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Verb production in the nonfluent and semantic variants of primary progressive aphasia: The influence of lexical and semantic factors Karine Marcotte ik

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, Naida L. Graham , Sandra E. Black hil

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Toronto Rehabilitation Institute, Toronto, Canada

b

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École d'Orthophonie et d'Audiologie, Faculty of Medicine, Université de Montréal, Montréal, QC, Canada c

Centre de Recherche de l'Hôpital du Sacré-Cœur de Montréal, Montréal, QC, Canada d

Department of Speech-Language Pathology, Faculty of Medicine, University of Toronto, Toronto, ON, Canada e

Institute of Medical Science, University of Toronto, Toronto, ON, Canada

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L.C. Campbell Cognitive Neurology Research Unit, Sunnybrook Health Sciences Centre, Toronto, ON, Canada g

Brain Sciences Research Program, Sunnybrook Research Institute, Toronto, ON, Canada h

Rotman Research Institute–Baycrest Centre, Toronto, ON, Canada

i

Department of Medicine (Neurology), University of Toronto, Toronto, ON, Canada j

Heart and Stroke Foundation, Partnership for Stroke Recovery, Ontario, ON, Canada k

Department of Medicine, Division of Neurology, University Health Network Memory Clinic, Western Hospital, Toronto, ON, Canada l

Department of Psychiatry (Geriatric Psychiatry), University of Toronto, Toronto, ON, Canada m

School of Rehabilitation Sciences, Faculty of Health Sciences, University of Ottawa, Ottawa, ON, Canada Published online: 30 Oct 2014.

To cite this article: Karine Marcotte, Naida L. Graham, Sandra E. Black, David Tang-Wai, Tiffany W. Chow, Morris Freedman, Elizabeth Rochon & Carol Leonard (2014) Verb production in the nonfluent and

semantic variants of primary progressive aphasia: The influence of lexical and semantic factors, Cognitive Neuropsychology, 31:7-8, 565-583, DOI: 10.1080/02643294.2014.970154 To link to this article: http://dx.doi.org/10.1080/02643294.2014.970154

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Cognitive Neuropsychology, 2014 Vol. 31, Nos. 7–8, 565–583, http://dx.doi.org/10.1080/02643294.2014.970154

Verb production in the nonfluent and semantic variants of primary progressive aphasia: The influence of lexical and semantic factors Karine Marcotte1,2,3, Naida L. Graham1,4, Sandra E. Black1,5,6,7,8,9,10, David Tang-Wai9,11, Tiffany W. Chow8,9,12, Morris Freedman8,9, Elizabeth Rochon1,4,10, and Carol Leonard4,10,13 1

Toronto Rehabilitation Institute, Toronto, Canada École d’Orthophonie et d’Audiologie, Faculty of Medicine, Université de Montréal, Montréal, QC, Canada 3 Centre de Recherche de l’Hôpital du Sacré-Cœur de Montréal, Montréal, QC, Canada 4 Department of Speech-Language Pathology, Faculty of Medicine, University of Toronto, Toronto, ON, Canada 5 Institute of Medical Science, University of Toronto, Toronto, ON, Canada 6 L.C. Campbell Cognitive Neurology Research Unit, Sunnybrook Health Sciences Centre, Toronto, ON, Canada 7 Brain Sciences Research Program, Sunnybrook Research Institute, Toronto, ON, Canada 8 Rotman Research Institute–Baycrest Centre, Toronto, ON, Canada 9 Department of Medicine (Neurology), University of Toronto, Toronto, ON, Canada 10 Heart and Stroke Foundation, Partnership for Stroke Recovery, Ontario, ON, Canada 11 Department of Medicine, Division of Neurology, University Health Network Memory Clinic, Western Hospital, Toronto, ON, Canada 12 Department of Psychiatry (Geriatric Psychiatry), University of Toronto, Toronto, ON, Canada 13 School of Rehabilitation Sciences, Faculty of Health Sciences, University of Ottawa, Ottawa, ON, Canada

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Differential patterns of impairment with respect to noun and verb production have been observed in the nonfluent and semantic variants of primary progressive aphasia. However, the factors influencing this discrepancy remain unclear. The present study evaluates verb retrieval in primary progressive aphasia using a naming task and a story completion task. Findings indicate that patients with the semantic variant are influenced by familiarity, frequency, and age of acquisition in both object and action naming, whereas patients with the nonfluent variant are not. Surprisingly, there were no differences in either group between object and action naming, presumably because the lists were well matched on pertinent variables. In the story completion task, greater impairment in semantically heavier than in semantically lighter verbs was observed for the semantic variant, and grammaticality and verb tense agreement was significantly lower in the nonfluent variant. The present findings suggest that lexicosemantic attributes affect verb production in the semantic variant, whereas both lexicosemantic and syntactic attributes affect verb production in the nonfluent variant.

Correspondence should be addressed to Karine Marcotte, École d’orthophonie et d’audiologie, Université de Montréal–Faculté de médecine, C.P. 6128, succursale Centre-Ville, Montréal, QC, H3C 3J7, Canada (E-mail: [email protected]). The authors would like to thank Amy Lewis, Shayna Sparling, Danna Rybko, and Ashleigh Wishen for help with testing subjects, as well as Kate Orgill and Bruna Seixas Lima for the transcriptions. Canadian Institutes of Health Research (CIHR) [grant number 82744]; Toronto Rehabilitation Institute (K.M.); Department of Medicine at the University of Toronto and Sunnybrook Health Sciences Center, the Brill Chair in Neurology, the Brain Sciences Research Program, and Sunnybrook Research Institute (S.E.B.). © 2014 Taylor & Francis

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Keywords: Verb production; Semantic dementia; Nonfluent primary progressive aphasia; Semantic weight; Lexical factors; Naming; Verb story completion task.

Primary progressive aphasia (PPA) is a result of neurodegenerative changes affecting the frontotemporal region and is characterized by a progressive language impairment, which eventually evolves to dementia (Mesulam & Weintraub, 2008). According to the most recent classification (Gorno-Tempini et al., 2011), anomia and single-word comprehension deficits are the core features of the fluent variant, also known as the semantic variant (svPPA). Errors are frequent in these two tasks due to the loss of semantic knowledge (Hodges, Martinos, Woollams, Patterson, & Adlam, 2008). In svPPA, speech remains fluent, well articulated, and grammatically correct, but becomes progressively circumlocutory and lacking in content words (Hodges et al., 1992; Snowden, Neary, & Mann, 1996). svPPA is generally associated with bilateral atrophy in the anterior temporal lobes, usually more pronounced in the left hemisphere (Galton et al., 2001). The nonfluent variant (nfPPA) is characterized by agrammatism in language production and/or effortful speech (Gorno-Tempini et al., 2011). Naming impairment is also a characteristic of nfPPA, but greater difficulty has been observed in verb naming than in object naming (Silveri & Ciccarelli, 2007). nfPPA is associated with left frontal and insular atrophy (Gorno-Tempini et al., 2004); in the early stages, the language profile resembles that of poststroke Broca’s aphasia and gradually evolves to resemble a global aphasia (Mesulam, 2001).1 The discrepancy between noun and verb production in patients with PPA has triggered some controversy. For instance, in a study by Rhee, Antiquena, and Grossman (2001), severe verb impairments (in both production and comprehension) were observed in both svPPA and nfPPA patients. Conversely, Hillis, Oh, and Ken (2004)

