Action and object naming in frontotemporal dementia, progressive supranuclear palsy, and corticobasal degeneration

Neuropsychology 2006, Vol. 20, No. 5, 558 –565

Copyright 2006 by the American Psychological Association 0894-4105/06/$12.00 DOI: 10.1037/0894-4105.20.5.558

Action and Object Naming in Frontotemporal Dementia, Progressive Supranuclear Palsy, and Corticobasal Degeneration M. Cotelli

B. Borroni

Istituto di Ricovero e Cura a Carattere Scientifico San Giovanni di Dio—Fatebenefratelli and University of Turin

University of Brescia

R. Manenti

A. Alberici

Istituto di Ricovero e Cura a Carattere Scientifico San Giovanni di Dio—Fatebenefratelli, Vita-Salute San Raffaele University, and San Raffaele Scientific Institute

Istituto di Ricovero e Cura a Carattere Scientifico San Giovanni di Dio—Fatebenefratelli

M. Calabria

C. Agosti

Istituto di Ricovero e Cura a Carattere Scientifico San Giovanni di Dio—Fatebenefratelli and University of Padua

University of Brescia

A. Are´valo

V. Ginex and P. Ortelli

Vita-Salute San Raffaele University, San Raffaele Scientific Institute, and University of California, San Diego

Vita-Salute San Raffaele University and San Raffaele Scientific Institute

G. Binetti and O. Zanetti

A. Padovani

Istituto di Ricovero e Cura a Carattere Scientifico San Giovanni di Dio—Fatebenefratelli

University of Brescia

S. F. Cappa Vita-Salute San Raffaele University and San Raffaele Scientific Institute Action naming has been reported to be disproportionately impaired in comparison to object naming in patients with frontotemporal dementia (FTD). This finding has been attributed to the crucial role of frontal cortex in action naming. The investigation of object and action naming in the different subtypes of FTD, as well as in the related conditions of progressive supranuclear palsy (PSP) and corticobasal degeneration (CBD), may thus contribute to the elucidation of the cerebral correlates of the action– object discrepancy as well as provide clues to the underlying cognitive mechanisms. The results indicated that, with the exception of semantic dementia, action naming was more impaired than object naming in all patient groups. The discrepancy was similar in frontal variant of FTD and Alzheimer’s disease patients, whereas patients with nonfluent primary progressive aphasia, PSP, and CBD were significantly more impaired in the oral production of actions than of objects. These findings indicate that action naming impairment is not a general feature of FTD, but rather is associated with conditions that affect the frontoparietal–subcortical circuits involved in action knowledge and action representation. Keywords: frontotemporal dementia, language impairment, naming

Several studies have reported that patients with frontotemporal dementia (FTD) are more severely impaired in tasks that involve verb, rather than noun, processing. Cappa et al. (1998) reported

that although both FTD and Alzheimer’s disease (AD) groups were impaired in object naming, in the case of actions the discrepancy between object and action naming was significantly larger in

M. Cotelli, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Giovanni di Dio—Fatebenefratelli, Brescia, Italy, and Center for Cognitive Science, Department of Psychology, University of Turin, Turin, Italy; B. Borroni and C. Agosti, Department of Medical Sciences, Neurological Clinic, University of Brescia, Brescia, Italy; R. Manenti, IRCCS San Giovanni di Dio—Fatebenefratelli and Department of Neuroscience and San Raffaele Turro Neurology, Vita-Salute San Raffaele University and San Raffaele Scientific Institute, Milan, Italy; A. Alberici, G. Binetti, and O. Zanetti, IRCCS San Giovanni di Dio—Fatebenefratelli; M. Calabria, IRCCS San Giovanni di Dio—Fatebenefratelli and Department of General Psychology, University of Padua, Padua, Italy; A. Are´valo, Department of Neuroscience and San Raffaele Turro Neurology, Vita-Salute San Raffaele University and San Raffaele

Scientific Institute, and Center for Research in Language, University of California, San Diego; V. Ginex, P. Ortelli, and S. F. Cappa, Department of Neuroscience and San Raffaele Turro Neurology, Vita-Salute San Raffaele University and San Raffaele Scientific Institute; A. Padovani, Department of Medical Sciences, Neurological Clinic, and Center for Neurodegenerative Disorders and Behavioral Disorders, EULO, University of Brescia. We wish to thank Marcella Broli, as well as Arianna Fogliata for her help with clinical assistance. We also thank the patients and caregivers for their patience. Correspondence concerning this article should be addressed to S. F. Cappa, Vita-Salute San Raffaele University, DIBIT Via Olgettina 58, 20132, Milano, Italy. E-mail: [email protected] 558

