action (verb) fluency in schizophrenia: getting a grip on odd speech

6
Action (verb) uency in schizophrenia: Getting a grip on odd speech Johanna C. Badcock a,b, , Milan Dragović a,b , Coleman Garrett b , Assen Jablensky a,b a School of Psychiatry and Clinical Neurosciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Perth, Australia b Centre for Clinical Research in Neuropsychiatry, Gascoyne House, John XXIII Avenue, Mt Claremont, WA 6010, Perth, Australia article info abstract Article history: Received 16 September 2010 Received in revised form 25 October 2010 Accepted 3 November 2010 Available online 15 December 2010 Background: Formal thought disorder (TD) is a key symptom of schizophrenia with a significant impact on interpersonal relationships. Current cognitive models emphasize disordered language functioning and abnormalities accessing semantic representations. The cortical mechanisms for language and motor function are closely linked, hence action-related language may be impaired in TD, yet existing studies have focussed exclusively on object (noun) rather than action (verb) semantics. Method: In order to examine this issue both action (verb) and traditional semantic (tools, fruits, musical instruments) and phonological (FAS) fluency tasks were completed by individuals with schizophrenia (N=53) and healthy controls (N=69). Fluency performance was measured as the total number of correct words generated in 60 s. The Schizotypal Personality Questionnaire (SPQ) was used to index odd and disorganized speech, as well as positive and negative symptoms. Results: Fluency on all tasks was impaired in schizophrenia, compared to controls, with a similar effect size. Within the schizophrenia group Odd Speech was correlated with poor fluency for actions, tools and musical instruments but not fruit or phonological fluency. These action-related fluency deficits were also correlated with Constricted Affect and Social Anxiety but not with Unusual Perceptions/Odd Beliefs. Conclusion: These results point to a unique connection and possible common aetiology between action fluency and odd speech in schizophrenia rather than a general impairment in language/executive functions common to fluency tasks. The findings provide the first evidence of a specific role of action-based language production deficits in TD together with a joint effect on social interaction skills. Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved. Keywords: Action uency Verb processing Semantic uency Phonological uency Schizophrenia Thought disorder 1. Introduction Formal thought disorder (TD) occurs in a range of acute psychotic conditions but in individuals with schizophrenia a residual level of thought disorder often persists, including during periods of remission and drug treatment (Levy et al., 2010). These trait-like disturbances in the form of thought are largely assessed by examining the patient's spoken language, which is character- ized by odd, disorganized or disconnected speech and verbal under-productivity (Andreasen and Grove, 1986; Harvey et al., 1984, 1990; Marengo and Harrow, 1987). Ongoing speech and language disturbance makes it difcult to engage in psychological treatments (Chrichton and Galletly, 2009; Clegg et al., 2007) or in everyday social interactions (Bowie and Harvey, 2008) and is a signicant predictor of poor outcome (Norman et al., 1999). Despite the clinical and personal signicance of TD, research- ers continue to grapple with the exact mechanisms involved. There is a growing convergence on the view that TD involves specic, rather than generalized, impairments in speech and language production (Covington et al., 2005; Marini, et al., 2008; Walenski et al., 2010) and semantic processing (Doughty et al., 2008; Elvevåg et al., 2002; Levy et al., 2010; Soriano et al., 2008). Schizophrenia Research 126 (2011) 138143 Corresponding author. Centre for Clinical Research in Neuropsychiatry, Private Mail Bag No1, Claremont, WA 6910, Australia. Tel.: + 61 8 9347 6429; fax: +61 8 9384 5128. E-mail addresses: [email protected] (J.C. Badcock), [email protected] (M. Dragović). 0920-9964/$ see front matter. Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.schres.2010.11.004 Contents lists available at ScienceDirect Schizophrenia Research journal homepage: www.elsevier.com/locate/schres

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Page 1: Action (verb) fluency in schizophrenia: Getting a grip on odd speech

Schizophrenia Research 126 (2011) 138–143

Contents lists available at ScienceDirect

Schizophrenia Research

j ourna l homepage: www.e lsev ie r.com/ locate /schres

Action (verb) fluency in schizophrenia: Getting a grip on odd speech

Johanna C. Badcock a,b,⁎, Milan Dragović a,b, Coleman Garrett b, Assen Jablensky a,b

a School of Psychiatry and Clinical Neurosciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Perth, Australiab Centre for Clinical Research in Neuropsychiatry, Gascoyne House, John XXIII Avenue, Mt Claremont, WA 6010, Perth, Australia

a r t i c l e i n f o

⁎ Corresponding author. Centre for Clinical ResearcPrivate Mail Bag No1, Claremont, WA 6910, Australia. Tfax: +61 8 9384 5128.