reported a selective verb impairment in the frontal variant of frontotemporal dementia and in nfPPA, whereas there was a greater impairment in noun naming in svPPA (Hillis et al., 2004). These conflicting results have stimulated much interest in the investigation of verb production deficits in the different variants of PPA. Assessment of verb processing is also relevant to the domain of syntactic processing, as difficulty with verbs may arise from the greater syntactic complexity of verbs than of nouns (Berndt, Haendiges, Mitchum, & Sandson, 1997; Zingeser & Berndt, 1990). However, inconsistencies arise with respect to findings on verb production abilities in nfPPA in connected speech. For example, Thompson, Lange, Schneider, and Shapiro (1997) examined connected speech in three agrammatic patients and reported increased noun-to-verb ratios, indicating difficulty with verb production. Similarly, a greater impairment on action (verb) naming than object (noun) naming was reported in a groups of patients with nfPPA (Hillis et al., 2006; Thompson, Lukic, King, Mesulam, & Weintraub, 2012). In contrast, Graham, Patterson, and Hodges (2004) first reported normal ratios of nouns to verbs, providing evidence that verb production was not reduced in connected speech in a group of 14 patients with nfPPA. Normal ratios of nouns to verbs in the speech of patients with nfPPA have subsequently been reported elsewhere (Fraser et al., 2013; Knibb, Woollams, Hodges, & Patterson, 2009; Meteyard & Patterson, 2009). Taken together, these studies provide conflicting evidence regarding grammatical class and verb production in nfPPA. Less attention has been paid to the semantic aspects (i.e., the content) of the speech of patients with nfPPA. Yet, it seems reasonable to assume

1 There is a third variant, termed logopenic PPA. The number of logopenic patients recruited for this study was too few in number (n = 5). In any event, the question of interest in this study is most relevant to nfPPA and svPPA variants.

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that their speech is reduced in semantic content, given that communication difficulties are usually a presenting complaint. Indeed, the limited data available suggest impairments at this level. For example, the picture descriptions of individuals with nfPPA have been found to contain significantly fewer units of information than those of control participants (Graham et al., 2004). Similarly, a longitudinal case study reported decline in information units with disease progression (Rogers & Alarcon, 1998). With respect to svPPA, it is generally accepted that syntactic and phonological processing are relatively spared. (Grossman, 2002; Hodges, 2001; Snowden et al., 1996). A small number of studies have assessed syntactic comprehension and demonstrated that it is generally well preserved (Breedin & Saffran, 1999; Grossman & Moore, 2005; Hodges & Patterson, 1996; Kavé, Leonard, Cupit, & Rochon, 2007; Rochon, Kave, Cupit, Jokel, & Winocur, 2004). A few studies have systematically examined verb production in svPPA. In addition to the findings that svPPA patients tend to have greater difficulty with nouns than with verbs, they tend to have disproportionate difficulty with lowfrequency words and with concrete concepts than with high-frequency regular words and abstract concepts (Breedin, Saffran, & Coslett, 1994; Cipolotti & Warrington, 1995; Kertesz, Davidson, & McCabe, 1998; Warrington, 1975). Bird, Lambon Ralph, Patterson, and Hodges (2000) reported a longitudinal study using a picture description task in three svPPA patients. They focused on the nature of the content words in the patients’ speech (rather than the syntactic aspects discussed above) and found that noun production was affected at an earlier stage of the disease, and more severely than verb production. Consistent with this study, Kavé et al. (2007) also reported an increased use of verbs and a decreased use of nouns, relative to control participants, in a case of svPPA. Similarly, Wilson et al. (2010) found that svPPA patients produced a greater proportion of verbs than did controls and patients with nfPPA. The finding seems robust, but its basis is open to interpretation. Bird et al. (2000) concluded that it was an artefact arising from increased

reliance on higher frequency words (verbs tend to be higher in frequency than nouns). Another feature of the speech of svPPA patients is the clear degradation in semantic content. This is revealed by a decline in the amount of information produced, a reduction in the variety of nouns and verbs used, and increased use of vague or general terms (Bird et al., 2000; Chapman et al., 2005; Kavé et al., 2007). The reduction in the content in speech produced by individuals with svPPA is clear from these studies, but several aspects regarding the impact of a semantic impairment upon the production of connected speech remain to be resolved, including its impact on verb retrieval. Verb retrieval impairments have been extensively studied in stroke-induced aphasia (e.g., Berndt et al., 1997; Miceli, Silveri, Villa, & Caramazza, 1984; Thompson et al., 1997; Zingeser & Berndt, 1990). Impaired verb retrieval has generally been associated with patients suffering from agrammatism, as in Broca’s aphasia. Individuals with agrammatic aphasia generally have greater difficulty retrieving verbs than nouns in confrontation naming (e.g., Miceli et al., 1984; Zingeser & Berndt, 1990). It has been proposed that grammatically more complex items are more difficult to produce than simpler ones (Bastiaanse & van Zonneveld, 2004). According to this hypothesis, greater difficulty with verbs is a matter of grammatical complexity (e.g., Kim & Thompson, 2000) and not of a greater complexity of verbs in general. Another interpretation for differential performance is that verb difficulty is not uniform across all verbs. For example, “light” verbs have sparse semantic specifications and are often core primitives in the semantic representations of more complex verbs (e.g., get, give). “Heavy” verbs, on the other hand, have more complex semantic representations and are therefore more constrained with respect to the contexts in which they occur (e.g., purchase, donate; Barde, Schwartz, & Boronat, 2006; Breedin, Saffran, & Schwartz, 1998; Gordon & Dell, 2003; Kim & Thompson, 2004). Breedin et al. (1998) studied the influence of semantic verb weight in individuals with nonfluent agrammatic aphasia following a cerebrovascular accident and used a verb story Cognitive Neuropsychology, 2014, 31 (7–8)

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completion task. They found that semantically lighter verbs (i.e., less specific verbs) were more difficult for these patients to produce than semantically heavier verbs. In sum, the evidence suggests that both syntactic and semantic attributes of verbs influence verb production in stroke-induced aphasia. A task similar to that used by Breedin et al. (1998) was used to compare the performances of individuals with agrammatic aphasia, individuals with probable Alzheimer’s disease, and healthy elderly participants (Kim & Thompson, 2004). As in the original study, patients with agrammatic aphasia (and healthy controls) were better with heavier verbs than with lighter verbs. Conversely, patients with probable Alzheimer’s disease performed better with lighter than with heavier verbs. Theories of sentence production vary in the degree to which they posit independence or interdependence of the different components of the language processing system. A contentious issue in the literature involves the degree to which syntactic processes are carried out in an autonomous (i.e., modular) fashion, separate from other nonsyntactic processes. Some models posit separate, modular stages in sentence production (e.g., Bock & Levelt, 1994), while others posit a high degree of interaction between syntactic and nonsyntactic factors (Bates & MacWhinney, 1989). Instead of autonomous levels of processing, constraint-based connectionist models (e.g., Haskell & MacDonald, 2003) propose that language production is accomplished via a distributed system in which syntax and semantics function interactively as sources of constraint on the intended utterance. Performance is expected to be influenced by linguistic distributions, and therefore frequencybased effects are expected in all aspects of language processing, including both sentence structure and single words. As described above, differential patterns of impairment with respect to noun and verb production have been observed in nfPPA and svPPA. In line with the models just outlined, two main classes of explanations for noun/verb dissociations have been given in the literature. The

