
damage, verbal fluency
Address correspondence to Nicolle Zimmermann, Pontifical Catholic University of Rio Grande do Sul, Ipiranga Avenue, 6681 - Building 11 - 9th
Floor, Room 932, Porto Alegre, Brazil. E-mail: nicolle.zimmermann@gmail.com
APPLIED NEUROPSYCHOLOGY: ADULT, 0: 1–9, 2013
Copyright #Taylor & Francis Group, LLC
ISSN: 2327-9095 print=2327-9109 online
DOI: 10.1080/09084282.2013.802693
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INTRODUCTION
Verbal fluency tasks are among the most frequently used
instruments in the neuropsychological assessment of
executive functions related to linguistic and mnemonic
abilities, such as lexical access and semantic memory
(Kave
´, Heled, Vakil, & Agranov, 2010; Pen˜a-Casanova
et al., 2009; Ruff, Light, Parker, & Levin, 1997). Although
performance in these tasks is generally analyzed in terms
of the total number of words retrieved,recent studies have
suggested that this analysis may not provide a compre-
hensive assessment of the cognitive functions involved
in verbal fluency tasks. The analysis of other variables in
verbal fluency performance could allow for a more accu-
rate identification of cognitive deficits in abilities such as
initiation, inhibition, monitoring, cognitive flexibility,
and semantic memory (Errens, 2011; Troyer, 2000).
Verbal fluency tasks are indispensable tools in clinical
neuropsychology, particularly due to their sensitivity in
diagnosing cognitive impairment in neurological samples,
such as in patients with traumatic brain injury (Kave
´
et al., 2010), and in psychiatric disorders, like schizophre-
nia (Owens et al., 2011). Studies have also demonstrated
that verbal fluency performance can be used to discrimi-
nate between different types of dementia and stages of
mild cognitive impairment (Cerhan et al., 2002). There-
fore, it is crucial that performance in these tasks is anal-
yzed in the most comprehensive way possible, so that
their diagnostic potential is explored to the fullest extent.
Phonemic or letter-based fluency, which demands the
spoken elicitation of words beginning with specific
letters—for example, F, A, and S (Benton & Hamsher,
1989)—and semantic or categorical fluency, which
involves the generation of words from the semantic cate-
gory ‘‘animals,’’ are the most traditionally used verbal
fluency tasks in neuropsychological assessment. Each of
these tasks is usually carried out during the course of
1 min (Rosen, 1980). However, different verbal fluency
paradigms and qualitative-quantitative analyses have
been developed during the history of neuropsychology.
Semantic and phonemic clusters can be in terms of the
strategies used to retrieve words, such as selecting words
that have similar meanings or that start with the same
sound or letter (Laine, 1988). Additionally, it is possible
to analyze the type of errors made, such as rule viola-
tions, perseverations, and number, gender, and size var-
iations (Benton & Hamsher, 1989). Fernaeus and
Almkvist (1998) suggested that assessing these variables
at every 30 s of the task allows for the comprehension of
changes in performance over time.
Verbal fluency tasks with durations other than 1 min
have also been developed. The Montreal Communication
Evaluation Battery (Joanette, Ska, & Co
ˆte
´, 2004;
Brazilian version, Fonseca, Parente, Co
ˆte
´,Ska,&
Joanette, 2008a, 2008b; Fonseca, Parente, Co
ˆte
´,&
Joanette, 2007), for example, includes verbal fluency
tasks with 2.5-min durations (unconstrained verbal
fluency task [UVF]) and 2-min durations (phonemic
verbal fluency task [PVF] and semantic verbal fluency
task [SVF]).
Performance in verbal fluency tasks can be assessed
by analyzing the total number of words produced
throughout the task, as well as by the number of words
retrieved in individual segments of the task. The latter
has proved especially useful for assessing different pro-
cesses involved in word retrieval. Venegas and Mansur
(2011), for instance, investigated the performance of eld-
erly individuals in each quarter of a 1-min-long verbal
fluency task and found that individuals produced a
significantly greater number of words during the first
quarter. Raboutet et al. (2010) also found that healthy
subjects retrieved words more easily in the beginning
of the task. Those authors proposed that the effort
required for word production increases with time and
demands progressively more attention and executive
control as the task continues. As such, the processes
involved in word retrieval during each segment of the
verbal frequency tasks may differ, with later segments
relying more on attentional and executive processes.
Further evidence regarding the different processes
involved in verbal fluency tasks was also obtained in
studies with clinical samples. Hurks et al. (2004) studied
the performance of subjects with attention-deficit hyper-
activity disorder (ADHD) and healthy controls in SVF
and PVF. The study revealed an interaction between
group and productivity over time, as children with
ADHD produced fewer words than did controls in the
first 15 s of the PVF. It is possible that children in the
clinical sample had deficits in the automatic processes
involved in word retrieval, which are likely responsible
for the words produced in the beginning of verbal fluency
tasks. To further investigate the processes involved in
different time segments of the tasks, Hurks et al. (2010)
assessed verbal fluency performance in childhood during
different intervals of time. Results demonstrated that the
automatic processing displayed in the first 15 s of the task
develops 2 years earlier than do the controlled processes
involved in the production of words from 16 s to 60 s into
the task. Although the comparison between verbal flu-
ency segments displayed sensitivity in the identification
of developmental changes in cognitive functioning, the
authors affirmed that the applicability of such an analy-
sis in a clinical setting still had to be further investigated.