E-mail addresses: [email protected] ([email protected] (M. Dragović).

0920-9964/$ – see front matter. Crown Copyright ©doi:10.1016/j.schres.2010.11.004

a b s t r a c t

Article history:Received 16 September 2010Received in revised form 25 October 2010Accepted 3 November 2010Available online 15 December 2010

Background: Formal thought disorder (TD) is a key symptom of schizophrenia with asignificant impact on interpersonal relationships. Current cognitive models emphasizedisordered language functioning and abnormalities accessing semantic representations. Thecortical mechanisms for language and motor function are closely linked, hence action-relatedlanguage may be impaired in TD, yet existing studies have focussed exclusively on object(noun) rather than action (verb) semantics.Method: In order to examine this issue both action (verb) and traditional semantic (tools, fruits,musical instruments) and phonological (FAS) fluency tasks were completed by individualswith schizophrenia (N=53) and healthy controls (N=69). Fluency performance wasmeasured as the total number of correct words generated in 60 s. The Schizotypal PersonalityQuestionnaire (SPQ) was used to index odd and disorganized speech, as well as positive andnegative symptoms.Results: Fluency on all tasks was impaired in schizophrenia, compared to controls, with asimilar effect size. Within the schizophrenia group Odd Speech was correlated with poorfluency for actions, tools and musical instruments but not fruit or phonological fluency. Theseaction-related fluency deficits were also correlated with Constricted Affect and Social Anxietybut not with Unusual Perceptions/Odd Beliefs.Conclusion: These results point to a unique connection and possible common aetiologybetween action fluency and odd speech in schizophrenia rather than a general impairment inlanguage/executive functions common to fluency tasks. The findings provide the first evidenceof a specific role of action-based language production deficits in TD together with a joint effecton social interaction skills.

Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved.

Keywords:Action fluencyVerb processingSemantic fluencyPhonological fluencySchizophreniaThought disorder

1. Introduction

Formal thought disorder (TD) occurs in a range of acutepsychotic conditions but in individuals with schizophrenia aresidual level of thought disorder often persists, including duringperiodsof remissionanddrug treatment (Levyet al., 2010). Thesetrait-like disturbances in the formof thought are largely assessedby examining the patient's spoken language, which is character-

h in Neuropsychiatryel.: +61 8 9347 6429

.C. Badcock),

2010 Published by Els

,;

evier B.

ized by odd, disorganized or disconnected speech and verbalunder-productivity (Andreasen and Grove, 1986; Harvey et al.,1984, 1990; Marengo and Harrow, 1987). Ongoing speech andlanguagedisturbancemakes it difficult to engage inpsychologicaltreatments (Chrichton andGalletly, 2009; Clegg et al., 2007) or ineveryday social interactions (Bowie and Harvey, 2008) and is asignificant predictor of poor outcome (Norman et al., 1999).

Despite the clinical and personal significance of TD, research-ers continue to grapple with the exact mechanisms involved.There is a growing convergence on the view that TD involvesspecific, rather than generalized, impairments in speech andlanguage production (Covington et al., 2005; Marini, et al., 2008;Walenski et al., 2010) and semantic processing (Doughty et al.,2008; Elvevåg et al., 2002; Levy et al., 2010; Soriano et al., 2008).

V. All rights reserved.

Page 2: Action (verb) fluency in schizophrenia: Getting a grip on odd speech

Table 1Demographic, cognitive and clinical characteristics of participants.

SZ group(n=53)

HC group(n=69)

p-value a Effect size b

N (% males) N (% males)

Sex 46 (86.8) 49 (71.0) b0.05

Mean (SD) Mean (SD)

Age (years) 31.8 (8.8) 40.2 (13.2) b0.01Education (years) 10.7 (1.6) 13.4 (2.4) b0.01 1.32Premorbid IQ (NART) 95.0 (10.5) 109.6 (6.8) b0.01 1.65Current IQ (SILS) 89.0 (14.2) 110.7 (5.9) b0.01 1.99Medication(CPZ equivalent)

698.4 (346) –

Length ofillness (years)

10.8 (8.2) –

139J.C. Badcock et al. / Schizophrenia Research 126 (2011) 138–143

For example, Marini and colleagues concluded that languageproduction in schizophrenia consists of relatively mild andvariable difficulties at the microlinguistic level (involvingphonology, morphology and syntax), with more severe andpervasive deficits emerging at the macrolinguistic level (relatingto pragmatics).