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first emphasizes impairment in syntactic processing and arises out of the modular view; verbs are more grammatically complex than nouns, and difficulty with verbs is thought to arise from damage to the syntactic component of the language system (Friedmann & Grodzinsky, 1997; Miceli et al., 1984). In the second class of explanations, sometimes guided by connectionist principles, the disparity is thought to arise from inherent differences in nouns and verbs (relative to, for instance, word frequency or the semantic weight of verbs), rather than a grammatical-class specific deficit. According to Gordon and Dell’s (2003) connectionist model, a decrement in light verbs arises from syntactic impairment, since these lighter verbs tend to appear in a wider range of syntactic contexts than heavier verbs. Based on this model of lexical access in sentence production, nfPPA patients would be expected to produce more heavy than light verbs, and svPPA patients would be expected to produce more light than heavy verbs. To our knowledge, this prediction has only been examined with three nfPPA patients who were found to perform better with lighter verbs (Graham & Rochon, 2007), but this has not yet been studied in a larger group of patients, nor with svPPA patients. The present study evaluates verb retrieval in two groups of patients with PPA—one with the nonfluent variant and the other with the semantic (respectively, nfPPA and svPPA). First, verb retrieval is assessed using a naming task, which allows us to determine whether participants are influenced by word class (i.e., nouns vs. verbs), frequency, familiarity, or age of acquisition. Second, verb production in sentences is assessed using the story completion task developed by Breedin et al. (1998) and further validated by Barde et al. (2006). This story completion task manipulates semantic specificity of the target verb in a way that connected speech tasks cannot. This will allow us to determine whether participants tend to produce semantically heavier or lighter verbs, given equivalent cues. Based on Gordon and Dell’s (2003) model of lexical access in sentence production, nfPPA patients are expected to produce more heavy than light verbs. In contrast, we expect svPPA patients

VERB PRODUCTION IN PRIMARY PROGRESSIVE APHASIA

to produce more light than heavy verbs. We also include an analysis of sentence grammaticality and verb tense to further our understanding of the use of verbs in connected speech in these patient groups.

METHOD

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Participants Twenty-three individuals with the diagnosis of PPA and 15 age- and education-matched healthy controls participated in the study. Patients were recruited through four memory clinics in Toronto, and a certified and experienced neurologist diagnosed each of them. Control participants were recruited from a volunteer pool. All participants were native speakers of English, or completed some of their education in English. Exclusion criteria were (a) a known history of drug or alcohol abuse and (b) a history of other neurological and/ or major psychiatric illness. The Research Ethics Boards of all hospitals involved in recruitment, as well as the board at the University of Toronto, approved the study. Written consent was obtained from all participants. Patients with PPA Patients were diagnosed with PPA and were classified as one of three variants—nonfluent progressive aphasia (nfPPA), semantic variant (svPPA), and logopenic—according to the recently proposed consensus classification (Gorno-Tempini et al., 2011) based on a series of evaluations by a multidisciplinary team. Only patients with a classification of nfPPA or svPPA were included in this study as participants of the logopenic variant were too few in number (n = 5). In addition, data from one participant with nfPPA and one participant with svPPA were excluded as their performances were, respectively, 2 standard deviations above and 2 standard deviations below the mean on the verb story completion task. Table 1 presents demographic information and mean neuropsychological and language evaluation scores for both patient groups as well as for the control group.

Materials Stimuli Naming. The battery developed by Druks and Masterson (2000), An Object and Action Naming Battery, was used to investigate the impact of frequency, familiarity, and age of acquisition on object and verb naming. The battery consists of pictures of 162 nouns and 100 verbs that are comparable with respect to imageability and visual complexity (Druks & Masterson, 2000). Because the battery consists of so many items, for the purpose of our investigation, the entire battery was administered over the course of two sessions. The pictures were divided into two sets of items (each set consisting of 81 nouns and 50 verbs), which were matched on frequency, familiarity, and age of acquisition. The nouns and verbs in each set were then randomized separately to determine a presentation order (counterbalancing variables in each quarter of the test). Each set of items to be named was administered on different days. While each item is administered only once, for the purpose of analyses, the battery provides three predetermined subsets in which nouns and verbs are matched on frequency, familiarity, and age of acquisition. This allows for the independent investigation of the influence of these factors on object versus action naming. Each of these matched subsets is composed of 100 nouns and 100 verbs. Story completion. The story completion task used was developed by Breedin et al. (1998) and further validated by Barde et al. (2006). The task consists of short stories about which the participant is required to answer a question—for example: “The bus stopped and let people on. Mary went/walked to the back. There were plenty of seats there. What did Mary do when she got on the bus?” The task is composed of two versions of 41 stories, which contrast light versus heavy verbs (e.g., come vs. drive), general versus specific verbs (e. g., eat vs. dine), or patient versus patient + state (e.g., drop vs. break) verbs. Briefly, the patient condition consists of verbs for which the direct object assumes the thematic role of patient whereas the patient + state condition includes verbs in which Cognitive Neuropsychology, 2014, 31 (7–8)

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Table 1. Demographic and neuropsychological data for each participant group

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Variable Demographic information Age Years of education Sex Handedness General cognitive function Mini-Mental State Examination (/30) Montreal Cognitive Assessment (/30) Dementia Rating Scale (/144) Language production Boston Naming Test (/60) Semantic fluency–Animals Orthographic fluency–FAS Language comprehension Test for Reception of Grammar Peabody Picture Vocabulary Test Pyramid and Palm Tree Test: Pictures (/52) Pyramid and Palm Tree Test: Words (/52) Visuospatial Copy of Rey Complex Figure (/36) Visual Object and Space Perception Cube analysis subtest (/10) Visual Object and Space Perception Dot Counting analysis subtest (/10) Visual Object and Space Perception Object Decision subtest (/20) Verbal short-term memory Digit Span: Forward Digit Span: Backward Nonverbal short-term memory Pointing Span: Forward Pointing Span: Backward Nonverbal memory Recall of Rey Complex Figure (/36) Nonverbal reasoning Raven’s Coloured Progressive Matrices Executive functioning Wisconsin Card Sorting Test

Controls (n = 15)

nfPPA (n = 12)

69.7 (8.7) 16.6 (4.4) 6F 15 R

68.7 (11.7) 14.5 (3.8) 6F 11 R

65.6 (7.0) 17.7 (5.7) 5F 10 R

ns ns

29.1 (.9) 26.5 (2.2) 141.9 (2.1)

