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European Journal of Neurology 2007, 14: 632–637 doi:10.1111/j.1468-1331.2007.01797.

Action and object naming in Parkinson’s disease without dementia


M. Cotellia, B. Borronib, R. Manentic, M. Zanettib, A. Arévaloc,d, S. F. Cappac and A. Padovanib
a
IRCCS S. Giovanni di Dio – Fatebenefratelli, Brescia, Italy; bDepartment of Neurology, University of Brescia, Brescia, Italy; cVita Salute
University and San Raffaele Scientific Institute, Milan, Italy; and dCenter for Research in Language, University of California at San Diego,
San Diego, CA, USA

Keywords: The present study aimed to assess the ability in objects and actions naming in Par-
language, naming, kinson’s disease (PD) patients. Further, we wished to assess the effect of a particular
Parkinson’s disease conceptual dimension, i.e. manipulability, on the naming of object and actions.
Patients were recruited from the Department of Neurology, University of Brescia.
Received 3 November 2006 Thirty-two were diagnosed as PD, according to published criteria, and 15 healthy
Accepted 12 March 2007 volunteers matched in age and education to patientsÕ sample. All patients underwent a
detailed clinical and neurological evaluation. The stimuli used in the action–object
picture naming task were taken from the Center for Research in Language-Interna-
tional Picture Naming Project corpus. To assess the effect of manipulability (or the
involvement of fine hand movements) the noun–verb stimuli were re-categorized into
manipulable and non-manipulable items (i.e. objects which can or cannot be mani-
pulated and actions which do or do not involve fine hand movements). Patients
showed a deficit both in action and object naming, compared with controls. In
addition, patients with PD but not controls were significantly more impaired in action
than in object naming. The current study supports the view that action naming is
affected in patients with PD, possibly reflecting the presence of prefrontal dysfunction.

result, a functional MRI study showed that left pre-


Introduction
frontal cortex and left parietal lobule are selectively
The prevalence, natural history and pathophysiological activated during verb production, whilst left inferior
mechanisms of cognitive dysfunction in Parkinson’s temporal lobe is involved in noun production [8].
disease (PD) are complex issues. Some studies indicate Moreover using repetitive transcranial magnetic
that non-demented patients at an early stage of PD stimulation, Shapiro et al. [9] proved that left prefrontal
already show atrophy in the hippocampus and in the cortex is selectively engaged in the production of verbs,
prefrontal cortex [1–4]. As it is known that patients at whilst Cappa et al. [10] underlined the selective
an early stage of PD can show impaired executive relevance of left prefrontal cortex in action naming.
functions and memory abilities, a magnetic resonance In the degenerative spectrum there are some
imaging (MRI) study suggested that in these patients evidences that action and object naming is impaired in
left hippocampal atrophy is related to impaired mem- frontal pathologies such as fronto-temporal dementia
ory and prefrontal atrophy is associated with impaired [11] and the dissociation between action (more
vigilance [5]. impaired) and object naming performances seems to
The neurological correlates of action naming be greater in fronto-temporal dementia than in
impairment may also be relevant for the interpretation Alzheimer’s patients [12]. Our previous study showed
of the responsible cognitive mechanisms. Several pa- the usefulness of the investigation of action naming
tient studies highlighted the involvement of different abilities in distinguishing fronto-temporal dementia
cerebral areas during noun and verb processing, from Alzheimer’s dementia and also in differentiating
suggesting that left prefrontal cortex is involved in verb the numerous clinical variants that belong to fronto-
processing whilst left temporal lobe is crucial for noun temporal dementia [11].
processing [6]. A recent PET study underlined that the The simple possibility that tasks involving verbs are
production of verbs activated a left frontal network more ÔdifficultÕ than task involving nouns seems to be
whilst the production of nouns activated a greater refuted by the observation of a double dissociation, as
temporal lobe activation [7]. In agreement with this well as by the lack of correlation with the severity of
language impairment or of dementia. Other hypotheses
Correspondence: Maria Cotelli, IRCCS S. Giovanni di Dio –
include the possible relationship of verb processing
Fatebenefratelli, Via Piastroni, 4 Brescia, Italy (tel.: +39 0303501593; impairments with grammatical disorders, typically
fax: +39 0303501513; e-mail: mcotelli@fatebenefratelli.it). associated with frontal damage [13]; a link with