Overall, studies of TD also point to the importance of left-sided, frontally-mediated mechanisms involved in languageproduction (Dibben et al., 2009; Horn et al., 2009; Champagne-Lavau and Stip, 2010). Tests of verbal fluency, involving the rapidgeneration of words under different constraints, are generallyconsidered to be particularly sensitive to frontal lobe functioning(Costafreda et al., 2006, 2009) and reduced hemisphericlateralization (Kircher et al., 2009; Knecht et al., 2000). Largeeffect sizes arepresent inbothphonological andsemanticfluencyin individuals with schizophrenia compared to healthy, non-clinical controls suggesting uniform difficulties in word genera-tion at the diagnostic level (Elvevåg et al., 2001), whilst at thesymptom level poor semantic fluency may be particularlyassociated with the presence of TD (Doughty and Done, 2009)though the evidence is inconsistent (DeFreitas et al., 2009).Previous fluency studies, however, have focused almost exclu-sively on object (noun) semantics despite mounting evidencethat action-related words (e.g. verbs) automatically engage adistributed network of motor-related regions in the frontal lobes(Fischer and Zwaan, 2008; Hickok, 2010; Pulvermüller, 2005;Tomasino et al., 2010). Thesemotor processes are notmerely by-products of post-lexical imagery, they are critical to normalspeech and language production. Furthermore, research bySemin (2009) shows that verbs possess functional properties(e.g. influencing causal attributions) that are central to successfulinterpersonal communication. Preliminary evidence of verbgeneration difficulties in schizophrenia has been provided in astudy by Woods et al. (2007) but neither specific symptomcorrelates nor the influence of motor abnormalites has beenexamined.

Given these findings we hypothesized that impaired pro-duction of action-related language may be an importantmechanism underpinning TD in schizophrenia. In order toinvestigate this possibility we first compared action (verb),semantic (noun) and phonological (letter) fluency performancebetween individuals with schizophrenia and healthy controls inorder to examine whether action fluency is differentiallyimpaired in the former. Following this we examined theassociation between action fluency and odd speech within theschizophrenia group to test the hypothesis that impaired actionfluency is linked to increasing levels of odd speech. In order totest the specificity of our findings we also examined theassociation between odd speech and phonological fluency,together with fluency for word categories that are, or are not,semantically linked to actions (tools, musical instruments vs.fruit respectively). Finally, we examined the role of motorasymmetry (handedness) andmotor speed in the production ofaction-related language.

SPQ total score 38.2 (16.7) 14.8 (9.9) b0.001 1.71Cognitive–perceptual 16.8 (8.5) 5.0 (4.2) b0.001 1.76Interpersonal 17.6 (7.7) 6.8 (6.2) b0.001 1.54Disorganization 8.2 (4.4) 4.1 (3.5) b0.001 1.03

Note. SPQ, Schizotypal Personality Questionnaire; NART, National AdultReading Test — Revised; SILS, Shipley Institute of Living Scales.

a χ2/t-test.b Cohen's d estimate.

2. Method

The study was approved by the Human Research EthicsCommittees of TheUniversity ofWesternAustralia and theNorthMetropolitan Area Mental Health Service in Perth, Western

Australia. Written informed consent was obtained from allparticipants prior to testing.

2.1. Participants

The following analysis is based on a sample of participantsdrawn from the West Australian Family Study of Schizophrenia(WAFSS; Hallmayer et al., 2005; Jablensky, 2006). All partici-pants who had completed the Action (Verb) fluency task wereincluded in the analysis (subject to exclusion criteria detailedbelow), yielding 53 patients (18–53 years) with a DSM-IV andICD-10 diagnosis of schizophrenia or schizophrenia spectrumdisorder (SZ group), together with 69 healthy (non-clinical)controls (HC; 19–60 years). Participant characteristics areshown in Table 1. Individualswith schizophreniawere recruitedfrom both inpatient and community-based services associatedwith Graylands Hospital, Perth and at the time of testing weretaking their usual antipsychotic medications (of 31% who weretaking antipsychotics—52.8%were receiving atypicals only, 5.7%typicals only, and 58.5% typicals and atypicals).