21.9 (3.9)a 15.3 (7.1)a 114.2 (17.8)a

23.2 (6.2)a 16.9 (6.3)a 114.0 (17.2)a

*** *** ***

37.1 (12.4)a 9.8 (7.1)a 18.1 (10.1)a

13.5 (9.6)a,b 7.2 (4.3)a 19.7 (11.9)a

*** *** ***

78.7 (1.8) 195.2 (4.7) 50.8 (.9) 50.9 (1.2)

59.2 (10.2)a,c 169.2 (18.5)a 46.8 (2.8)a 47.8 (3.3)

70.7 (12.0) 109.8 (42.4)a,b 44.0 (6.1)a 40.9 (5.6)a,b

*** *** *** ***

33.4 (1.5) 8.3 (2.1) 9.9 (0.3)

25.7 (7.0)a,c 8.7 (1.9) 9.6 (0.5)a

32.9 (3.0) 9.4 (1.8) 9.9 (0.3)

*** ns *

17.5 (1.5)

15.8 (2.7)

15.5 (2.0)

*

54.4 (4.7) 20.4 (4.4) 47.1 (12.5)

svPPA (n = 11)

Group effect

7.2 (0.7) 5.0 (1.2)

5.1 (1.2)a,c 3.3 (0.9)a

6.3 (1.1) 3.6 (0.9)a

*** ***

5.0 (1.3) 4.9 (1.2)

4.7 (1.1) 4.2 (1.5)

5.4 (0.8)a 4.9 (0.7)

ns ns

17.6 (6.5)

10.9 (6.7)

11.0 (8.3)

*

31.5 (4.2)

24.3 (7.1)a,c

31.4 (4.8)

***

4.0 (0.8)

1.3 (1.3)a,c

3.1 (1.6)

***

Note: Values shown are means, with standard deviations in parentheses. PPA = primary progressive aphasia; nfPPA = nonfluent variant of PPA; svPPA = semantic variant of PPA; F = female; R = right. a Significantly impaired relative to normal controls. bSignificantly impaired relative to nfPPAs. cSignificantly impaired relative to svPPAs. *p , .05. ***p ≤ .001.

the direct object undergoes a change of state as the result of the action. Procedure Naming. An Object and Action Naming Battery (Druks & Masterson, 2000) was administered

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over the course of two test sessions. Participants were asked to name each picture, and no feedback other than general encouragement was provided. As described in the test manual, for the action pictures the experimenter frequently repeated the questions “What is he/she doing?” and “What is

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happening here” to ensure that participants named the verb, rather than an object in the picture. Responses were audio-recorded and transcribed verbatim. Latencies were not measured. Responses were scored as correct if the expected object or verb was produced. Accurate (or erroneous) self-corrections were scored as correct (or incorrect) as long as the correction was produced before moving on to the next test item. Phonemic paraphasias were scored as incorrect. Story completion. The two versions of the story completion task were administered during separate test sessions, with at least 24 hours between each session. Participants listened to a story presented live by the examiner and then answered a question about it. They were instructed to respond in complete sentences and to use words from the story. Five practice trials were given prior to the first test trial. During the practice trials, feedback was provided when the participant did not answer with a complete sentence or when the words used were not from the story. During the test trials, no feedback was provided other than general encouragement. Responses were audio-recorded and transcribed verbatim for scoring. As in the original studies (Barde et al., 2006; Breedin et al., 1998), responses were first scored as correct on the basis of the verb only. Error responses were classified according to the type of verb produced. Following Breedin et al. (1998), errors were classified as (a) “lighter” (i.e., semantically less specific or complex than the target); (b) “heavier” (i.e., semantically richer or more complex than the target); (c) “equivalent” with respect to semantic specificity; and (d) incorrect (i.e., “unrelated”, no verb, or no response). We also added a fifth category, “paraphasia” (i.e., the response incorporated a semantic, verbal, or phonemic paraphasia). In addition to scoring the error responses on the basis of the type of verb produced, we also noted the verb tense used by the participants to determine the proportion of errors that retained the target verb tense. Similarly, we rated the grammaticality of the responses to determine the proportion of sentences that were grammatical.

Reliability for the story completion task All of the responses were independently scored by one of the authors (K.M.). In addition, an independent rater who was blind to the purpose of the study scored 21.5% of the responses. Agreement between the scores of the two raters, including scoring of both accurate responses and error types, was 95.3%. Interrater agreement for the scoring of verb tense was 99.2%. Regarding the scoring of the grammaticality of the sentences, interrater agreement was 78.8%. The main source of disagreement consisted of sentences that did not have a subject (e.g., Bought an oak chest.). It was decided that a sentence would be considered grammatically correct when it included at least a subject and a verb. With this more specific definition of grammaticality, interrater agreement was 97.4%. Data analysis All statistical analyses were done using SPSS® v19.0, and the significance level was set at p , .05. Post hoc comparisons were made using the Bonferroni correction.

RESULTS Naming Action naming In order to examine the influence of frequency, familiarity, and age of acquisition on action naming by the different groups, separate two-way analyses of variance (ANOVAs), 3 (groups) × 3 (levels of variable analysed), were conducted on mean percentage naming accuracy on the subsets of items that were matched on the variable being analysed (as described earlier under Stimuli). Regarding frequency, the analysis indicated significant main effects of group, F(2, 105) = 36.616, p , .001, and frequency, F(2, 105) = 6.357, p , .005. The interaction between group and frequency was also found to be significant, F(4, 105) = 3.092, p , .05. Post hoc testing revealed that for verbs of both low and medium frequency, both the nfPPA and the svPPA groups made significantly more errors than the control group but Cognitive Neuropsychology, 2014, 31 (7–8)

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did not differ from each other (mean accuracy for low, nfPPA 70%, p , .005; svPPA 45%, p , .001, controls 98%; mean accuracy for medium, nfPPA 74%, p = .001; svPPA 62%, p , .001, controls 98%). For the high-frequency verbs, the nfPPA group also made significantly more errors (p , .05) than the controls (mean accuracy: 81% vs. 97%). With respect to familiarity, significant main effects were found for group, F(2, 105) = 42.147, p , .001, and familiarity, F(2, 105) = 4.768, p , .05. However, there was no interaction between group and verb familiarity, F(4, 105) = 2.393, p = .055. Regarding age of acquisition, significant main effects of group, F(2, 105) = 37.9808, p , .001, and age of acquisition, F(2, 105) = 8.056, p , .001, were found, and there was a significant interaction, F(4, 105) = 3.191, p , .05. Post hoc testing revealed significant differences between all three groups for verbs acquired late, with the svPPA group (mean accuracy 44%) producing more errors than both the control group (mean accuracy 97%, p , .001) and the nfPPA group (mean accuracy 68%, p , .05). The nfPPA group

also differed significantly from the control group (p , .001). For verbs acquired early, both the svPPA (mean accuracy 62%) and the nfPPA (mean accuracy 74%) groups made significantly more errors (p , .001, p , .005, respectively) than the control group (mean accuracy 97%), but did not differ significantly from each other. For verbs acquired very early, the three groups did not differ from each other. To investigate the within-group differences for the different levels of each variable, one-way ANOVAs were conducted for each group separately to compare the performance within group on the three levels of each variable. Mean correct raw scores and mean percentage correct for all three levels of each three linguistic variables studied (i.e., frequency, familiarity, and age of acquisition) and one-way ANOVA values are reported in Table 2 for each group. For both the control and nfPPA groups, none of the variables of frequency, familiarity, or age of acquisition significantly influenced action naming. Conversely, the svPPA group showed a significant effect for all three factors [frequency, F(2, 20) = 7.156, p , .005; familiarity, F(2, 20) = 6.154, p , .01;