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FTD than in AD patients, independent of the severity of dementia or of overall language impairment. Rhee, Antiquena, and Grossman (2001) found that FTD patients were significantly less accurate and required significantly longer response times to make word–picture matching decisions about verbs compared with nouns. These results were considered to support the hypothesis, based on focal lesion studies, of a central role of the frontal lobe in verb processing (see reviews in Cappa & Perani, 2003; Shapiro & Caramazza, 2003). The results of imaging studies in normal subjects have partially supported this hypothesis. Using a lexical decision task, Perani et al. (1999) found that some left hemispheric areas, including the dorsolateral frontal and lateral temporal cortex, were activated only by verbs, whereas there were no brain areas more active in response to nouns. More recently, using event-related MRI, Shapiro, Moo, and Caramazza (2006) found verb-specific responses in the left prefrontal and parietal areas, whereas noun-specific activations involved the inferior temporal lobe. The diagnostic label of FTD encompasses a number of heterogeneous clinical presentations, in which different patterns of neuropsychological impairment in linguistic processing, executive function, and action organization reflect the location of the underlying pathology. Regional differences in brain atrophy reflect the clinical features of the varieties of frontotemporal degeneration. Studies with voxel-based morphometry have shown that nonfluent primary progressive aphasia (NfPPA) is characterized by left inferior frontal and insular atrophy (Gorno-Tempini et al., 2004), whereas in semantic dementia (SD) the brunt of damage is to the anterior temporal lobe (Gorno-Tempini et al., 2004). The frontal variant of FTD (FvFTD) is characterized by atrophy of the anterior insula bilaterally, the right middle frontal gyrus, the left anterior cingulate gyrus, the left medial superior frontal gyrus, and the left premotor cortex (Rosen et al., 2002). Two other conditions, progressive supranuclear palsy (PSP) and corticobasal degeneration (CBD), which overlap both clinically and neuropathologically with FTD and are considered by some authorities to be part of the same pathological spectrum (for a review, see Kertesz & Munoz, 2004), are associated with a relatively specific pattern of cortical atrophy. CBD is characterized by an asymmetric (left ⬎ right) pattern of brain atrophy that involves the bilateral premotor cortex, superior parietal lobes, and striatum, whereas PSP is associated with atrophy of the midbrain, pons, thalamus, and striatum, with minimal involvement of the frontal cortex (Boxer et al., 2006; Padovani et al., 2006). The neurological correlates of action-naming impairment may also be relevant for the interpretation of the responsible cognitive mechanisms. The simple possibility that tasks involving verbs are more difficult than tasks involving nouns seems to be refuted by the observation of a double dissociation as well as by the lack of correlation with the severity of language impairment or of dementia. Other hypotheses include the possible relationship of verbprocessing impairments with grammatical disorders, typically associated with frontal damage (Berndt, Mitchum, Haendiges, & Sandson, 1997), a link with executive dysfunction (Silveri, Salvigni, Cappa, Della Vedova, & Puopolo, 2003), and the relation between verbs and action content. It is noteworthy that Rhee et al. (2001) found a correlation between executive dysfunction, assessed with such tests as the Stroop and Trail Making, and defec-

tive verb comprehension only in patients with FvFTD. In the case NfPPA, the significant correlation was with sentence comprehension. This finding suggests that different mechanisms of impairment may be responsible for defective verb processing. Similarly, Silveri et al. (2003) found a stronger correlation between actionnaming deficit and severity of dementia in the FvFTD than in AD. The correlation analysis also suggested that the naming disorder was due to a dysexecutive deficit in FTD and to the linguistic disorder in AD. We report a systematic investigation of object and action naming and comprehension in a relatively large sample of patients with a clinical diagnosis of FTD, which included all three subtypes of the disorder—FvFTD, NfPPA, and SD—as well as in PSP and CBD. The aim was to assess for the presence of a verb-processing impairment within these subgroups, which are characterized by different patterns of cognitive and linguistic impairment as well as by different locations of the pathological process. In particular, the prediction was of a more severe involvement of action naming in the variety associated with inferior frontal damage (NfPPA) than in FvFTD and SD. In the case of CBD and PSP, the predictions were less clear-cut. Although neither condition is typically associated with prominent language impairment, a verb deficit has been reported in PSP by Daniele, Giustolisi, Silveri, Colosimo, and Gainotti (1994) and more recently by Bak et al. (2006). Because both diseases affect prefrontal areas, as well as other cortical and subcortical structures involved in action organization and motor control, the presence of a verb deficit would support theories that predicate a relationship between action representation and verb processing (Pulvermuller, 2005; Pulvermuller, Hauk, Nikulin, & Ilmoniemi, 2005).