Healthy controls consisted of community volunteers, withno self-reported personal or family history of psychosis,recruited from the local community by random samplingfrom local telephone directories or among Red Cross blooddonors. Participants from both groups were screened toexclude a history of moderate–severe head trauma (loss ofconsciousnessN10 min), or neurological disorders, substanceabuse leading to treatment and systemic medical disease likelyto compromise cognitive function. Subjects who were notfluent speakers of English, had not completed at least 8th gradeeducation and/or were unable to give informed consent werealso excluded.

2.2. Clinical evaluation

Diagnostic assessment was based on standardized inter-views employing the Diagnostic Interview for Psychosis (DIP;

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140 J.C. Badcock et al. / Schizophrenia Research 126 (2011) 138–143

Castle et al., 2006) and scored using the OPCRIT diagnosticalgorithm (McGuffin, et al., 1991). Video-recorded interviewsand clinical charts were independently reviewed by two seniorclinicians who assigned consensus research diagnoses. Allpatients met both ICD-10 and DSM-IV criteria for a lifetimediagnosis of schizophrenia or schizophrenia spectrumdisorder.SZ participants were taking their usual medication at the timeof testing. Healthy community controls were also screened forpsychopathology using the DIP.

In addition, all study participants completed the 74-itemSchizotypal Personality Questionnaire (SPQ; Raine, 1991). Fromthis self-report questionnaire we derived individual's ratings onnine symptom subscales, and three composite factors (disorga-nization, cognitive/perceptual and interpersonal; Raine et al.,1994; Badcock and Dragović, 2006). The SPQ subscale OddSpeech was used to index ongoing, or trait-like, disturbances inspeech and language which was the focus of this study. The SPQhas acceptable internal consistency for all nine subscales(Cronbach's α range 0.71 to 0.78), and for the total score(Cronbach's α=0.91).

2.3. Cognitive assessment

All psychological testing was conducted individually, bytrained psychologists using standard administration procedures.

The action fluency task (Piatt et al., 1999) was used tomeasure an individual's capacity to generate action verbs.Participants were given the following instructions: “I wouldlike you to tell me as many different things as you can think ofthat people do. I do not want you to use the same word withdifferent endings, like eat, eaten, eating. Also, just give me singlewords suchas eat, or run, rather thana sentence. Canyougivemeone example of something that people do?” Unacceptableresponses were followed by a prompt to provide anotherexample of an action word. In the semantic fluency taskparticipants were required to produce as many differentresponses as possible for three semantic categories: tools, fruitsand musical instruments. In the phonological fluency taskparticipants were instructed to say as many words, beginningwith the specified letter (F, A or S), as they could (Benton et al.,1983). Each fluency task was scored by counting the totalnumber of appropriate responses generated in 60 s.

Current intelligence was estimated with the Shipley Instituteof Living Scale (Shipley, 1940; Zachary et al., 1985); whichcontains a 40-item vocabulary test and a 20-item test of abstractreasoning, from which estimates of WAIS-R full scale IQ(Wechsler, 1981) can be derived. Premorbid intellectual func-tioning was estimated using the National Adult Reading TestRevised (NART; Nelson and Willison, 1991; Crawford et al.,1992). NART-R error scores were also converted to WAIS-R IQscores. The Finger Tapping Test (Reitan, 1969) was used toexamine motor speed and coordination by comparing theaverage number of taps produced. Each participant firstcompleted a practice run to ensure the correct tapping stylewas used, which requires the wrist and forearm to lie flat on thetappingboardwhilst the indexfinger taps a brass plate byflexingand extending around the metacarpal–phalangeal joint. Partici-pants were instructed to “tap as rapidly as possible when youhear a tone, and stop when you hear a second tone (about 10 slater)”. Five trials were performed for each hand and the numberof taps for each hand was recorded. Finally, the Edinburgh

Inventory (EHI;Oldfield, 1971)was included to assess thedegreeof lateralization of handedness (lateralization quotient).

2.4. Data analysis

All analyses were performed using PASW Statistics 17. Thedata was initially screened for normality and outliers: valueswerenormallydistributedandnooutlierswerepresent. Betweengroups analyses aimed to examine both the severity and thefrequency of action fluency deficits. The groups differed on anumber of potential confounding variables, consequently re-peated measures analysis of covariance was used to examinewhether action fluency performance was differentially impairedin the SZ group relative to controls. Since Australian norms wereunavailable formostfluency tasks theperformanceof the currentsample of healthy controls— drawn from theWAFSS—was usedto calculate the percentage of individuals — in each group —

classified as impaired on allfluency tests, i.e., T-scoreb40. Finally,in order to test whether odd speech in the schizophrenia samplewas associated with a deficit in action fluency correlationsbetween SPQ subscales and fluency measures were examined.