Table 2. Mean correct raw score and percentage correct of each group for action naming on the Object and Action Naming Battery Controls Variable Frequency High-frequency actions Medium-frequency actions Low-frequency actions p-value from within-group ANOVA Familiarity Very familiar actions More familiar actions Less familiar actions p-value from within-group ANOVA Age of acquisition Very early acquisition actions Early acquisition actions Late acquisition actions p-value from within-group ANOVA

nfPPA

svPPA

n

Raw score

% correct

Raw score

% correct

Raw score

% correct

24 48 28

23.2 (1.0) 46.9 (1.0) 27.3 (1.4) .763

97 98 98

19.4 (5.1) 35.5 (11.9) 19.5 (7.5) .419

81 74 70

19.5 (4.5) 29.6 (9.5) 12.6 (7.6) .003

81 62 45

26 46 28

25.5 (1.1) 45.9 (3.9) 27.4 (0.9) .677

98 100 98

20.9 (6.2) 33.5 (11.3) 19.9 (10.3) .552

80 73 71

19.5 (10.3) 29.9 (10.3) 12.3 (6.8) .006

74 65 44

25 47 28

24.4 (0.9) 45.8 (1.4) 27.1 (1.1) .791

98 97 97

20.6 (6.2) 34.9 (10.3) 19.0 (7.6) .663

82 74 68

20.4 (4.3) 29.0 (10.6) 12.3 (6.5) .001

81 62 44

Note: Means; standard deviations in parentheses. PPA = primary progressive aphasia; nfPPA = nonfluent variant of PPA; svPPA = semantic variant of PPA; ANOVA = analysis of variance. Object and Action Naming Battery: Druks and Masterson (2000).

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and age of acquisition, F(2, 20) = 8.638, p , .001]. For frequency, post hoc tests revealed that participants with svPPA made significantly more errors (p , .005) on verbs of low frequency (mean accuracy 45%) than on those of high frequency (mean accuracy 81%). With respect to familiarity, the svPPA group made significantly more errors (p , .005) on verbs that were less familiar (mean accuracy 44%) than on those that were very familiar (mean accuracy 74%). Finally, for age of acquisition, the svPPA group made significantly more errors (p , .001) on verbs that were acquired late (mean accuracy 44%) than on those that were acquired very early (mean accuracy 81%). Object naming As with action naming, in order to examine the influence of frequency, familiarity, and age of acquisition on object naming by the different groups, separate two-way ANOVAs, 3 (groups) × 3 (levels of variable analysed), were conducted. Regarding frequency, the analysis indicated significant main effects of group, F(2, 105) = 52.394, p , .001, and frequency, F(2, 105) = 10.809, p , .001. The interaction between group and object frequency was also significant, F(4, 105) = 5.308, p , .001. Post hoc testing revealed that for nouns of low and medium frequency, both the nfPPA and svPPA groups made significantly more errors than the control group but did not differ from each other (mean accuracies: low frequency, nfPPA 75%, p = .035; svPPA 38%, p , .001, controls 98%; medium frequency, nfPPA 77%, p , .005; svPPA 59%, p , .001, controls 98%). With high-frequency objects, both the nfPPA and svPPA again made significantly more errors than controls (nfPPA 85%, p , .05; svPPA 81%, p , .005, controls 99%), but svPPA patients also made more errors than nfPPA patients (p , .001). For the variable familiarity, the analysis also indicated significant main effects of group, F(2, 105) = 54.454, p , .001, and familiarity, F(2, 105) = 7.734, p , .001, as well as a significant interaction, F(4, 105) = 2.847, p , .05. Post hoc testing revealed that for nouns that were less familiar and for nouns that were more familiar, both

the nfPPA and svPPA groups made significantly more errors than the control group (mean accuracies: less familiar: nfPPA 76%, p , .05; svPPA 40%, p , .001; controls 97%; more familiar: nfPPA 78%, p , .05; svPPA 53%, p , .001; controls 99%). The svPPA group also made significantly more errors than the nfPPA group on nouns that were less familiar (p = .001) and more familiar (p , .01) and significantly more errors (mean accuracy 75%; p , .001) than the control group on nouns that were very familiar (mean accuracy 99%). For age of acquisition, the analysis indicated significant main effects of group, F(2, 105) = 66.789, p , .001, and age of acquisition, F(2, 105) = 13.418, p , .001, and a significant interaction, F(4, 105) = 4.657, p , .005. Post hoc testing revealed that for nouns that were acquired late, both the nfPPA and svPPA groups made significantly more errors than the control group (mean accuracies: nfPPA 69%, p , .001; svPPA 35%, p , .00; controls 96%), and the svPPA group made significantly more errors than the nfPPA group (p , .001). For nouns acquired early, the svPPA group (mean accuracy 46%) also made significantly more errors than both the controls (mean accuracy 97%; p , .001) and the nfPPA group (mean accuracy 79%; p , .001). For nouns that were acquired very early, the svPPA group (mean accuracy 75%) also made significantly more errors (p , .001) than the control group (mean accuracy 97%). To investigate the within-group differences for the different levels of each variable, one-way ANOVAs were conducted for each group separately to compare performance on the three levels of each variable. Mean correct raw scores and mean percentage correct for all three levels of each variable (i.e., frequency, familiarity, and age of acquisition) and one-way ANOVA values are reported in Table 3 for each group. For the control group, the only variable that was significant was familiarity, F(2, 42) = 3.55, p = .049: Although performance was essentially at ceiling for all levels, very familiar objects (mean accuracy 99%) were named significantly more accurately (p , .05) than less familiar objects (mean accuracy Cognitive Neuropsychology, 2014, 31 (7–8)

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Table 3. Mean correct raw score and percentage correct of each group for object naming on the Object and Action Naming Battery Controls

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Variable Frequency High-frequency objects Medium-frequency objects Low-frequency objects p-value from within-group ANOVA Familiarity Very familiar objects More familiar objects Less familiar objects p-value from within-group ANOVA Age of acquisition Very early acquisition objects Early acquisition objects Late acquisition objects p-value from within-group ANOVA

nfPPA

svPPA

n

Raw score

% correct

Raw score

% correct

Raw score

% correct

24 48 28

23.8 (0.4) 47.1 (1.5) 27.5 (0.9) .527

99 98 98

20.4 (5.1) 37.0 (11.0) 21.1 (7.0) .241

85 77 75

19.4 (2.8) 28.5 (10.1) 10.6 (7.4) .000

81 59 38

26 46 28

25.9 (0.4) 45.3 (0.6) 27.3 (1.0) .049

99 99 97

22.5 (5.0) 36.1 (11.7) 21.2 (8.2) .270

87 78 76

19.5 (4.5) 24.5 (10.7) 11.2 (6.8) .003

75 53 40

25 47 28

24.5 (0.5) 45.3 (1.0) 27.1 (1.2) .409

97 97 96

21.6 (4.7) 37.1 (11.9) 19.3 (6.1) .228

87 79 69

18.8 (3.5) 21.6 (11.7) 9.8 (7.3) .001

75 46 35

Note: Means; standard deviations in parentheses. PPA = primary progressive aphasia; nfPPA = nonfluent variant of PPA; svPPA = semantic variant of PPA; ANOVA = analysis of variance. Object and Action Naming Battery: Druks and Masterson (2000).