Method Patient and Control Groups Patients were recruited from the Department of Neurology of the University of Brescia, the San Raffaele Turro Neurology Department, and the Memory Clinic of the Centro San Giovanni di Dio Fatebenefratelli Scientific Institute of Brescia, Italy. Twenty-four patients were diagnosed as affected by FTD according to published criteria (Davis, Price, Moore, Campea, & Grossman, 2001; McKhann et al., 2001; Neary et al., 1998; Price, Davis, Moore, Campea, & Grossman, 2001). This group included 16 patients with FvFTD, 6 patients with a fluent form of progressive aphasia (also known as SD), and 2 patients with NfPPA. The subtype diagnosis, based on the criteria mentioned above, was confirmed at follow-up (minimum 1 year). Ten were diagnosed as probable PSP according to National Institute of Neurological Disease and Stroke PSP criteria (Litvan et al., 1997), and 10 had a clinical diagnosis of CBD (Lang, 1994). To assess the impact of dementia on action naming, we also included 10 patients diagnosed with probable AD, based on criteria from the National Institute of Neurological and Communication Disorders and Stroke— Alzheimer’s Disease and Related Disorders Association (McKhann et al., 1984), as well as 10 healthy volunteers, matched for age and education. The latter group had normal neurological examinations and brain MRIs, with no history of mental illness or cognitive decline. All patients underwent a detailed clinical and neurological evaluation. A motor examination was conducted and the levodopa response was measured with the motor examination section of the Unified Parkinson’s Disease Rating Scale. Upper limb apraxia was evaluated with a movement imitation test (De Renzi, Motti, & Nichelli, 1980). Only CBD patients were

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impaired on the latter test. Routine laboratory tests, including thyroid hormone dosage, vitamin B12, serum folate, and serologic test of syphilis, were taken for all patients. Each patient underwent a structural brain MRI, and visual ratings of MRI images documented frontotemporal atrophy. Voxel-based analysis was performed in each group and confirmed previous reports (Padovani et al., 2006). Patients with potentially confounding neurological and psychiatric disorders, clinically known hearing or vision impairment, a past history of alcohol abuse, psychosis, or major depression, and MRI evidence of relevant cerebrovascular changes were excluded from the study. The use of psychopharmacological agents that could interfere with test performance or diagnosis was considered as a further exclusion criterion. Only patients with a mild form of cognitive decline were included (Clinical Dementia Rating ⫽ 0.5 to 1; Mini-Mental State Examination [MMSE; Folstein, Folstein, & McHugh, 1975] score ⬎ 18). Demographic and clinical data of patients and control participants are reported in Table 1. We performed a one-way analysis of variance (ANOVA) with MMSE as a within-subjects factor and Group (FvFTD, SD, PSP, CBD, AD, controls) as a between-subjects factor. The results indicated a significant effect of group, F(5, 56) ⫽ 9.277, p ⬍ .0001. Post hoc analysis showed that the control group performed significantly better than FvFTD ( p ⬍ .003), SD ( p ⬍ .0001), and AD ( p ⬍ .0001) patients. Cognitive assessment was followed by an experimental evaluation on a second visit. Baseline cognitive assessment included screening tests for dementia (MMSE and Clinical Dementia Ratings) and tests of nonverbal reasoning (Raven’s Colored Matrices); auditory language comprehension (Token Test); verbal fluency with phonemic and semantic cues; verbal short-term memory (Digit Span Forward); long-term memory for prose (logical memory), constructional abilities, and visual spatial recall (Rey’s Complex Figure); attention; and executive function (Trail Making A and B; Lezak, Howieson, & Loring, 2004).