Another method of investigating changes in verbal
fluency performance over time was proposed by Errens
(2011), who analyzed performance in the 1st and 2nd
minute of the task separately by looking at the total num-
ber of words retrieved in each interval. In this study, how-
ever, the authors could not find differences between the
performance of a control group and individuals with
2ZIMMERMAN ET AL.
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diabetes mellitus in the number of words retrieved.
Group comparisons of performance in different cognitive
tasks allow for the identification of dissociations, which is
a classical method for investigating cognitive processes in
neuropsychology. This concept is based on situations
where a sample or individual displays impairment in a
given task, while another sample or individual has no
impairment in the same task. A double dissociation
occurs when two samples or individuals exhibit an inverse
pattern of performance in two different tasks (Baldo,
Schwartz, Wilkins, & Dronkers, 2010).
The different ways in which performance in verbal
fluency tasks can be analyzed allow for a more specific
investigation of cognitive functioning in different clinical
samples and help to identify clinical profiles. One of the
profiles to which verbal fluency studies can make signi-
ficant contributions is that of individuals with right-
hemisphere brain damage (RBD). The literature regarding
this particular clinical group suggests that its deficits are
predominantly related to pragmatic, prosodic, lexical-
semantic, and discursive abilities (Co
ˆte
´,Payer,Giroux,&
Joanette, 2007). Verbal fluency tasks can be used to ident-
ify impairments in the lexical-semantic abilities of indivi-
duals with RBD, as they can detect tendencies to retrieve
fewer prototypical words than those produced by healthy
individuals (Beausoleil, Monetta, Leblanc, & Joanette,
2001). Research has also explored the executive compo-
nents that may underlie pragmatic impairment in indivi-
duals with RBD (Champagne, Desautels, & Joanette,
2004; Champagne-Lavau, Stip, & Joanette, 2007). How-
ever, nonlinguistic hypotheses for impairments in verbal
fluency performance have not been sufficiently explored
in this sample. Given the evidence toward the involvement
of executive and attentional processes in verbal fluency
tasks, it is essential that impairments in these functions
are considered in order to fully understand the nature of
cognitive deficits associated with RBD.
Among the wide range of processes referred to as
‘‘executive’’ and ‘‘attentional,’’ some may be especially
relevant to verbal fluency performance. One such execu-
tive process is cognitive control, of which involvement in
verbal fluency performance was briefly discussed with
regards to the behavioral evidence reviewed. A system-
atic review of functional neuroimaging studies also
identified a common activation network related to
cognitive control (prefrontal, dorsal anterior cingulate,
and parietal cortices) involved in the performance of
executive function tasks in 193 studies (Niendam et al.,
2012). As for attentional processes, a study by Lo
´pez-
Campo, Betancur, Aguirre-Acevedo, Puerta, and Pinedo
(2005) showed a common factor structure underlying
performance in verbal fluency and verbal sustained
attention tasks in an ADHD sample.
Given the results of the aforementioned studies, the
current investigation elected to focus on possible
relationships between verbal fluency performance,
executive control, and verbal sustained attention. Based
on data regarding increased cognitive demands of verbal
fluency performance over time, we hypothesized that
longer verbal fluency tasks might overload the cognitive
control required for performance. This hypothesis was
investigated through comparisons between the perfor-
mance of stroke patients with RBD and a normative
sample on brief and extended versions of a verbal fluency
task. The present findings could shed light on dissocia-
tions between individuals’ performance in verbal fluency
tasks of different durations and could indicate whether
these tasks differ in their ability to identify cognitive
impairment. Furthermore, the current study investigated
which verbal fluency criterion (unconstrained, semantic,
or phonemic) displayed greater sensitivity in identifying
impairments in individuals with RBD; whether associa-
tions between verbal sustained attention and verbal
fluency performance can be identified in this sample;
and whether this relationship is different for extended
and brief versions of verbal fluency tasks.
METHOD
Participants
Forty adults with RBD were recruited from public and
private hospitals in the city of Porto Alegre, Brazil.
All participants were native speakers of Brazilian Portu-
guese, ranged in age from 32 to 74 years old, and had 1
to 19 years of formal schooling. All participants had suf-
fered an ischemic or hemorrhagic stroke in the right
hemisphere, and none had a previous history of psychi-
atric or neurological diseases. All participants were
right-handed and had no uncorrected sensory deficits.
The initial sample was composed of 46 patients; how-
ever, 2 participants were excluded for being left-handed,
1 for having a bilateral brain lesion, and 3 for having no
formal education. Exclusion criteria were investigated
through a questionnaire, screening by a medical team,
and telephone interviews with the patients’ relatives.
Some variation was observed in the sites of lesions sus-
tained by participants in the study: 50% had frontal
lesions, 37.5% had temporal lesions, 52.5% had parietal
lesions, 2.5% had occipital lesions, and 42.5% had mixed
subcortical and cortical lesions. Table 1 displays the
sociodemographic and clinical data collected from the
patients.
Materials and Procedures
All participants provided written and informed consent,
and the current research project was approved by the
Ethical Committee of the Pontifical Catholic University
VF DISSOCIATIONS 3
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of Rio Grande do Sul (protocol #10=05134). Parti-
cipants were assessed individually in well-lit and quiet
rooms. The instruments used in this study were part of
a larger neuropsychological test battery completed by
participants during approximately four sessions lasting
1 hr each. A sociocultural and clinical questionnaire
was used to investigate sample characteristics. The fre-
quency of reading and writing habits was investigated
through patients’ descriptions of the frequency with
which they read magazines, books, newspapers, and
other reading material, as well as the frequency with
which they wrote essays, notes, and other types of text.