3. Results

3.1. Between groups comparison (schizophrenia, controls)

As can be seen in Table 1, the two groups differedsignificantly in age, sex, years of education and intelligence. Ingeneral, controlswere older, had completedmore education andhad higher levels of intelligence. Repeated measures analysis ofcovariance (performance adjusted for age and education) wasconducted to examine performance between groups (SZ, HC)with total fluency scores (standardized action, semantic andphonological scores) as the within-subjects factor. The resultsshowed a largemain effect of group, F(1,115)=41.60, pb0.001,η2=0.27, no significant fluency task effect, F(2,230)=2.19,p=0.12, η2=0.02, and, importantly, no significant group byfluency task interaction, F(2,230)=1.21, p=0.30, η2=0.01.Univariate tests, summarized in Table 2, show that individualswith schizophrenia generated significantly fewer words on theaction fluency task, as well as on the semantic and phonologicaltasks, compared to the HC group—with a similar effect size foreach comparison.

Further analysis showed (Table 2) that only a small pro-portion of theHC group (10–17%) could be classified as impairedon any fluency task, i.e., T-scoreb40. Importantly, only 15.9% oftheHCgroupwas impaired on actionfluency compared to 66%ofthe SZ group, consequently the relationship between odd speechand action fluency was examined within the SZ group only.

3.2. Relationship between odd speech and action fluency withinthe SZ group

Pearson correlations between action, semantic and pho-nological fluency measures and SPQ subscale scores in theschizophrenia group are shown in Table 3. Action fluency wassignificantly, negatively correlated with Odd Speech, Con-stricted Affect and Social Anxiety, but was not significantlyassociated with positive psychotic symptom subscales (Un-usual Experiences, Odd Beliefs, and Ideas of Reference). At thefactor level action fluency was not significantly correlated

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Table 2Average action (verb), semantic and phonological fluency scores in theschizophrenia (SZ) and healthy control (HC) groups (unadjusted mean, SD)and percentage of individuals classified as impaired (T-score b40).

SZ group HC group p-value a Effectsize b

Action fluency 13.2 (5.6) 20.1 (4.9) b0.01 1.31Semantic fluency

Tool 9.8 (4.6) 13.9 (3.4) b0.01 1.01Music 12.2 (3.8) 16.7 (3.7) b0.01 1.20Fruit 10.5 (3.5) 15.6 (3.8) b0.01 1.40Total 32.5 (9.7) 46.2 (7.9) b0.01 1.55

Phonological fluency(FAS)

27.4 (10.4) 42.5 (11.7) b0.01 1.36

Action fluency (%) 66.0 15.9 b0.01 0.56Semantic fluency (%)

Tool (%) 58.5 17.4 b0.01 0.46Music (%) 73.6 11.6 b0.01 0.57Fruit (%) 54.7 10.1 b0.01 0.47

Phonological fluency(FAS, %)

73.6 11.6 b0.01 0.73

a t-test.b Cohen's d estimates (for t-tests) and odds ratios converted to Cohen's d

(for percentages).

Table 3Correlations between SPQ scores and action, semantic and phonological fluencyscores within the schizophrenia group.

SPQ subscales Fluency measures

Action Tools Fruit Musicalinstruments

Phonological

Ideas ofreference

−0.11 −0.24 −0.07 −0.22 −0.05

Social anxiety −0.31 −0.27 −0.29 −0.28 −0.18Odd beliefs −0.12 −0.12 −0.07 0.01 0.18Unusualperception

−0.18 −0.23 −0.26 −0.18 −0.02

Eccentricbehaviour

−0.16 −0.19 −0.24 −0.14 −0.23

No close friends −0.28 −0.27 −0.30 −0.32 −0.31Odd speech −0.31 −0.29 −0.12 −0.30 −0.16

Odd speech⁎ −0.30 −0.24 −0.10 −0.30 −0.16Odd speech⁎⁎ −0.33 −0.28 −0.09 −0.25 −0.12