Experimental Evaluation: Action–Object Naming The stimuli used in the action– object picture-naming task were taken from the Center for Research in Language—International Picture-Naming Project corpus (Bates et al., 2000), which contains 795 black and white two-dimensional line drawings representing actions and objects. These items have been tested and normed in healthy and patient populations across seven different international sites and languages. Items are coded for a number of variables known to influence naming difficulty. Among others, these are initial word frequency, age of acquisition, and picture imageability scores, which were tested to see whether they significantly influenced participants’ naming performance. For this particular set of patients, we used a subset of 120 items from the original corpus. These were 60 actions and 60 objects, with half (30) of the items in each category being easy and half difficult. We defined difficulty on the basis of native Italian participants’ reaction times (RTs) in previous norming studies, by using the Italian-language adaptation of the stimuli. A

subset of these items was then assigned to difficulty bins, where all items with mean RTs of at least two standard deviations above the grand mean were classified as “difficult,” and items with RTs at least two standard deviations below the mean were classified as “easy.” All the selected stimuli were high-imagery items. The nouns and verbs corresponding to the set of objects and actions were matched for word frequency and word length (De Mauro, Mancini, Vedovelli, & Voghera, 1994). The items were presented to each participant in three prerandomized orders. Each participant (patients and controls) was asked to orally name each test stimulus as it was presented. For the comprehension assessment, participants performed action– object comprehension tasks taken from the Battery for Analysis of the Aphasic Deficits (Miceli, Laudanna, Burani, & Capasso, 1994). The stimuli for this task also included black and white line-drawn figures representing objects and actions, and items were presented both in auditory and visual forms in a word–picture matching task. Finally, we also tested the impact of a semantic variable, that is, manipulation, on the current data by recategorizing the action stimuli into actions that do or do not involve fine hand movements, by using an objective categorization method based on the assessment of the gestural responses produced by a sample of normal subjects presented with the written actions (Are´valo, Butler, Perani, Cappa, & Bates, 2005). For this further categorization, participants were asked to read the target words for the same noun–verb stimuli and produce “the first posture, movement, or expression” that came to their mind when thinking about the item. Videotaped gestures were then coded according to a complex rating system based on the apraxia literature. An item was considered “manipulable” if at least 70% of participants who gestured to it produced obvious fine-grained movements of the fingers (especially in a grasping motion); all other items were classified as “nonmanipulable.” In addition, we excluded from subsequent analyses any item that also elicited significant involvement of other major body parts (i.e., mouth, foot, or whole body), in order to avoid any obvious confounds (Ehrsson, Geyer, & Naito, 2003). The patients’ performance was reanalyzed after recategorization of the action items according to this classification.

Results Action and Object Naming We performed a repeated measures ANOVA with Stimulus Category (object and action) as a within-subjects factor and Group (FvFTD, SD, PSP, CBD, AD, controls) as a between-subjects factor. The results indicated significant effects of both stimulus category, F(1, 56) ⫽ 80.8, p ⬍ .0001, ␩2 ⫽ .591, and the Stimulus ⫻ Group interaction, F(5, 56) ⫽ 10.03, p ⬍ .0001, ␩2 ⫽ .473. The mean scores on oral naming of objects and actions for each group of patients are summarized in Figure 1.

Table 1 Demographic and Clinical Data FvFTD (n ⫽ 16)

NfPPA (n ⫽ 2)

SD (n ⫽ 6)

PSP (n ⫽ 10)

CBD (n ⫽ 10)

AD (n ⫽ 10)

Controls (n ⫽ 10)

Variable

M

SD

M

SD

M

SD

M

SD

M

SD

M

SD

M

SD

Age (years) Education (years) MMSE

64.8 9.7 20.3

9.1 4.2 6.1

68.8 12.0 22.2

8.8 3.9 4.8

62.5 9.0 25.0

10.0 5.7 4.2

70.5 9.3 27.4

8.3 5.6 2.1

63.8 6.0 25.3

6.2 2.8 2.6

75.0 8.0 22.4

6.1 3.2 1.8

63.4 8.6 28.9

3.7 2.1 0.7

Note. FvFTD ⫽ frontal variant of frontotemporal dementia; SD ⫽ semantic dementia; NfPPA ⫽ nonfluent primary progressive aphasia; PSP ⫽ progressive supranuclear palsy; CBD ⫽ corticobasal degeneration; AD ⫽ Alzheimer’s disease; MMSE ⫽ Mini-Mental State Examination.