The maximum attainable score in the reading and
writing measures was 28.
Verbal Fluency Tasks
The Montreal Communication Evaluation Battery
(originally developed in French language in Canada,
Protocole Montre
´al d’E
´valuation de la Communication
[Protocole MEC] by Joanette et al., 2004; adapted to
Brazilian Portuguese as Bateria Montreal de Avaliac
¸a˜o
da Comunicac
¸a˜o by Fonseca et al., 2008b) contains
fluency tasks with three different production criteria
(unconstrained, phonemic, and semantic). The tasks are
described in greater detail in the following paragraphs.
Unconstrained verbal fluency. The patient was
required to evoke as many words as possible—with the
exception of proper nouns—during 2.5 min, while
keeping their eyes closed.
Phonemic verbal fluency. In this task, patients were
asked to say as many words that started with the letter
‘‘p’’ as they could (except for proper nouns) for 2 min.
Semantic verbal fluency. Participants were given
2 min to elicit as many words for clothes as they could
remember.
Sustained Attention–Reverse Counting
In the sustained attention–reversed counting task
(Brazilian Brief Neuropsychological Assessment Battery
[NEUPSILIN]; Fonseca, Salles, & Parente, 2008, 2009),
participants were asked to count backwards out loud
from 50 to 30. The maximum attainable score in this
task is 20.
Data Analysis
To compare verbal fluency task performance within sub-
jects, a chi-square analysis with the categorical variable
of ‘‘impaired’’ or ‘‘adequate’’ performance was conduc-
ted for each task. Patients’ performance was assessed
based on the sum of all words retrieved in the verbal flu-
ency tasks and also, separately, only during the first
1-min interval of each task. Performance was classified
by calculating Zscores (participant score minus norma-
tive mean divided by the normative standard deviation).
Normative groups from the verbal fluency tasks
(MEC Battery) are divided into three age groups (19-
to 39-year-olds; 40- to 59-year-olds; 60- to 75-year-olds),
which are then dichotomized into high (7 or more years
of formal education) and low (2 to 6 years of formal
education) education groups; each group is composed
of 50 individuals in a total sample of 300. In the present
study, 7.5% of patients were compared to the 19- to
39-year-old high education group (UVF M¼61.88,
SD ¼23.8; PVF M¼15.26, SD ¼3.61; SVF M¼30.98,
SD ¼6.29); 22.5% to the 40- to 59-year-old high
education group (UVF M¼56.78, SD ¼24.03; PVF
TABLE 1
Sociodemographic and Clinical Characteristics of the Clinical Sample
Variables N M SD
Age (years) 40 57.58 11.30
Education (years) 40 8.63 5.12
Reading and writing habits (frequency) 40 10.58 6.06
Mini-Mental State Examination 36 25.28 3.08
Time postonset (months) 40 23.18 28.32
Geriatric Depression Scale (15 items) 39 5.49 3.33
Stroke type 85% ischemic; 15% hemorrhagic
Lesion site
a
52.2% cortical
b
; 20% subcortical; 25% mixed
c
(cortical and subcortical);
2.5% right-sided but not specified
Left hemineglect 17.5% presence; 82.5% absence
a
According to Kang et al. (2010).
b
Frontal and parietal damage (n¼6); frontal and temporal damage (n¼1).
c
Parietal and temporal damage (n¼6); frontal, temporal, and parietal damage (n¼2); parietal damage (n¼2); frontal, temporal, parietal, and
occipital damage (n¼1); frontal damage (n¼3).
4ZIMMERMAN ET AL.
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M¼13.36, SD ¼4.49; SVF M¼28.42, SD ¼7.69); 20%
to the 40- to 59-year-old low education group (UVF
M¼39.56, SD ¼18.52; PVF M¼9.76, SD ¼3.17; SVF
M¼20.78, SD ¼5.69); 22.5% to the 60- to 75-year-old
high education group (UVF M¼43.72, SD ¼16.11;
PVF M¼10.84, SD ¼2.88; SVF M¼23.48,
SD ¼5.57); and 27.5% to the 60- to 75-year-old low edu-
cation group (UVF M¼31.46, SD ¼14.41; PVF
M¼8.46, SD ¼2.62; SVF M¼18.28, SD ¼4.45).