Constricted affect −0.38 −0.31 −0.37 −0.37 −0.28Suspiciousness −0.19 −0.21 −0.10 −0.16 −0.13SPQ total score −0.30 −0.32 −0.26 −0.29 −0.17

Cogperc −0.18 −0.24 −0.14 −0.18 −0.02Interp −0.34 −0.33 −0.33 −0.33 −0.23Disorg −0.24 −0.25 −0.20 −0.24 −0.21

Motor speed(number of taps)

0.34 0.46 0.34 0.28 0.38

Fluency measuresTools .62 –

Fruit .58 .52 –

Musicalinstruments

.72 .44 .55 –

Phonological .61 .53 .58 .48 –

In bold pb0.05.⁎ Partial coefficient of correlations (adjusted for overall motor speed).⁎⁎ Partial coefficients of correlations (adjusted for age and education).

141J.C. Badcock et al. / Schizophrenia Research 126 (2011) 138–143

with Disorganization since action fluency scores are specifi-cally correlated with Odd Speech but not with EccentricBehaviour.

Examination of Table 3 shows that fluency for two ‘action-related’ semantic categories (tools andmusical instruments)wasalso significantly, negatively correlated with Odd Speech, butperformance on the semantic category ‘fruit’wasnot. In addition,whilst action and phonological fluency were significantly inter-correlated the relationship between phonological fluency andOdd Speech was not.

Follow-up correlations between laterality quotients on theEHI (Spearman's rho), length of illness or CPZ levels and action-related fluency tasks were calculated to examine whetherdifficulties generating action-related language in the SZ wereassociated with either increased duration of illness or decreasedcerebral lateralization.1 None of the correlations was significant(all psN0.05). Finally, the potential mediating or confoundingeffects of general motor speed, age and education, on therelationship between Odd Speech and action-related fluencymeasures was explored: partial coefficients of correlation werecalculated using the number of taps by both hands (indicator ofoverall motor speed) and all fluency measures (see Table 3).Similarly partial correlations (adjusted for age and education)were calculated between Odd Speech and all fluency measures(Table 3). The relationship (magnitude and statistical signifi-cance) between Odd Speech and action fluency was unchangedthough the association with both musical instruments and toolfluency was nowmarginally non-significant.

4. Discussion

The current results confirm the presence of a significantaction (verb) fluency deficit in a sizeable proportion ofindividuals with chronic schizophrenia (66%), with perfor-mance over 1 standard deviation below that of healthy controls

1 EHI quotients in this SZ group ranged from −80 to +100.

(d=−1.31; Woods et al., 2007). In addition, impairments insemantic and phonological fluency, with a similar effect size,were also evident in the schizophrenia sample. Thus at thegroup level there was no evidence of a differential impairmentin action fluency in schizophrenia (Elvevåg et al., 2001), unlikethat reported in other disorders (Bak et al., 2006; Bertella et al.,2002; Woods et al., 2010). This finding points to abnormalitiesin processes — and underlying neural structures — that arecommon toword generation tasks and is consistentwith recentevidence suggesting that impaired verbal fluency is associatedwith a less strongly connectedand less globally integratedbrainfunctional organization (Lynall et al., 2010).

Within the schizophrenia sample difficulty generating actionverbs was significantly associated with increased scores on OddSpeech (but not Eccentric Behaviour), together with higherscores on Constricted Affect and Social Anxiety. Elevated levels ofOdd Speech were also associated with poorer performancegenerating words for the semantic categories ‘tools’ and ‘musicalinstruments’but notwith the number ofwords generated for thecategory ‘fruit’ or for the phonological fluency task. This suggeststhat the association between action verbfluency andOddSpeechcannot simply be explained as an effect of generalized impair-ment in verbal production or executive functions common tofluency tasks or as a secondary effect of medication. Generatingresponses to the semantic categories ‘tools’ and ‘musicalinstruments’ does not involve production of verbs per se butobjects strongly associated with actions, consequently oneinterpretation of the current findings is that odd speech, whichis characteristic of TD, entails a specific impairment in the

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production of action-related language. A residual level of TDmaypersist in schizophrenia if this underlying mechanism has notbeen targeted during treatment.