ACTION AND OBJECT NAMING

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Figure 1. A: Oral action and object naming in FvFTD, SD, PSP, CBD, AD, and control patients. B: Oral action and object naming in NfPPA patients and controls. Results are expressed as the mean percentage of correct responses. FvFTD ⫽ frontal variant of frontotemporal dementia; SD ⫽ semantic dementia; PSP ⫽ progressive supranuclear palsy; CBD ⫽ corticobasal degeneration; AD ⫽ Alzheimer’s disease; C ⫽ control; NfPPA-1 ⫽ nonfluent primary progressive aphasia (Patient 1); NfPPA-2 ⫽ nonfluent primary progressive aphasia (Patient 2). *p ⬍ .05, action naming versus object naming.

We performed post hoc analyses (Tukey tests) to compare patients’ and controls’ performance. These analyses revealed that the average naming deficits (for actions and objects) in FvFTD, SD, PSP, CBD, and AD patient groups differed significantly from control subject performance (FvFTD vs. control subjects: p ⬍ .0002; SD vs. control subjects: p ⬍ .0001; PSP vs. control subjects: p ⬍ .006; CBD vs. control subjects: p ⬍ .05; AD vs. control subjects: p ⬍ .02). The performance of the 2 patients with NfPPA was compared with the average performance of control subjects. Chi-square analysis performed on counts of correct responses showed that NfPPA patients were more impaired in naming than controls, ␹2(1, N ⫽ 2) ⫽ 59.71 p ⬍ .0001. Simple contrasts revealed that patients with FvFTD, PSP, CBD, and AD were significantly more impaired in oral naming of actions than objects (FvFTD: p ⬍ .003; PSP: p ⬍ .0001; CBD: p ⬍ .0001; AD: p ⬍ .001). Chi-square analysis performed on NfPPA patients’

performances showed that they were significantly more impaired in oral naming of actions than objects (correct response mean ⫾ standard deviation: objects ⫽ 71.65 ⫾ 33.02 vs. actions ⫽ 32.50 ⫾ 27.15), ␹2(1, N ⫽ 2) ⫽ 30.45, p ⬍ .0001. In contrast, there were no differences between object and action naming in patients with SD. Patients in the PSP and CBD groups displayed significantly larger discrepancies than did FvFTD patients (Tukey test: PSP, p ⬍ .004: PSP ⬎ FvFTD ⬎ control subjects; CBD, p ⬍ .003: CBD ⬎ FvFTD ⬎ control subjects). NfPPA patients displayed significantly larger discrepancies than did control subjects, ␹2(1, N ⫽ 2) ⫽ 16.32, p ⬍ .001. However, the discrepancy between action and object naming was not significantly different between FvFTD and AD patients. For a qualitative error analysis, see Table 2. Errors were classified into the following categories: semantically related errors (e.g., bicchiere [“glass”] ⱖ bottiglia [“bottle”]), semantically un-

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Table 2 General Distribution of the Various Error Types Made by Different Groups in Action and Object Naming Error

FvFTD

SD

NfPPA

PSP

CBD

AD

23 4 11 0 31 0 31

49 12 0 0 24 0 15

28 9 0 0 51 0 12

40 30 10 0 14 0 6

5 2 62 9 0 22

52 15 0 0 0 33

35 26 0 0 0 39

40 25 2 0 0 33

Action Semantically related Semantically unrelated Phonologically related Phonologically unrelated Substitution with noun Semantic error on stem Anomia

45 19 3 0 31 0 2

57 18 1 0 17 0 7 Object

Semantically related Semantically unrelated Phonologically related Phonologically unrelated Substitution with noun Anomia

43 16 11 2 0 20

22 30 0 0 4 44

Note. Results are expressed as the mean percentage of errors. FvFTD ⫽ frontal variant of frontotemporal dementia; SD ⫽ semantic dementia; NfPPA ⫽ nonfluent primary progressive aphasia; PSP ⫽ progressive supranuclear palsy; CBD ⫽ corticobasal degeneration; AD ⫽ Alzheimer’s disease.

related errors (e.g., bastone [“walking stick”] ⱖ strada [“street”]), phonologically related errors (e.g., tavolo [“table”] ⱖ favolo), phonologically unrelated errors (e.g., sedia [“chair”] ⱖ febie), substitution with noun (e.g., casa [“house”] ⱖ fiore [“flower”]), semantic errors on stem (e.g., camminare [“to walk”] ⱖ piedere [“foot” ⫹ verb]), and anomia. To determine whether the interaction was due to the confounding influence of age, education, and MMSE score, we conducted an analysis of covariance with age, education, and MMSE as covariates. We used as a dependent variable the difference score (object-naming score minus action-naming score). The analysis showed again the group effect, F(5, 53) ⫽ 8.66, p ⬍ .0001; and the post hoc analysis (Tukey test) confirmed the discrepancy differences described before (FvFTD ⬍ CBD: p ⬍ .004; FvFTD ⬍ PSP: p ⬍ .004). In contrast, the discrepancy between action and object naming was not significantly different between FvFTD and AD patients.