Normative groups for the attention task were divided
into four groups according to age (19- to 39-year-olds;
40- to 59-year-olds; 60- to 75-year-olds; ages 76 and
older) and education (1 to 4 years; 5 to 8 years; 9 or
more years of formal education). The total normative
sample for the NEUPSILIN Battery is 1,017 (Fonseca,
Salles, et al., 2008). In the present study, 7.5% of
patients were compared to the 19- to 39-year-olds with
1 to 4 years of education (M¼16.10, SD ¼6.64);
12.5% to the 40- to 59-year-olds with 1 to 4 years of
formal education (M¼14.10, SD ¼7.20), 10% to the
same age range but with 5 to 8 years of education
(M¼18.85, SD ¼3.51), and 20% to 40- to 59-year-olds
TABLE 2
Frequency of Deficits in Verbal Fluency and Sustained Attention Tasks by Participant
Participant=Task
Zscore
Reverse Counting TaskUVF 2 min 30 s UVF 1 min PVF 2 min PVF 1 min SVF 2 min SVF 1 min
RBD1 0.47 0.41 0.01 0.47 0.36 0.55 0.17
RBD2 1.97 0.56 1.73 0.01 1.07 1.33 0.17
RBD3 0.70 1.38 1.02 2.31 1.79 1.01 0.17
RBD4 1.74 1.51 0.90 2.72 2.27 1.65 0.3
RBD5 1.91 1.6 2.01 0.78 2.79 1.65 0.3
RBD6 0.78 0.65 1.64 0.19 0.71 0.12 0.3
RBD7 1.95 1.68 1.77 1.94 2.66 1.31 0.3
RBD8 0.78 1.77 1.27 0.78 1.23 1.65 2.45
RBD9 0.22 0.99 0.40 0.97 0.05 1.14 0.3
RBD10 0.74 1.34 1.52 2.14 1.88 0.46 0.33
RBD11 0.49 1.85 1.02 1.75 0.18 2.33 0.3
RBD12 0.70 0.82 1.64 1.36 1.36 0.97 0.3
RBD13 1.43 1.43 1.58 1.11 1.54 2.06 0.82
RBD14 1.22 0.32 0.21 0.06 1.54 1.02 1.1
RBD15 0.89 0.68 0.63 0.52 0.57 1.82 0.82
RBD16 1.16 1.23 1.16 0.65 0.84 1.5 3.09
RBD17 1.54 0.65 1.71 0.91 2.60 1.82 0.24
RBD18 0.13 0.23 0.34 0.72 0.84 1.11 0.82
RBD19 0.73 0.23 0.61 0.65 0.74 0.55 0.82
RBD20 0.03 0.01 0.47 0.33 1.54 0.4 1.96
RBD21 0.08 0.32 0.21 0.33 0.04 1.35 0.39
RBD22 0.41 0.76 0.49 0.52 0.49 0.79 0.39
RBD23 1.49 0.76 1.99 0.84 2.60 0.31 0.57
RBD24 0.89 1.1 0.75 1.5 1.54 1.35 0.01
RBD25 1.29 0.97 0.96 0.02 0.09 0.83 0.29
RBD26 1.41 2.23 0.96 2.6 1.52 3.26 0.29
RBD27 1.78 0.29 1.41 0.78 2.06 1.91 0.29
RBD28 2.62 2.54 0.53 0.63 0.99 1.34 0.06
RBD29 2.34 0.44 2.33 0.58 2.96 2.18 0.29
RBD30 0.91 3.07 0.87 2.6 0.80 2.99 0.18
RBD31 0.36 0.97 0.04 0.63 0.09 1.64 0.29
RBD32 0.82 0.83 1.22 0.18 0.09 2.45 0.29
RBD33 1.41 0.83 1.41 0.23 2.42 0.56 0.29
RBD34 1.63 1.09 0.09 0.62 0.96 0.17 0.04
RBD35 0.59 1.5 1.36 0.88 1.64 2.11 0.39
RBD36 0.93 2.18 0.23 1.14 0.06 0.38 1.75
RBD37 1.77 2.62 0.71 3.6 2.31 0.93 2.32
RBD38 2.18 1.22 1.03 0.62 1.29 0.72 0.28
RBD39 1.14 1.91 0.39 2.2 0.51 2.11 0.57
RBD40 1.91 1.22 1.83 1.41 2.76 1.28 2.32
Percentage of deficit (%)
Absence 77.5% 75% 75% 80% 67.5% 62.5% 85%
Presence 22.5% 25% 25% 20% 32.5% 37.5% 15%
UVF ¼unconstrained verbal fluency; PVF ¼phonemic verbal fluency; SVF ¼semantic verbal fluency; RBD ¼right brain damage.
VF DISSOCIATIONS 5
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with 9 or more years of education (M¼19.89,
SD ¼0.36); 15% of the sample was compared to the
60- to 75-year-olds with 1 to 4 years of formal education
(M¼16.05, SD ¼6.92), 15% to the same age group but
with 5 to 8 years of schooling (M¼18.18, SD ¼4.67),
and 20% of participants were compared to the 60- to
75-year-olds with 9 or more years of education
(M¼19.18, SD ¼2.80).
Normative data from the original MEC Battery and
NEUPSILIN Battery databases were consulted to calcu-
late Zscores. Data analyses showed that the normative
data fulfilled the required criteria for calculating Zscores,
as the following characteristics were observed: (a)
normally distributed raw scores; (b) comparative groups
of approximately 50 individuals; and (c) no ceiling effect
on raw scores (Bridges & Holler, 2007; McIntosh &
Brooks, 2011). Performance was considered impaired
when Zscores were 1.5, a well-established cutoff
point in the literature, as can be seen in Kave
´et al.
(2010) and Schoenberg et al. (2006).
RESULTS
Tables 2 and 3 present quantitative and qualitative
analyses of the frequency of performance impairments
in the sample. Table 2 presents the frequency of deficits
in fluency tasks with different durations and production
criteria, while Table 3 presents associations and
dissociations between performance in these tasks.
AscanbeseeninTable3,13individualsdisplayed
impaired performance in the brief UVF task and adequate
performance in the longer UVF task, or vice versa. Five of
these individuals (3 with impaired performance on the
brief version and 2 with impaired performance on the
extended version) also displayed impairments in the per-
formance of the sustained attention task.
Eleven individuals displayed impaired performance in
only one of the two versions of the PVF task. Three of
the individuals with impairments on the extended
version versus 2 with impaired performance on the brief
version of the PVF task also displayed attentional defi-
cits. Dissociations in the classification of performance
as impaired or unimpaired between the brief and
extended SVF tasks were also observed in 17 cases.
Three individuals—2 with impaired performance on
the extended SVF task and 1 with impairments on the
brief SVF task—also displayed impaired performance
on the sustained attention task.