97%). Because performance was at ceiling, and the standard deviations were low, it is not possible to assess any potential role of familiarity in the controls’ naming of objects on the basis of this significant result. For the nfPPA group, none of the variables of frequency, familiarity, or age of acquisition was shown to influence object naming. As observed with action naming, the svPPA group showed a significant effect for all three variables [i.e., frequency, F(2, 30) = 11.768, p , .001; familiarity, F(2, 30) = 7.211, p , .005; and age of acquisition, F(2, 30) = 9.494, p , .001]. For frequency, post hoc tests showed that objects of high frequency (mean accuracy 81%) were produced significantly more accurately (p , .001) than objects of low frequency (mean accuracy 38%). For familiarity, nouns that were very familiar (mean accuracy 75%) were produced significantly more accurately (p , .005) than those that were less familiar (mean accuracy 40%). Finally, for the variable age of acquisition, objects acquired very early (mean accuracy 75%) and early (46%) were produced significantly more accurately (p , .001, p , .05,

respectively) than those acquired late (mean accuracy 35%). Action versus object naming In order to examine possible differences between object and verb naming per group on each of the variables of frequency, familiarity, and age of acquisition, separate two-way ANOVAs were conducted. None of the groups showed a significant difference between object and verb naming as a function of any of the variables.

Story completion task Correct responses Table 4 shows the mean raw scores and mean percentage correct by group for the different verb types (i.e., light, heavy, general, specific).2 As can be seen, healthy elderly participants correctly produced the target verbs in each verb category nearly 95% of the time. Participants with svPPA correctly produced the target verbs 68–86% of the time, and participants with nfPPA correctly produced the target verb less

2 In Barde et al. (2006), the patient versus patient + state contrast provided less consistent results. As such, this contrast was excluded from our analyses, resulting in the analysis of responses to 33 of the 41 stories.

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Table 4. Mean correct raw score and percentage correct of each group for the story completion task

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Controls

nfPPA

svPPA

Verb type

n

Raw score

% correct

Raw score

% correct

Raw score

% correct

Light verbs Heavy verbs t test (p value) General verbs Specific verbs t test (p value) Light + general verbs Heavy + specific verbs t test (p value)

19 19

18.1 (1.3) 18.3 (0.8) .609 13.4 (0.9) 13.1 (1.0) .218 31.4 (1.7) 31.4 (1.7) .888

95 96

9.8 (5.1) 8.9 (6.4) .456 6.7 (4.4) 5.8 (4.3) .136 14.7 (10.5) 16.4 (9.0) 0.193

52 47

16.3 (2.5) 14.4 (4.8) .146 11.7 (2.6) 9.5 (4.1) .013* 28.0 (4.5) 23.9 (8.7) .031*

86 76

14 14 33 33

96 94 95 95

48 41 45 50

84 68 85 72

Note: Means; standard deviations in parentheses. PPA = primary progressive aphasia; nfPPA = nonfluent variant of PPA; svPPA = semantic variant of PPA. * p , .05.

than 50% of the time. Paired t-tests were conducted separately for each group to compare verb contrasts of interest. The difference in correct production of light versus heavy verbs was not significant for any of the groups. For the general versus specific verb contrast, the svPPA group produced general verbs significantly more accurately than specific verbs, t(11) = 3.4, p , .005. Considering that confidence ratings were comparable using both specificity (general vs. specific) and semantic weight (light vs. heavy), Barde et al. (2006) collapsed the two conditions together. Thus, when combining light + general verbs and contrasting them with heavy + specific verbs, the svPPA produced light + general verbs significantly more accurately than heavy + specific verbs, t(11) = 2.6, p , .05. Between-group differences for each verb type were examined using one-way ANOVAs, and all were found to be significant. For heavy verbs, the post hoc analysis showed that the nfPPA group (mean accuracy 47%) made significantly more errors than both the svPPA group (mean accuracy 76%, p , .05) and the control group (mean accuracy 96%, p , .001). The difference between performance by the svPPA group and the control group was not significant. For light verbs, the post hoc analysis showed that the nfPPA group (mean accuracy 52%) made significantly more errors than both the svPPA group (mean accuracy 86%, p , .001) and the control group (mean accuracy 95%,

p , .001). For the specific verbs, the post hoc analysis showed that the nfPPA group (mean accuracy 41%) made significantly more errors than both the svPPA group (mean accuracy 68%, p , .05) and the control group (mean accuracy 94%; p , .001). The difference between performance by the svPPA group and the control group was also significant (p , .01). For the general verbs, the post hoc analysis showed that the nfPPA group (mean accuracy 48%) made significantly more errors than both the svPPA group (mean accuracy 84%; p , .001) and the control group (mean accuracy 96%; p , .001). When combining heavy + specific verbs, the post hoc analysis showed that the nfPPA group (mean accuracy 50%) made significantly more errors than both the svPPA group (mean accuracy 72%, p , .05) and the control group (mean accuracy 95%, p , .001). The difference between performance by the svPPA group and the control group was not significant. When combining the light + general verbs, the post hoc analysis showed that the nfPPA group (mean accuracy 45%) made significantly more errors than both the svPPA group (mean accuracy 85%, p , .001) and the control group (mean accuracy 95%, p , .001). Error analysis The type of errors produced when the participants failed to recall the target verbs were also analysed. Cognitive Neuropsychology, 2014, 31 (7–8)

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Figure 1. Mean percentage correct scores of each group for each error type in the verb story completion task. PPA = primary progressive aphasia; nfPPA = nonfluent variant of PPA; svPPA = semantic variant of PPA.

Error scores are expressed as a percentage of the total number of errors for each participant. Mean percentages of errors are represented in Figure 1 for each group. Considering the differences in error distribution that have been found between heavy and light verbs (Graham & Rochon, 2007), errors were analysed separately for heavy + specific and light + general verbs. Two multivariate ANOVAs (MANOVAs), 3 (groups) × 5 (categories of errors), were performed with group as the independent variable and the proportion of each error category as the dependent variable. For heavy + specific verbs, a significant group effect was found, F(10, 62) = 4.407, p , .001, for the error categories of “lighter” (p , .001), “heavier” (p , .05), and “paraphasia” (p , .05). For “lighter” errors, post hoc tests revealed that the proportion of errors made by the nfPPA group (mean = 46%) that were classified as