Understanding Action and Object Names We performed a repeated measures ANOVA with Stimulus Category (object and action) as the within-subjects factor and Group (FvFTD, SD, PSP, CBD, AD, controls) as the betweensubjects factor. The results indicated a significant Stimulus ⫻ Group interaction effect, F(5, 56) ⫽ 7.75, p ⬍ .0001, ␩2 ⫽ .418; and a group effect, F(5, 56) ⫽ 10.66, p ⬍ .00001, ␩2 ⫽ .488. Mean scores on comprehension of actions and objects for each patient group are summarized in Figure 2. Post hoc analysis (Tukey test) showed that SD patients performed significantly worse than other patient groups and control subjects. In object–action comprehension tasks, only FvFTD, SD, and AD patients differed significantly from control participants; FvFTD: object comprehension, F(1, 56) ⫽ 4.46, p ⬍ .05; action comprehension, F(1,

56) ⫽ 12.41, p ⬍ .0009; SD: object comprehension, F(1, 56) ⫽ 149.8, p ⬍ .0001; action comprehension, F(1, 56) ⫽ 10.869, p ⬍ .002; AD: object comprehension, F(1, 56) ⫽ 3.75, p ⫽ .05; action comprehension, F(1, 56) ⫽ 5.86, p ⬍ .02. In addition, the same groups showed an object–action dissociation in the comprehension task; FvFTD: F(1, 56) ⫽ 30.96, p ⬍ .00001; SD: F(1, 56) ⫽ 10.13, p ⬍ .003; AD: F(1, 57) ⫽ 8.84, p ⬍ .005.

Naming of Manipulation and Nonmanipulation Actions Of 60 action items, 28 were classified as manipulation actions, and 11 were classified as nonmanipulation actions (see Figure 3). The analyses were conducted on the percentage of correct responses. Specifically, for each diagnostic group, we divided the number of correct answers by the total number of manipulation (or nonmanipulation) items presented to each participant. We performed a repeated measures ANOVA with Manipulation Actions as the within-subjects factor and Group (FvFTD, SD, PSP, CBD, AD) as the between-subjects factor. Results indicated a significant Group ⫻ Manipulation Actions interaction, F(4, 47) ⫽ 3.00, p ⬍ .03, ␩2 ⫽ .203. Mean scores on action oral naming are summarized in Figure 4. Simple contrasts revealed that the difference between manipulation and nonmanipulation actions was significant for CBD subjects (M ⫾ SD: manipulation actions ⫽ 62.50 ⫾ 14.3; nonmanipulation actions ⫽ 79.10 ⫾ 16.6), F(1, 47) ⫽ 8.42, p ⬍ .006; and for AD subjects (M ⫾ SD: manipulation actions ⫽ 54 ⫾ 13.8; nonmanipulation actions ⫽ 70.40 ⫾ 11.9), F(1, 47) ⫽ 8.27, p ⬍ .007. Chi-square analysis performed on NfPPA patients’ correct responses did not show a significant difference between manipulation and nonmanipulation actions, ␹2(1, N ⫽ 2) ⫽ 0.60, p ⬎ .05.

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Figure 2. A: Comprehension scores of objects and actions in FvFTD, SD, PSP, CBD, AD, and control patients. B: Comprehension scores of objects and actions in the NfPPA patients and controls. Results are expressed as the mean percentage of correct responses. FvFTD ⫽ frontal variant of frontotemporal dementia; SD ⫽ semantic dementia; PSP ⫽ progressive supranuclear palsy; CBD ⫽ corticobasal degeneration; AD ⫽ Alzheimer’s disease; C ⫽ controls; NfPPA-1 ⫽ nonfluent primary progressive aphasia (Patient 1); NfPPA-2 ⫽ nonfluent primary progressive aphasia (Patient 2). *p ⬍ .05, action versus object comprehension.

Discussion

Figure 3.