The chi-square analysis showed no differences
between the number of individuals classified as having
impaired performance by the two versions of the UVF
task, v
2
(39) ¼0.430, p¼.512; the same results were
found for the PVF, v
2
(39) ¼0.000, p¼1.000, and SVF
tasks, v
2
(39) ¼0.615, p¼.433. Descriptive data pertain-
ing to the clinical sample’s performance can be
consulted in Table 4. For descriptive data pertaining
to control group performance, see Fonseca, Parente,
et al. (2008b), Fonseca et al. (2009), and Zimmermann,
Parente, Joanette, and Fonseca (in press). In summary,
(a) the number of individuals classified as having
impaired performance did not differ between fluency
tasks of different durations; (b) the SVF task identified
the greatest number of deficits; and (c) some cases
displayed associated verbal fluency and attentional
deficits regardless of the task version.
DISCUSSION
The present study investigated the performance of
patients with RBD in verbal fluency tasks with different
durations (brief and extended) and production criteria,
and its relationship with sustained attention. The present
findings did not reveal significant differences in the num-
ber of individuals identified as having verbal fluency
impairments by tasks with different durations. However,
the presence of double dissociations suggested that per-
formance in longer verbal fluency tasks may evidence
impairments that are not apparent in traditional, 1-min-
long fluency tasks. A greater number of individuals were
also identified as having impaired verbal fluency perfor-
mance in the SVF tasks than in the PVF and UVF tasks.
Finally, deficits in verbal sustained attention were not
associated with impaired performance in any of the flu-
ency tasks used in this study.
TABLE 3
Frequency of Associations and Dissociations Between Versions
Tasks=Versions 1þ212þ1þ2þ12
UVF 6=40 24=40 3=40 7=40
PVF 6=40 27=40 2=40 5=40
SVF 8=40 27=40 6=40 9=40
–1 ¼absence of deficit on the brief version of the verbal fluency
task; þ1¼presence of deficit on the brief version of the verbal fluency
task; 2¼absence of deficit on the extended version of the verbal flu-
ency task; þ2¼presence of deficit on the extended version of the ver-
bal fluency task.
TABLE 4
Descriptive Data for Verbal Fluency Tasks
Tasks M SD
UVF 2 min 32.45 23.16
UVF 1 min 16.55 10.67
SVF 2 min 16.95 7.57
SVF 1 min 12.43 5.40
PVF 2 min 15.65 8.06
PVF 1 min 10.80 5.88
M¼mean; SD ¼standard deviation.
6ZIMMERMAN ET AL.
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Brief Versus Extended Fluency Tasks and the
Identification of Deficits
The present results indicate that verbal fluency deficits
are identified in similar proportions by tasks with differ-
ent durations. Notwithstanding, such results must be
interpreted with considerable caution, as double disso-
ciations were found between brief and extended verbal
fluency tasks (i.e., deficits in the brief version and absence
of deficit in the extended version, or vice versa). These
findings open up new perspectives in the discussion
regarding the nature of the executive deficits detected
in clinical groups using verbal fluency tasks. It is possible
that patients with deficits in the extended tasks and no
deficits in the brief versions might have difficulty main-
taining lexical search strategies over time. These deficits
may be due to asymmetries between the ability to suffi-
ciently explore clusters and present efficient switching.
At the same time, the opposite pattern might represent
deficits in executive functions such as initiation and pro-
cessing speed (Hurks et al., 2004). Such hypotheses must
be further investigated to achieve a better understanding
of the double dissociations in the present results and of
the relationships between verbal fluency and executive
deficits and other cognitive processes.
Although some aspects of the present findings still
need to be further explored, as a whole, they are consist-
ent with the literature on the importance of the first
seconds of word retrieval in verbal fluency tasks (Hurks
et al., 2004; Venegas & Mansur, 2011). The first time
intervals are the most productive ones in terms of word
retrieval and rely more heavily on automatic processes
such as lexical retrieval, verbal initiation, and semantic
memory (Hurks et al., 2004). Perhaps a qualitative
analysis of retrieval in the last time intervals might be
an appropriate way of assessing the controlled processes
involved in verbal fluency, such as planning, sustained
attention, and strategy search. In other words, impor-
tant information regarding executive functioning may
be obtained from assessing the last segments of time
in the extended verbal fluency tasks, as this is when
executive processes are most likely at work.
In conclusion, the present results underscore the impor-
tance of studying verbal fluency duration through the
analysis of word production curves over time. Participants
with different executive impairments may display distinct
patterns of word production. In this way, previous find-
ings about the exclusive importance of the first time inter-
vals in verbal fluency need to be reexamined.
Contributions of Verbal Fluency Tasks with Different
Production Criteria to Cognitive Assessment
Following RBD
Verbal fluency performance relies on a basic set of cog-
nitive processes, such as sustained attention, strategy
search, inhibition, and working memory (Birn et al.,
2010). However, several studies evidence differences
between clinical populations in the performance of
verbal fluency tasks with different production criteria
(Kave
´et al., 2010; Radanovic et al., 2009).