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“lighter” was significantly greater (p , .001) than that of the control group (mean = 11%) For “heavier” errors, the post hoc tests also indicated a significant difference (p , .001) between the nfPPA and control groups with the nfPPA group producing a greater proportion of “heavier” errors (mean = 2%) than the control group (mean = 0%). For errors classified as “paraphasia” errors, post hoc tests showed a significant difference (p , .01) between the control group and the svPPA group with the svPPA group producing a greater proportion of paraphasic errors (mean = 27%) than the control group (mean = 0%). For light + general verbs, the group effect was also significant, F(10, 62) = 3.00, p , .001, for the error categories of “lighter” (p , .01) only. For “lighter” errors, post hoc tests revealed that the proportion of errors made by the nfPPA group (mean = 42%) that were classified as

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Table 5. Mean correct raw score and percentage correct for grammaticality and verb tense analysis in the story completion task Controls

nfPPA

svPPA Group effect

Variable

Raw score

% correct

Raw score

% correct

Raw score

% correct

Grammaticality (/66) Verb tense (/66)

60.7 (9.9) 64.9 (1.3)

92 98

23.8 (21.7)a 53.2 (9.3)a,b

36 81

37.8 (21.7) 60.9 (3.8)

57 92

*** ***

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Note: Means; standard deviations in parentheses. PPA = primary progressive aphasia; nfPPA = nonfluent variant of PPA; svPPA = semantic variant of PPA. a Significantly different from normal controls (p ≤ .001). bSignificantly different from svPPAs (p ≤ .001). ***p ≤ .001.

“lighter” was significantly greater (p , .01) than that of the control group (mean = 11%).

Grammaticality A one-way between-group ANOVA was conducted on the percentage of responses deemed to be grammatical3 and was found to be significant, F(2, 34) = 9.795, p , .001. The post hoc analysis showed that the proportion of grammatically correct responses produced by the nfPPA group (mean = 36%) was significantly lower than that of the control group (mean = 92%, p , .001). No other differences were significant. Mean proportions and one-way ANOVA values are reported in Table 5 for each group.

Verb tense A one-way between-group ANOVA was performed on the percentage of responses that retained the same verb tense as the target. It was found to be significant, F(2, 34) = 13.744, p , .001. The post hoc analysis showed that the percentage of responses made by the nfPPA group that retained the same tense as the target (mean = 81%) was significantly lower than that of both the svPPA group (mean = 92%, p , .01) and the control group (mean = 98%, p , .001), which did not significantly differ from each other. Mean correct raw scores and percentage correct are also reported in Table 5 for each group.

DISCUSSION This study was designed to assess verb retrieval in nfPPA and svPPA, using a naming task and a verb story completion task. Findings indicate that naming in individuals with svPPA is influenced by familiarity, frequency, and age of acquisition for both objects and actions, whereas naming in individuals with nfPPA is not influenced by these variables. Surprisingly, neither patient group showed differences between object and action naming when subsets of the naming stimuli were well matched on relevant variables. Moreover, results of this study provide evidence that verb production is affected by semantic complexity for the svPPA group. As predicted, svPPA patients showed greater impairment in production of semantically heavier than of semantically lighter verbs. Unexpectedly, nfPPA patients did not show greater impairment with lighter verbs. This contrasts with findings obtained by Barde et al. (2006) in stroke patients and with results from lesions to the syntactic nodes in Gordon and Dell’s model (Gordon & Dell, 2003) but confirms the results obtained in three patients suffering from nfPPA (Graham & Rochon, 2007). Lexical variables were found to influence both action and object naming in svPPA. Consistent with previous studies that showed a significant frequency effect in svPPA (Hodges, Graham, & Patterson, 1995; Lambon Ralph, Graham, Ellis, & Hodges, 1998; Parkin, 1993; Woollams,

3 For this analysis, data from one control participant were excluded, as the percentage of grammatically correct sentences that he produced was 2 standard deviations below the control group mean.

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Cooper-Pye, Hodges, & Patterson, 2008), object naming by svPPA patients in the present study was affected by frequency. While word frequency is a lexical variable (Jescheniak & Levelt, 1994), it reflects processing at all levels, including semantics. Although word frequency is an important predictor of object naming, age of acquisition has also proven to be an important predictor, an even larger one than frequency in connectionist model simulations (Ellis & Lambon Ralph, 2000). As expected, familiarity and age of acquisition also influenced object naming in svPPA in our study, similar to the findings of Lambon Ralph et al. (1998) and Woollams et al. (2008). According to the regression hypothesis (Jakobson, 1968), vocabulary loss would be inversely related to vocabulary acquisition. This hypothesis has already been explored in PPA; however, even if certain effects of age of acquisition have been observed, previous evidence has not provided clear evidence in support of this hypothesis (Ukita, Abe, & Yamada, 1999). To the best of our knowledge, this is the first study to examine the influence of frequency, familiarity, or age of acquisition on naming of actions in svPPA. Naming accuracy was affected by all of these factors, with better performance on items that were higher in frequency or familiarity, or had an early age of acquisition. This mirrors the pattern of results observed with naming of objects by the participants with svPPA. The nfPPA patients were impaired on naming of both objects and actions, but their scores were not significantly impacted by different levels of frequency, familiarity, or age of acquisition, in contrast to the svPPA patients. As far as we are aware, this is the first time the effect of these factors has been assessed in the naming of nfPPA patients. Unlike previous evidence showing greater difficulty in object naming for svPPA patients and verb naming for nfPPA patients (Cotelli et al., 2006; Hillis et al., 2006; Hillis et al., 2004; Silveri & Ciccarelli, 2007), both word classes were similarly impaired in this study. Neither group was differentially impaired in object versus verb naming. Although svPPA has been associated with a more pronounced noun impairment, the impact of

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frequency in the noun/verb difference was demonstrated by Bird et al. (2000) in their longitudinal study. The authors suggested that the noun deficit observed in the early stage of the disease could be attributed to the lower frequency of nouns (as compared to verbs). A proportionate naming deficit between objects and verbs in nfPPA is consistent with previous functional neuroimaging studies (e.g., Berlingeri et al., 2008; Soros, Cornelissen, Laine, & Salmelin, 2003; Thompson et al., 2007; Tyler, Russell, Fadili, & Moss, 2001) and lesional neuropsychological studies (e.g., Aggujaro, Crepaldi, Pistarini, Taricco, & Luzzatti, 2006; De Renzi & di Pellegrino, 1995; Tranel, Adolphs, Damasio, & Damasio, 2001). However, the findings from this study could also suggest that an apparent selective deficit for nouns in svPPA and verbs in nfPPA may be an artefact of inherent differences between nouns and verbs. When we used large sets of well-matched nouns and verbs, we documented equivalent levels of impairment in both word classes in svPPA and nfPPA. Given that the predominant areas of brain atrophy in svPPA and nfPPA are in the anterior temporal and left inferior frontal regions, respectively, our results suggest that these areas do not play a critical and selective role in the processing of nouns and verbs. This is consistent with the findings reported by Crepaldi et al. (2013) who performed a meta-analysis of the literature on functional neuroimaging of noun and verb processing and concluded that the brain areas involved are not spatially segregated (and involve a wide network of regions, including frontal, temporal, and parietal areas). Similar to svPPA, a verb advantage has been reported in AD. The research showed that both AD patients and healthy controls were slower and made more errors in action naming than object naming. Druks et al. (2006) proposed that the verb advantage observed in AD could be due to inadequate linguistic matching. Another possible explanation for this differential result may arise as the result of a potential confound related to semantic property differences between objects and verbs that were not well controlled for in previous studies (e.g., refers to motion vs. sensation). This

