Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-17T17:28:17.978Z Has data issue: false hasContentIssue false
  • English
  • Français

Verbal Initiation, Suppression, and Strategy Use and the Relationship with Clinical Symptoms in Schizophrenia

Published online by Cambridge University Press:  22 June 2016

Andrew K. Martin ,
Emily C. Gibson ,
Bryan Mowry  and
Gail A. Robinson
Andrew K. Martin*
Affiliation:
Queensland Brain Institute, The University of Queensland, Brisbane, Australia Centre for Clinical Research, The University of Queensland, Brisbane, Australia
Emily C. Gibson
Affiliation:
Neuropsychology Research Unit, School of Psychology, The University of Queensland, Brisbane, Australia
Bryan Mowry
Affiliation:
Queensland Brain Institute, The University of Queensland, Brisbane, Australia Queensland Centre for Mental Health Research, The University of Queensland, Brisbane, Australia
Gail A. Robinson
Affiliation:
Neuropsychology Research Unit, School of Psychology, The University of Queensland, Brisbane, Australia
*
Correspondence and reprint requests to: Andrew K. Martin, Queensland Brain Institute, The University of Queensland, Brisbane, Australia. E-mail: a.martin11@uq.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives: Individuals with schizophrenia have difficulties on measures of executive functioning such as initiation and suppression of responses and strategy development and implementation. The current study thoroughly examines performance on the Hayling Sentence Completion Test (HSCT) in individuals with schizophrenia, introducing novel analyses based on initiation errors and strategy use, and association with lifetime clinical symptoms. Methods: The HSCT was administered to individuals with schizophrenia (N=77) and age- and sex-matched healthy controls (N=45), along with background cognitive tests. The standard HSCT clinical measures (initiation response time, suppression response time, suppression errors), composite initiation and suppression error scores, and strategy-based responses were calculated. Lifetime clinical symptoms [formal thought disorder (FTD), positive, negative] were calculated using the Lifetime Dimensions of Psychosis Scale. Results: After controlling for baseline cognitive differences, individuals with schizophrenia were significantly impaired on the suppression response time and suppression error scales. For the novel analyses, individuals with schizophrenia produced a greater number of initiation errors and subtly wrong errors, and produced fewer responses indicative of developing an appropriate strategy. Strategy use was negatively correlated with FTD symptoms in individuals with schizophrenia. Conclusions: The current study provides further evidence for deficits in the initiation and suppression of verbal responses in individuals with schizophrenia. Moreover, an inability to attain a strategy at least partly contributes to increased semantically connected errors when attempting to suppress responses. The association between strategy use and FTD points to the involvement of executive deficits in disorganized speech in schizophrenia. (JINS, 2016, 22, 735–743)