The processing of action-related words normally engages adistributed cortical network including corresponding motorrepresentations in motor and premotor cortex. In contrast, thetemporoparietal region has been linked to noun retrieval(Damasio and Tranel, 1993). The current results build onthese earlier findings and significantly extend the first studiesof rapid verb generation in schizophrenia (Marvel, et al., 2004;Woods et al., 2007) which pointed to specific search — ratherthan selection—deficitswithin these somewhat separable verband noun processing networks in schizophrenia. In particular,one potential interpretation of the current data is that oddspeech characteristic of TD may arise as a result of relativelygreater difficulty activating frontal-motor brain regions. Con-sistent with this interpretation, reduced motor facilitation haspreviously been shown during action observation in schizo-phrenia (Enticott et al., 2008). We explored the possibility thatsuchdifficultiesmay arise fromaltered lateralizationof cerebralfunction in the SZ group (Crow, 2000; Costafreda et al., 2006).Previous reports show that handedness is linearly and highlysignificantly related to the side of language dominance (Knechtet al., 2000), however, there was no support in the current datafor a link between the observed deficit in action-relatedfluencyand lateralization of handedness. In contrast, significantcorrelations between fluency andmotor tapping tasks suggeststhat motor slowing may contribute — at least in part — to theobserved difficulties generating action-related language(Woods et al., 2005).

It is clear that more direct evidence is needed concerning thenatureand functional role, if any, of themotor/premotor cortex inTD, though recent research raises some interesting possibilities.For, example, somatotopic activation of motor and premotorcortex is elicited by idiomatic, as well as literal, expressionsrelated to actions (e.g. “she grasped the idea”; Boulenger et al.,2009); consequently, abnormal activation of these regions maycontribute to the pragmatic language dysfunction (such asdifficulties understanding non-literal language) commonly asso-ciated with TD. Previous research (Semin, 2009; Foroni andSemin, 2009) also illustrates the importance of action verbs insocial interaction and emotional expression, consequently adeficit in action fluency may have a joint impact on TD,constricted affect and social dysfunction. Clearly further researchis needed to investigate these suggestions.

Interestingly, action verb fluency was linked to Odd Speechbut not to Cognitive–Perceptual symptoms (Unusual Percep-tions/Odd Beliefs). Previous studies have argued that formalthought disorder and auditory hallucinations may co-occur, ororiginate from common disturbances in speech planning(Hoffman, 1986) and cortical language system dysfunctions(Horn et al., 2009; Sommer and Diederen, 2009). While thecurrent findings do not rule out the presence of overlappingcognitive and biological processes in TD and auditory halluci-nations, theydo suggest that somedistinctmechanismsare alsoinvolved (Ventura et al., 2010).

While the sample size was adequate in the current study, thewithin-subjects design is limited to analysis of correlations. Theexperimental fluency tasks used in the current project have beenused extensively in studies of schizophrenia but may notgeneralize to the production of action-related language in

everyday life. The fluency tasks used do not clearly differentiatebetween impairments due to a degraded store of knowledge ofaction verbs vs. difficulties gaining access to action-relatedlanguage. TD was also indexed by a self-report measure of oddspeech rather thanclinicianor observer ratedassessment. Finally,whilst action fluency impairment has been related to infectionwith human immunodeficiency virus (HIV), the HIV status ofparticipants in this study was unknown (Woods et al., 2005,2010).We are currently extending our research to examine verbproduction in natural language use and including both clinicianand observer assessments of TD.

Role of funding sourceThis project was conducted within the framework of theWestern Australian

Family Study of Schizophrenia, funded by grants #404046 and #513874 [to CIAProf. Assen Jablensky] from the National Health and Medical Research Council ofAustralia (NHMRC), with additional contributions from the North MetropolitanArea Health Services (NMAHS) in Perth, Western Australia; the NH&MRC andNMAHS had no further role in the design, analysis, interpretation and writing ofthe manuscript or in the decision to submit it for publication.

ContributorsJohanna Badcock designed the study and wrote the manuscript; Milan

Dragovic coded and retrieved the data from the WAFSS database, performed theanalyses, prepared tables and figures and commented on the completed draft ofthemanuscript. ColemanGarret providedgeneral research assistance, contributedto the initial review of the literature and performed preliminary analyses of data.Assen Jablensky reviewed diagnostic interviews and commented on the finalmanuscript. All authors contributed to themanuscript and agreed to submit it forpublication.

Conflict of interestAll other authors declare that they have no conflicts of interest.

AcknowledgementsWe thank Assoc/Prof. MikeWeinborn for his comments on an earlier draft of

this manuscript. We also thank all participants in the study, and the staff of theCentre for Clinical Research inNeuropsychiatry (CCRN) for assistancewith patientrecruitment.

References

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