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possibility is supported in a neuroimaging study by Siri et al. (2008), which showed that nouns and verbs were processed by a shared neural system when semantic factors were well controlled—that is, the same picture was used to name either a noun or a verb. Moreover, a difference in activation in the left inferior frontal gyrus when processing verbs and nouns emerged as a function of processing morphological demands. In particular, the weakest activation was found for infinitive verbs whereas the strongest was found for action nouns. Thus, the processing of nouns and verbs appears to be closely interrelated (Siri et al., 2008). Given that our set of nouns and verbs was well matched, perhaps it is not entirely surprising that differential performance between the patient groups did not emerge. With regard to the verb story completion task, the results yielded a significant difference between lighter and heavier verbs in the svPPA patients, which was driven by the difference between general and specific verbs. Specifically, svPPA patients performed better on the combination of general and light verbs than on the combination of specific and heavy verbs. This was also found in the Alzheimer’s disease patients studied by Kim and Thompson (2004), and the svPPA patients studied by Méligne et al. (2011). According to Gordon and Dell’s model (2003), heavy verbs are more affected when semantic connections are lesioned. Accordingly, svPPA patients were better at producing general, light verbs than more specific, heavy verbs. For the nfPPA patients, accuracy on light and general verbs was equivalent to that on heavy and specific verbs. Thus, the nfPPA patients did not show the decrement in light verbs, which was observed on the same task in agrammatic patients with stable lesions (Barde et al., 2006; Breedin et al., 1998). This disparity in performance may have arisen due to differences in the nature of the nonfluent aphasia arising from vascular versus neurodegenerative pathology (see Patterson, Graham, & Lambon Ralph, 2006; but for an alternative view see Thompson & Mack, 2014). The cerebrovascular accident (CVA) patients studied by Breedin et al. (1998) were nonfluent and were

selected because they had particular difficulty with production of verbs in spontaneous speech. In contrast, although the nonfluent patients studied here exhibited impaired verb naming, they did not show a selective deficit in naming verbs, nor did they show a particular difficulty with production of verbs in spontaneous speech. Most of these patients were included in an earlier study in which we documented normal proportions of nouns and verbs in connected speech in nfPPA (Fraser et al., 2013), a finding that is not expected in the frank agrammatism often observed in nonfluent aphasia following stroke. Interestingly, Barde et al. (2006) contrasted the performance of agrammatic CVA patients with that of a group of nonagrammatic CVA patients who were closely matched to the agrammatic group on pertinent measures, including the degree of impairment in naming verbs. The nonagrammatic CVA patients showed similar performance on the light versus heavy verbs, which is the same pattern as that observed here in the nfPPA patients. Documentation of this pattern of performance in the nfPPA patients adds to the small literature demonstrating differences in the language impairment in patients with nfPPA versus those with agrammatic aphasia arising from vascular pathology. Although we have just suggested that the nfPPA patients do not have a selective verb deficit, they did perform significantly more poorly on the verb story completion task than the svPPA patients (in all conditions), despite better performance than the svPPA patients in naming of verbs. This result may have arisen because the nfPPA patients have particular difficulty with production of verbs in sentences, suggesting a syntactic impairment. Although these patients produced normal proportions of nouns and verbs in connected speech (Fraser et al., 2013), in production of connected speech they were able to choose which verbs to use. In contrast, the task used here may be more difficult because only the target verb was considered acceptable. The relatively poorer performance (in comparison with the svPPA patients) on the verb story completion task could also have arisen from difficulty with other aspects of the task. In particular, although each story is brief, accurate responses Cognitive Neuropsychology, 2014, 31 (7–8)

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rely upon the ability to retain the exact wording of the stimulus in working memory. The nfPPA (but not svPPA) patients exhibited an impairment in working memory (as measured by forward digit span, see Table 1), and this may have compromised their performance on the verb story completion task. In addition, the nature of their aphasia means that they tend to speak more slowly than the svPPA patients or controls, and this would add to the burden on working memory. Further work in which the demands on working memory are systematically evaluated and in which the same verbs are used for naming and sentence production tasks could shed light on the interpretation of our findings. The use of two different tasks helps to clarify verb retrieval impairments in the two variants of PPA studied here. The naming task examined lexical factors, whereas the verb story completion task examined the semantic weight of the verb. Further, the two tasks allowed for a comparison of word retrieval at the single word and sentence level. Overall for the verb story completion task, svPPA patients performed better than nfPPA patients. Others (Gordon & Dell, 2003) have found that production of verbs in connected speech can be relatively more impaired than single word verb naming. Although we did not directly compare performance in the two tasks in this study, it appears that the verb production deficits for nfPPA patients were similar in both tasks, whereas the svPPA patients were more impaired in single word naming of verbs than in the verb story completion task. This difference is compatible with the suggestion by Bastiaanse & van Zonneveld (1998), that a more pronounced deficit in verb naming is located at the conceptual–semantic or lexical level. Along with neurological, neuroimaging and neuropsychological examination, diagnosis of PPA typically requires multiple language measures, and it is thus important to extract as much information as possible from each test. Among these measures, syntactic abilities have been shown to be impaired in the milder stages of nfPPA (Mesulam, Wieneke, Thompson, Rogalski, & Weintraub, 2012; Weintraub et al., 2009). For this reason, the grammaticality of the sentences

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produced in the sentence completion task was also examined. Not surprisingly, grammaticality was more impaired in the nfPPA than in the svPPA patients. We also analysed the verb tense in comparison to the target. The results yielded an interesting finding. Similar to grammaticality, verb tense was also more impaired in the nfPPA patients. The nfPPA patients retained the appropriate verb tense in their response significantly less often than the svPPA patients and healthy controls. This may be consistent with the finding by Thompson et al. (1997), in which greater difficulties producing inflected than uninflected verb forms was reported for nfPPA patients. The present study makes several important contributions to our understanding of verb processing in general and to verb production in the nonfluent and semantic variants of PPA, in particular. First, the study directly compared the two variants, providing evidence for a verb deficit in both groups. However, the pattern of performance in the two groups suggests that verb deficits may arise from different levels. Specifically, verb deficits in svPPA seem to be largely restricted to the lexical– semantic level, as has been found in probable Alzheimer’s disease (Kim & Thompson, 2004). On the other hand, nfPPA patients showed a syntactic impairment, as revealed by the grammaticality and verb tense analysis. However, results of the present study show that the production patterns in our cohort of nfPPA patients are different from those of individuals with stroke-induced agrammatic aphasia (Barde et al., 2006; Breedin et al., 1998), which does not support the predictions made by Gordon and Dell’s (2003) model. Manuscript received 17 October 2013 Revised manuscript received 1 August 2014 Revised manuscript accepted 23 September 2014 First published online 30 October 2014

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Verb production in the nonfluent and semantic variants of primary progressive aphasia: the influence of lexical and semantic factors.

Differential patterns of impairment with respect to noun and verb production have been observed in the nonfluent and semantic variants of primary prog...
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