Neuroimaging findings have proved essential to the
understanding of dissociations among verbal fluency
tasks with different production criteria. Differences in
the performance of verbal fluency tasks with semantic
versus phonemic production criteria were described in
healthy individuals by Birn et al. (2010). The authors pro-
posed that while PVF demands word retrieval based on
spelling, SVF relies more heavily on semantic memory
storage. Differences were also found in the patterns of
brain activity associated with each task: While SVF was
associated with activity in the left fusiform and the left
middle frontal gyrus, PVF led to activity in the left pre-
motor=inferior frontal gyrus. A recent review also inves-
tigated the role of the right hemisphere in lexical-semantic
and phonemic processing (Vigneau et al., 2011). Results
from this study revealed that the right hemisphere has
limited participation in language processing and that its
role is mainly performed through interhemispheric
cooperation. Although these studies have assumed that
brain activity during verbal fluency tasks is exclusively
linked to linguistic processing, it is also possible that,
given the evidence linking verbal fluency to executive
functioning, the activated areas reported in neuroimaging
studies correspond to executive functioning and verbal
working-memory processes (Vigneau et al., 2011).
Given the evidence that verbal fluency tasks predomi-
nantly recruit left-hemisphere or bilateral regions and the
fact that the current study’s sample had RBD, the follow-
ing factors may account for the study’s results: (a) Indivi-
duals with RBD rely less on executive functions during
verbal fluency tasks; (b) individuals in the clinical sample
had difficulty using contextual information (semantic
cues) to expand word generation networks or strategies
in sentence processing (Vigneau et al., 2011), as evidenced
by the poor performance observed in SVF; and (c) indivi-
duals with RBD might have had trouble retrieving more
central and prototypical words from the semantic cate-
gory (Beausoleil et al., 2001). Further investigation of
verbal fluency performance in individuals with RBD is
required to shed light on these hypotheses, especially
because other studies (e.g., Kave
´et al., 2010) have
obtained SVF results similar to the present ones in a sam-
ple of patients with traumatic brain injury.
Another possible explanation for the differences in
performance between control participants and indivi-
duals with RBD was offered by Goulet, Joanette,
Sabourin, and Giroux (1997), who discussed differences
between SVF and PVF performance in RBD. These
authors challenged the notion that SVF impairments
would be more pronounced in individuals with RBD
VF DISSOCIATIONS 7
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due to this hemisphere’s role in the semantic component
of word processing. The authors focused instead on the
concept of associative productivity (or word pro-
ductivity), which refers to the number of words associa-
ted with a particular verbal stimulus. The authors
posited that differences in the associative productivity
of production criteria in verbal fluency tasks may be a
confounder and may influence results regarding fluency
performance in individuals with RBD. To verify this
hypothesis, the performance of healthy participants
was compared to that of individuals with RBD on SVF
and PVF tasks paired in terms of associate productivity.
Results demonstrated a group effect but not a significant
criteria effect, showing that when the productivity level is
controlled for, performance is equal in PVF and SVF.
This question must be further explored in future studies.
Sustained Attention and Verbal Fluency Impairment
We had hypothesized that there would be an association
between deficits in sustained attention and impairment
in verbal fluency tasks, especially in the extended ver-
sions of the latter, due to the need to maintain strategies
over time. However, there were more dissociations than
associations, perhaps because different attentional
demands were made by the verbal fluency tasks and
the attention task. These results suggest that verbal
fluency deficits, regardless of task length and production
criterion, cannot be solely attributed to sustained
attention deficits. Lastly, although attentional deficits
are frequent in brain-damaged individuals (Hyndman
& Ashburn, 2003), the present results indicated a low
incidence of attentional deficits in this sample.
Final Considerations
The current study suggested that verbal fluency tasks
with 1-min or 2-min durations are equally efficient in
identifying deficits in individuals with RBD, especially
when a quantitative accuracy analysis is used. How-
ever, double dissociations were found, meaning that
different individuals were classified as impaired by
each version of the fluency tasks. These results suggest
that the executive function deficits identified by fluency
tasks with different durations might be different.
While deficits in the brief tasks might represent impair-
ment in automatic processes, deficits in the extended
tasks might indicate impairments in controlled pro-
cesses. Furthermore, SVF tasks seemed to identify more
deficits when compared with fluency tasks with pho-
nemic and unconstrained criteria. These results may be
due to impairments in executive abilities related to the
right hemisphere, or to the fact that control individuals
tend to produce a larger number of words in SVF as
compared with UVF and PVF, so that reductions in the
number of words produced by the clinical sample in
SVF are more evident. Finally, verbal fluency perfor-
mance did not appear to be associated with sustained
attention impairments in the sample.
The current study did have some methodological
limitations, such as the fact that the 1-min fluency task
was manipulated through statistical analysis, rather than
applied in the testing setting this way. However, it is
important to note that patients’ behavior during the
fluency task did not change as a function of the duration
described in the task’s introduction. Additionally, the
present results must be interpreted considering the caveat
of analyzing deficits by Zscore only. Future studies must
strive to use additional methods of data analysis, from
the most classical (e.g., percentile) to the most recently
developed methods of case study statistics, such as the
Bayesian approach, which uses the control sample size
and standard deviation values as a ‘‘non-informative
prior distribution for the control variance,’’ as described
by Crawford, Garthwaite, and Wood (2010, p. 381).
Furthermore, the present results are limited to populations
with RBD. Future research must investigate and discuss
word production curves over time during verbal fluency
tasks, as such analyses might reveal underlying cognitive
strategies related to verbal fluency performance. We
hypothesize that in spite of the greater productivity
observed in the first time intervals of the task, the last inter-
vals might be more clinically significant to identify some of
the executive components assessed by this task. We also
suggest that future studies take into account variables such
as fluency duration, production criteria, clustering, and
switching to obtain more knowledge about the possible
interactions between these factors. Moreover, other psy-
chiatric and neurological samples must be investigated to
understand the applicability of these clinical analyses in
neuropsychological assessment. Finally, performance in
verbal fluency tasks with different durations should be
further explored in behavioral and neuroimaging studies.