632  2007 EFNS


Naming in PD 633

executive dysfunction [14]; and the relationship between dose motor fluctuations were always tested in the on
verbs and action content [15,16]. phase.
The aim of the present study was to systematically Patients with potentially confounding neurological
investigate action and object naming in a sample of and psychiatric disorders, clinically known hearing or
patients with a clinical diagnosis of PD [17]. Further- vision impairment, a past history of alcohol abuse,
more, a study on non-demented PD patients showed psychosis, or major depression, were excluded. Patients
that these patients were more impaired in verb with clinical presentations suggestive of progressive
generation tasks than in noun generation tasks. In the supranuclear palsy (PSP), multiple systemic atrophy or
same study, the authors showed a negative correlation vascular Parkinsonism were also excluded. The use of
between error rate in verb generation task and the medication that could interfere with test performance
performance in the memory subtest of the Dementia or diagnosis was considered as a further exclusion cri-
Rating Scale [18]. PD disease affects prefrontal areas, as terion. The use of psychopharmacological agents that
well as other cortical and subcortical structures in- could interfere with test performance (antipsychotics,
volved in action organization and motor control: the benzodiazepines) was considered as a further exclusion
presence of a verb deficit would support theories which criterion. Only patients without dementia were included
predicate a relationship between action representation in the study (Clinical Dementia Rating ¼ 0).
and verb processing [19,20]. The study also included a control group of 15 healthy
Given that both phonemic and semantic fluency are volunteers, matched in age and education to our patient
impaired in PD patients [17], there is the possibility that sample. All healthy volunteers performed a clinical and
the difficulty of the task may have differentially affected neurological examination, and the same patientsÕ
noun and verb generation. The present study investi- exclusion criteria were considered.
gates action and object naming abilities in PD patients. All participants were made fully aware about the
In particular, the prediction was a greater impairment aims of the research and the signature of an informed
of action naming compared with object naming in the consent was sought from all subjects. The work was
case of non-demented PD. conducted in accordance with local clinical research
The role of specific semantic factors in action naming regulations and conformed to the Helsinki
has not been frequently investigated. We thus tested the Declaration.
impact of a semantic variable, i.e. manipulation, on
naming performance by re-categorizing the action
Neuropsychological assessment
stimuli into stimuli which do or do not involve fine
hand movements. Baseline cognitive assessment included screening tests
Finally, we investigated the relationship between for global cognitive decline [Mini-Mental State Exam-
naming performance and other cognitive functions. ination (MMSE)], tests of non-verbal reasoning (Ra-
ven’s Colored Matrices), verbal fluency with phonemic
and semantic cues, memory for prose (logical memory),
Methods
constructional abilities and visuo spatial recall (Rey’s
Complex figure), and attention and executive function
Subjects
(Trail Making A and B) [22].
Thirty-two PD patients were recruited from the Center
for Movement Disorders, Department of Neurology,
Experimental evaluation: action–object naming
University of Brescia. Clinical diagnoses were estab-
lished by experienced neurologists on the basis of aki- The stimuli used in the action–object picture naming
nesia associated with one of the other two cardinal signs (PN) task were taken from the Center for Research in
(tremor, rigidity) and responsiveness to levodopa ther- Language-International Picture Naming Project corpus
apy. All patients fulfilled the UK Parkinson’s Disease CRL-IPNP [23], which contains 795 black and white 2-
Brain Bank criteria for the diagnosis of idiopathic PD D line drawings representing actions and objects. These
[21]. items have been tested and normed in healthy and pa-
All patients underwent a detailed clinical and neu- tient populations across seven different international
rological evaluation. A structural brain imaging study sites and languages. Items are coded for a number of
was performed in each patient. variables known to influence naming difficulty.
The motor disability was evaluated using the motor Amongst others, these are initial word frequency, age of
examination section of the Unified Parkinson’s Dis- acquisition, and picture imageability scores, which were
ease Rating Scale (UPDRS-III) [22] and using Hoehn tested to see whether they significantly influenced par-
and Yahr Scale (mean 1.66). Patients who had end-of- ticipantsÕ naming performance.