Examples of items from the picture naming task.

The present findings confirm the hypothesis that action naming is impaired in FTD as well as in PSP and CBD; moreover, they provide a number of additional insights into this clinical observation. The hypothesis that a particularly severe impairment in action naming, compared with object naming, is a differential feature of FTD in comparison with AD (Cappa et al., 1998) needs to be further qualified, as in FvFTD the dissociation is similar to that observed in AD patients. On the other hand, the discrepancy is larger in NfPPA as well as in CBD and in PSP. In contrast, we failed to observe a significant discrepancy in the case of SD. The previous report (Cappa et al., 1998) of a significantly larger dissociation in FTD than in AD can probably be explained by the contribution of the separate subgroups’ performance to the overall

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A. 100

% correct responses

90 80

*

Manip NonManip

*

70 60 50 40 30 20 10 0 FvFTD

SD

PSP

CBD

AD

B. 100 90 % correct responses

80

Manip NonManip

70 60 50 40 30 20 10 0 NfPPA-1

NfPPA-2

Figure 4. A: Effect of manipulation in FvFTD, SD, PSP, CBD, and AD patients. B: Effect of manipulation in NfPPA patients. Manip ⫽ manipulation; NonManip ⫽ nonmanipulation; FvFTD ⫽ frontal variant of frontotemporal dementia; SD ⫽ semantic dementia; PSP ⫽ progressive supranuclear palsy; CBD ⫽ corticobasal degeneration; AD ⫽ Alzheimer’s disease; NfPPA-1 ⫽ nonfluent primary progressive aphasia (Patient 1); NfPPA-2 ⫽ nonfluent primary progressive aphasia (Patient 2). *p ⬍ .05.

FTD performance. As to the relationship of the naming disorder with comprehension, only FvFTD, SD, and AD showed a mildly impaired performance, which was more severe for actions only for FvFTD and AD patients. Taken together, these results could indicate that severe action-naming disorder can be observed in patients with NfPPA, PSP, and CBD. The observation of a severe impairment in verb retrieval in the case of NfPPA is not unexpected. This variant is associated with a clinical picture that is reminiscent of Broca’s aphasia and reflects prominent pathological involvement of the anterior language areas. Hillis, Oh, and Ken (2004) reported a detailed investigation of action naming in a large sample of patients with this condition. They showed that the disorder is particularly severe in the oral modality, suggesting an impairment of modality-specific lexical representations. The results were less expected in the case of PSP and, in particular, of CBD. A verb-naming disorder in PSP had originally been reported by Daniele et al. (1994); recently, Bak et al. (2006) reported a familiar disorder resembling PSP that was characterized by a hereditary selective verb deficit. The finding of a severe verb

deficit in two conditions that are characterized clinically by a prominent movement disorder, rather than by language dysfunction, cannot but open the discussion about the relationships between action language and action representation (Hauk, Johnsrude, & Pulvermuller, 2004; Tettamanti et al., 2005). It is noteworthy that most of the cases classified clinically as progressive nonfluent aphasia in the large series recently reported by Josephs et al. (2006) were characterized by PSP and CBD pathology. The particularly severe impairment in the naming of manipulation actions in the case of CBD, but not of PSP, is an element further supporting the relationship between naming and acting. Soliveri, Piacentini, and Girotti (2005) have reported that although both CBD and PSP patients were impaired on apraxia tests, the qualitative features of errors were different, with more severe impairment of simple limb movement in CBD. It is remarkable that a similar manipulation effect was found in AD, in which limb apraxia can also be observed. Imaging studies may provide further insights about the relationships among the location of prevalent cortical involvement, the pattern of lexical impairment, and the specific feature of high-order motor dysfunction in these conditions. In the case of FvFTD, SD, and AD, the naming disorder was associated with mild word-comprehension impairment. It is worth underlining that there were no significant differences in object and action naming in SD, that is, in the subtype of FTD associated with the most severe naming impairment, thus excluding a link between defective action naming and overall severity of the naming disorder. In contrast, the discrepancy was present in the case of both FvFTD and AD and is open to different interpretations. It has been suggested that action naming may be more demanding in terms of cognitive resources and executive control. When presented with a picture, the naming of the object may be a more automatic response than the retrieval of the action name; this may be reflected in the large number of “substitution with name” errors that were present in all patient groups.

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Received January 19, 2006 Revision received May 16, 2006 Accepted May 22, 2006 䡲