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... Most of the VFT used in the literature have a duration of 1 min. However, some studies have suggested that longer tasks may allow for a more comprehensive analysis of the executive and lexical-semantic processes involved in VF by providing a better picture of changes in these abilities over time (Fernaeus & Almkvist, 1998;Joanette, Ska, & Cô té, 2004;Zimmermann et al., 2013). The words elicited in the first seconds of VFT are usually attributed to automatic processes, because they tend to be common words that are more likely to be easily accessible and automatically retrieved. ...
... As such, VFT with longer retrieval times require more attentional and executive control than shorter instruments (Joanette et al., 2004). Additionally, in a study by Zimmermann et al. (2013), a sample of clinical patients was found to be more likely to show impairment in an extended VFT as compared with a 1-min instrument, suggesting that longer tasks may be more sensitive to executive impairment. ...
... Furthermore, the paradigms employed generally have a duration of a minute, providing limited information about the development of the participant's retrieval strategy. The UVF is also a recent topic of research; however, it has proven to be important for assessing the participant's naturalistic semantic retrieval strategies (Fernaeus & Almkvist, 1998;Joanette et al., 2004;Zimmermann et al., 2013). Thus, this study sought to further reduce the gap of developmental studies on executive processing in VFT, especially in UVF tasks and with longer duration. ...
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Aim: Considering the data on the important role of verbal fluency tasks in neuropsychological diagnosis and the models of hemispherically specialised modulation of processes essential for different types of verbal fluency, we made an attempt to identify differences in correct and incorrect performance of 5 verbal fluency tasks between patients with vascular cerebral pathology, including hypertension, and healthy individuals. We also analysed task performance profiles within the groups. Materials and methods: The study included healthy volunteers (n = 36), hypertensive individuals (n = 33), and patients after left (n = 15) or right hemisphere stroke (n = 30) – 114 subjects in total. We used the Frenchay Aphasia Screening Test (FAST) to exclude patients with significant language difficulties/aphasia. We used 5 verbal fluency tasks: semantic (Animals), phonemic (“k”), verb fluency and two emotional tasks: Joy and Fear. We used general linear models for repeated measures for the analysis of correctly and incorrectly performed tasks. Results: The profiles of correct responses for all 5 tasks were similar in all groups, with quantitative intergroup differences. The highest number of correct responses appeared in the semantic, phonemic and verb fluency tasks, whereas the lowest number in the emotional tasks. Hypertensive individuals scored statistically insignificantly lower than healthy individuals, whereas patients after right/left hemisphere stroke scored significantly lower compared to both these groups. Despite a large number of errors, healthy individuals had the highest scores. Patients after right hemisphere stroke showed little differentiation in the number of correct responses in subsequent tasks. There were no intergroup differences in the level of performance of emotional tasks with different valences (positive and negative). Healthy and hypertensive individuals were characterised by a distinct heterogeneity of correct and incorrect responses in various tasks. Patients with brain pathology, regardless of its lateralisation, performed these tasks at a similar level, with left hemisphere damage resulting in the highest number of errors, mainly in semantic and phonemic tasks, and with right hemisphere pathology associated with errors in all types of tasks. The difficulties in patients with left hemisphere damage may result from weaker phonological and lexical processes, including access to semantic features of a word, while the low scores of patients with right hemisphere damage may be a consequence of impaired attention and executive processes. Conclusions: Patients with vascular pathology of the brain hemispheres achieved significantly lower scores in all types of fluency, while hypertensive individuals scored insignificantly lower than healthy subjects. This means that the method can be useful in differentiating between healthy individuals and patients with central nervous system damage, as well as those at risk. Future research should focus on a detailed analysis of the types of errors made by patients with hemispheric damage in various types of verbal fluency tasks. An analysis of the location of the pathology in the anterior-posterior dimension of each hemisphere could reveal specific features of verbal fluency.
... Verbal fluency (VF) tasks have traditionally been administered as a clinical neuropsychological paradigm to assess linguistic, mnestic and/or executive abilities; they are also among the most widely used linguistic fMRI paradigms (1)(2)(3)(4). The cognitive components assessed by this paradigm include executive abilities, such as initiation, inhibition, planning, updating and shifting; verbal long-term memory (word knowledge), both semantic and phonological; and lexical-semantic linguistic processes (5,6). ...
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The purpose of this study was to examine the impact of age and education on the neural and behavioral correlates of verbal fluency. Forty-eight healthy adult participants were included: high-educated young and elderly, low-educated young and elderly. Participants performed semantic and phonemic and a control task during fMRI scanning. The phonemic fluency data showed an education effect across age groups. As for the semantic fluency data, there was an education effect only in young participants. The second-level fMRI results showed, in phonemic fluency, a main effect of age in the left posterior cingulate, superior temporal gyrus (STG) and right caudate, whereas the main effect of education involved activation in the right semantic fluency, there were a main effect of age in the left paracentral lobule and posterior cingulate, a main effect of education in the left claustrum and an interaction in the right claustrum and STG and the hippocampus bilaterally.
... Secondly, we only used the standard time set for VF tasks -one-minute interval -, while a two-minute protocol might be advisable. 41 Finally, the clinical implications of this study highlight the screening role of VF tasks in differentiating healthy and cognitively impaired (as in MCI and AD) individuals. Moreover, FRWH must be considered when evaluating results together with schooling and more deeply investigated at history taking during clinical and neuropsychological assessments for dementia diagnosis and prognosis, taking into account the cognitive reserve factor, and for more specific and accurate intervention planning. ...