 2007 EFNS European Journal of Neurology 14, 632–637


634 M. Cotelli et al.

For this particular set of patients we used a subset of mouth, foot and whole body) was excluded from sub-
120 items from the original corpus. These were 60 ac- sequent analyses, in order to avoid any obvious con-
tions and 60 objects, with half (30) of the items in each founds [26]. Of 60 action items, 28 were classified as
category being ÔeasyÕ and half ÔdifficultÕ. The difficulty Ômanipulation actionsÕ and 11 as Ônon-manipulation
was defined on the basis of native Italian participantsÕ actionsÕ. The patientsÕ performance was re-analyzed
reaction times (RTs) in previous norming studies, using after re-categorization of the action items according to
the Italian-language adaptation of the stimuli. A subset this classification.
of these items were then assigned to difficulty bins,
where all items with mean RTs of at least 2 standard
Statistical analysis
deviations above the grand mean classed as ÔdifficultÕ,
and items with RTs at least 2 standard deviations below Demographic and clinical data between patients and
the mean classed as ÔeasyÕ. All the selected stimuli were controls were compared using Mann–Whitney U-test or
high-imagery items. chi-square test. Scores were compared using analyses of
The nouns and verbs corresponding to the set of variance (ANOVA) and post-hoc planned comparisons.
objects and actions were matched for word frequency Non-parametric correlation analyses were used to as-
and word length [24]. The items were presented to each sess between significantly impaired scores. All values
participant in three pre-randomized orders. Each par- are expressed as mean ± standard deviation. The sig-
ticipant (patients and controls) was asked to orally nificant level was set at P < 0.05. Analyses were con-
name each test stimulus as it was presented. ducted using a statistical software (SPSS Inc., Chicago,
In order to test the impact of manipulability on the IL, USA).
processing of nouns and verbs we re-categorized the
action stimuli into actions which do or do not involve
Results
fine hand movements, using an objective categorization
method, based on the assessment of the gestural re-
Confrontation Naming
sponses produced by a sample of normal subjects pre-
sented with the written actions [25]. For example, Thirty-two PD patients and 15 controls entered the
actions that involve fine hand movements are Ôto study. Demographic and clinical characteristics are
squeezeÕ or Ôto cutÕ, whilst an action that does not in- shown in Table 1.
volve fine hand movements is Ôto flyÕ (see Fig. 1). For No differences in MMSE [26] scores between PD
this further categorization participants were asked to patients and controls was found.
read the target words for the same noun–verb stimuli In regard to normative data, approximately one-third
and produce Ôthe first posture, movement or expressionÕ (28%) of the patients showed an impairment of visuo-
that came to their mind when thinking about the item. spatial recall (Rey Recall), whereas one-half (56%) of
Videotaped gestures were then coded according to a the patients showed an impairment of constructional
complex rating system based on the apraxia literature. abilities (Rey Copy). Furthermore, one-third (31%) of
An item was considered as ÔmanipulableÕ if at least 70% the patients showed an impaired verbal long-term
of participants who gestured to it produced obvious memory (Story Recall), and one-fourth (25%) showed
fine-grained movements of the fingers (especially in a an impairment of attentional resources (Trail Making
grasping motion); all other items were classified as Ônon- section A). The incidence of more pronounced neuro-
manipulableÕ. In addition, any item which also elicited psychological impairment as measured by abnormal
significant involvement of other major body parts (i.e.

Table 1 Demographic and clinical data in patients with Parkinson’s


disease (PD) and controls

Variable PD Controls P value

Number 32 15 –
Age, years 69.59 ± 7.4 63.4 ± 3.7 n.s.
Gender, female % 43% 42% n.s.
Education, years 7.06 ± 3.5 8.6 ± 2.1 n.s.
Age at onset, years 63.9 ± 9 – –
UPDRS-III 18.4 ± 14 0 0.0001
MMSE 27.5 ± 2.2 28.5 ± 0.9 n.s.

MMSE, Mini-Mental State Examination; UPDRS-III, Unified


Figure 1 Examples of manipulable and non-manipulable actions. Parkinson Disease Rating Scale.

 2007 EFNS European Journal of Neurology 14, 632–637


Naming in PD 635

Objects Table 2 Parkinson’s disease patientsÕ performance on a general


Actions standard neuropsychological assessment
100 *
Mean SD Cut-off
90
Non-verbal reasoning
80 CPM Raven [22] 21.7 5.1 18
70 Language
Controlled association letters test [22] 24.7 10 17
60 Controlled association categories test [22] 30.1 7.3 25
Memory
50 Story recall [22] 7.17 3.2 8
Rey recall figure [36] 10.1 7.4 9.47
40
PD C Constructional abilities
Rey copy figure [36] 23.4 7.1 28.88a
Figure 2 Mean scores for oral action and object naming in each Attentional and executive functions
group. PD: Parkinson’s disease, C: control subjects. Results are Trailtest A [22] 63.5 46 93
expressed as mean of percentage of correct responses. *Action– Trail making test B [22] 145.6 89 282
object naming, P < 0.05. Trail making test B ) A [22] 94.9 50 186
a
Score below cut-off.
performance in more than two tests was of three
patients (Table 2). (a) 40 Visuo spatial long term memory
In order to compare PD patients and normal con- 35
trolsÕ performances, a 2 (PD versus controls) · 2 (ob- 30
Raw scores

ject versus action) ANOVA was performed. This analysis 25


showed a significant effect of kind of stimulus 20
[F(1,45) ¼ 36.104, P < 0.001]; group [F(1,45) ¼ 15
512.654, P < 0.001] and interaction [F(1,45) ¼ 41.763, 10
P < 0.001]. Planned comparisons underlined that PD 5
patients showed a deficit both in action and object 0
naming, compared with controls (object naming: 0 10 20 30 40 50 60

P < 0.001; action naming:, P < 0.001). In addition, Dissociation

patients with PD but not controls were significantly (b) 18 Verbal long term memory
more impaired in action naming than in object naming 16

(objects mean ¼ 89.69 ± 10.07 versus actions mean ¼ 14


Raw scores

65.26 ± 21.47; P < 0.001). Means scores on oral 12

naming of nouns and verbs are reported in Fig. 2. 10


8
The effect of manipulation was analyzed, comparing
6
errors in the naming of manipulation and non-mani-
4
pulation action stimuli (action that do or do not involve
2
fine hand movements). We performed a repeated
0
measure ANOVA with Manipulability as within-subject 0 10 20 30 40 50 60
factor and Group (PD, control subjects) as between- Dissociation
subject factor. The main effects and interaction were
not significant. Figure 3 Correlation between dissociation of action/object nam-
ing and cognitive and neuropsychological scores. (a) Visuo-spatial
In particular, the difference between manipulable
recall, R2 ¼ 0.25; (b) verbal memory, R2 ¼ 0.22.
actions score and non-manipulable actions score was
not significant for PD subjects (manipulation mean ¼
20.9 ± 14.5 versus non-manipulation mean ¼ significant correlation between dissociation scores and
24.1 ± 19.9). These data indicate that the Ômanipula- visual spatial recall task (R ¼ )0.470, P < 0.009) and
tionÕ factor does not influence picture naming in PD memory for prose (R ¼ )0.438, P < 0.013) (see
patients. Fig. 3).
Finally, the correlation between dissociation scores in
action and object naming and neuropsychological tests
Discussion
was further analyzed.
A regression analysis controlling for age and MMSE The present findings provide additional evidence that
was performed. Regression models demonstrated a verb processing is impaired in PD, using a confrontation

 2007 EFNS European Journal of Neurology 14, 632–637


636 M. Cotelli et al.

naming task rather than verbal fluency [18,27]. Non- not of PSP, providing a further element supporting the
demented PD patients were significantly more impaired relationship between naming and action. Moreover,
in action naming than control subjects. We found a Soliveri et al. [35] reported that, whilst both CBD and
significant discrepancy between actions and objects PSP patients are impaired on apraxia tests, the qualit-
naming in these patients, but not in control subjects. ative features of errors were different, with more severe
The severe impairment in verb retrieval in PD impairment of simple limb movement in CBD. It is
patients could be the consequence of dopamine deple- remarkable that a similar manipulation effect was
tion in the striatum, disrupting the function of sub- found in AD, in which limb apraxia can also be
cortical prefrontal networks [28]. Both lesion and observed. However, we failed to observe a manipula-
imaging studies have supported the hypothesis of a tion effect in the case of PD. It is noteworthy that PD
central role of the left prefrontal and parietal areas in patients are not clinically characterized by an impair-
verb processing [29]. In particular, Perani et al. [30] ment of simple limb movement. Imaging studies may
using a lexical decision task found that some left hem- provide further insights about the relationship amongst
ispheric areas, including the dorsolateral frontal and the location of prevalent cortical involvement, the
lateral temporal cortex, were activated only by verbs, pattern of lexical impairment and the specific feature of
whilst there were no brain areas more active in response high-order motor dysfunction in these conditions.
to nouns. More recently, using event-related MRI,
Shapiro et al. [8] found verb-specific responses in the
Disclosure
left prefrontal and parietal areas, whilst noun-specific
activations involved the inferior temporal lobe. The The authors have reported no conflicts of interest.
present finding supports the hypothesis of a central role
played by prefrontal cortex in action naming. The
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