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... Although the first time intervals of the VFT used in the present study may have been the most productive, age and school type were still found to influence performance in the final intervals of each task. Studies have shown that the last intervals of VFT rely more heavily on EF, since the words elicited at this point in the task are not as readily available in memory as those evoked in the beginning of the instrument (Hurks et al., 2006;Zimmermann et al., 2013). Automatic processes are faster and operate with relatively less conscious effort than the controlled processes which are especially required in the final intervals of VFT and tend to be slower, more effortful and more attention-dependent (Fodor, 1983;Hurks et al., 2004;Shiffrin & Schneider, 1977). ...
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We investigated the role of age and school type on clustering and switching in verbal fluency tasks (VFTs) with Brazilian children. The children were administered unconstrained, phonemic and semantic VFTs with a duration of 150 or 120 s, respectively. Both age and school type influenced all variables and in terms of performance over time. Older children and private school students outperformed the remainder of the sample, with the first 30 s of each VFT usually being the most productive. Although the size of the clusters produced did not differ between groups, the types of clusters did show some variations, with semantic clusters being the most frequent. Our results revealed strong correlations between switching ability and word production in all three VFTs. In conclusion, the executive functions known as planning and cognitive flexibility play a crucial role in word production by organising and facilitating the recall of lexical information from memory.
... Sabe-se que vários estudos comparam os diferentes níveis de severidades do TCE (Aragón, Arango-Lasprilla, Bartolomé, Fernández & Krch, 2012;Channon & Watts, 2003;Jurado, Mataro, Verger, Bartumeus & Junque, 2000;Perlstein et al., 2004;Spitzet al., 2013) na avaliação da cognição. No entanto, poucos estudos foram encontrados em que o desempenho inferior encontrado nos pacientes se dá a partir da ocorrência de déficits baseado em dados normativos propriamente dito nas múltiplas tarefas mnemônicas, atencionais (Zimmermann et al., 2014) e executivas (Anderson & Knight, 2010;Clune-ryberg et al., 2011;Fonseca et al., 2012). A frequência de déficits cognitivos tem como relevância a caracterização neuropsicológica dos quadros (leve e grave), bem como o conhecimento científico e clínico para o avanço nos focos de intervenção em avaliação e reabilitação cognitiva. ...
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Background: an assessment instrument to evaluate communication impairment after right brain damage: the Montreal Communication Evaluation Battery, an adapted brazilian version of the original canadian instrument - Protocole Montréal d'Évaluation de la Communication. Instruments that evaluate discursive, pragmatic, lexical-semantic and prosodic impairments are important for the diagnosis of communication disorders which are present in approximately 50% of the individuals with right brain damage. Systematic studies of the communication profile after lesions on this side of the brain have been carried out only during the last two decades. Aim: to present the Montreal Communication Evaluation Battery to brazilian speech therapists. Conclusion: the described instrument is an useful tool in the clinic for assessing four processes related to the communicative and linguistic abilities: discursive, pragmatic-inferential, lexical- semantic and prosodic components. It is has been normalized, validated and its reliability has been confirmed. Although this instrument was developed and adapted for diagnosing communication disorders in individuals with right brain damage people, it can also be helpful in investigating communication sequels in traumatic brain injury, dementia, bilateral frontal lesions, left-brain damage, psychopathologies,
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Fluency tasks from two categories, animals and words beginning with a specified letter (“C”, “F”, “L”), were administered to normal elderly and to elderly with mild or moderate-to-severe senile dementia of the Alzheimer type. In both tasks, normals were superior to both dementia groups, while the mild dementia group was less impaired. Normals and mild dementia subjects retrieved more animal names than “CFL” words. Compared with normals, mild dementia subjects showed a greater performance decrement on the “CFL” words task than on animal naming. Moderate-to-severe dementia subjects showed no difference between tasks. Results suggest that (1) category structure influences retrieval processes, (2) components of the structure are affected differentially during the disease process.
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Background : The nature of the contribution of the right hemisphere to the semantic processing of words is still unclear. Moreover, studies that looked at this question using a production oral naming task offered contradictory results, partly because of differences in production criteria used for this task. Aims : The goal of this study was to investigate the contribution of the right hemisphere to lexico-semantic abilities using an unconstrained oral naming task, looking at both qualitative and qualitative dimensions of the words produced, including a time-course analysis. Methods and Procedure : A total of 30 right-hemisphere-damaged (RHD), 30 left-hemisphere-damaged (LHD) without aphasia or with only a mild aphasia, and 30 control subjects (NC) were submitted to an unconstrained oral naming task. Outcome and Results : Results showed that hemisphere-damaged subjects produced fewer words than NC and that LHD produced fewer semantic categories than NC and RHD. Time-course analysis showed that, for all groups, more words were produced at the beginning of the task. Qualitatively, RHD showed a tendency to produce a lower mean degree of prototypicality than NC. Finally, the cluster analysis identified three clusters according to the overall performance, revealing an interaction between education and the presence of a brain lesion. Conclusion : Altogether, these results indicate that the impairment of the semantic processing of words following a right-hemisphere lesion might be specifically determined by the prototypicality of words, a result that has some convergence with other results in the literature at the discourse or pragmatic levels. However, results also show the existence of an interaction between the ability to look at very mild lexico-semantic impacts of a brain lesion and the influence of degree of education on these abilities. The latter result stresses the importance of a strict control of education in any studies looking at very mild language disorders in brain-lesioned individuals.