Keywords

SchizophreniaInitiationSuppressionFormal thought disorderDisorganized speechHayling sentence completion task
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 22 , Issue 7 , August 2016 , pp. 735 - 743
Copyright
Copyright © The International Neuropsychological Society 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., rev.). Washington, DC: American Psychiatric Association.Google Scholar
Arcuri, S.M., Broome, M.R., Giampietro, V., Amaro, E. Jr., Kircher, T.T., Williams, S.C., & McGuire, P.K. (2012). Faulty suppression of irrelevant material in patients with thought disorder linked to attenuated frontotemporal activation. Schizophrenia Research Treatment, 2012, 176290. doi:10.1155/2012/176290 CrossRefGoogle ScholarPubMed
Aron, A.R., Fletcher, P.C., Bullmore, E.T., Sahakian, B.J., & Robbins, T.W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nature Neuroscience, 6(2), 115–116. doi:10.1038/nn1003 Google Scholar
Aron, A.R., Robbins, T.W., & Poldrack, R.A. (2014). Inhibition and the right inferior frontal cortex: One decade on. Trends in Cognitive Science, 18(4), 177–185. doi:10.1016/j.tics.2013.12.003 Google Scholar
Borofsky, L.A., McNealy, K., Siddarth, P., Wu, K.N., Dapretto, M., & Caplan, R. (2010). Semantic processing and thought disorder in childhood-onset schizophrenia: Insights from fMRI. Journal of Neurolinguistics, 23(3), 204–222. doi:10.1016/j.jneuroling.2009.07.004 CrossRefGoogle ScholarPubMed
Burgess, P.W., & Shallice, T. (1996). Response suppression, initiation and strategy use following frontal lobe lesions. Neuropsychologia, 34(4), 263–272. doi:0028-3932(95)00104-2 [pii] Google Scholar
Burgess, P.W., & Shallice, T. (1997). The Hayling and Brixton tests. Suffolk, UK: Thames Valley Test Company.Google Scholar
Cipolotti, L., Healy, C., Spano, B., Lecce, F., Biondo, F., Robinson, G., & Bozzali, M. (2016). Strategy and suppression impairments after right lateral and orbito-frontal lesions. Brain, 139, e10.Google Scholar
Clark, L.K., Warman, D., & Lysaker, P.H. (2010). The relationships between schizophrenia symptom dimensions and executive functioning components. Schizophrenia Research, 124(1-3), 169–175. doi:10.1016/j.schres.2010.08.004 Google Scholar
Collette, F., Van der Linden, M., Delfiore, G., Degueldre, C., Luxen, A., & Salmon, E. (2001). The functional anatomy of inhibition processes investigated with the Hayling task. Neuroimage, 14(2), 258–267. doi:10.1006/nimg.2001.0846 Google Scholar
Fioravanti, M., Carlone, O., Vitale, B., Cinti, M.E., & Clare, L. (2005). A meta-analysis of cognitive deficits in adults with a diagnosis of schizophrenia. Neuropsychology Review, 15(2), 73–95. doi:10.1007/s11065-005-6254-9 Google Scholar
Fleck, M.S., Daselaar, S.M., Dobbins, I.G., & Cabeza, R. (2006). Role of prefrontal and anterior cingulate regions in decision-making processes shared by memory and nonmemory tasks. Cerebral Cortex, 16(11), 1623–1630. doi:10.1093/cercor/bhj097 CrossRefGoogle ScholarPubMed
Gershon, E.S., DeLisi, L.E., Hamovit, J., Nurnberger, J.I. Jr., Maxwell, M.E., Schreiber, J., & Guroff, J.J. (1988). A controlled family study of chronic psychoses. Schizophrenia and schizoaffective disorder. Archives of General Psychiatry, 45(4), 328–336.Google Scholar
Goldberg, T.E., Aloia, M.S., Gourovitch, M.L., Missar, D., Pickar, D., & Weinberger, D.R. (1998). Cognitive substrates of thought disorder, I: The semantic system. The American Journal of Psychiatry, 155(12), 1671–1676.Google Scholar
Guillem, F., Rinaldi, M., Pampoulova, T., & Stip, E. (2008). The complex relationships between executive functions and positive symptoms in schizophrenia. Psychological Medicine, 38(6), 853–860. doi:10.1017/S0033291707002577 CrossRefGoogle ScholarPubMed
Hoffman, R.E., Stopek, S., & Andreasen, N.C. (1986). A comparative study of manic vs schizophrenic speech disorganization. Archives of General Psychiatry, 43(9), 831–838.Google Scholar
Joshua, N., Gogos, A., & Rossell, S. (2009). Executive functioning in schizophrenia: A thorough examination of performance on the Hayling Sentence Completion Test compared to psychiatric and non-psychiatric controls. Schizophrenia Research, 114(1-3), 84–90. doi:10.1016/j.schres.2009.05.029 Google Scholar
Kaladjian, A., Jeanningros, R., Azorin, J.M., Grimault, S., Anton, J.L., & Mazzola-Pomietto, P. (2007). Blunted activation in right ventrolateral prefrontal cortex during motor response inhibition in schizophrenia. Schizophrenia Research, 97(1-3), 184–193. doi:10.1016/j.schres.2007.07.033 CrossRefGoogle ScholarPubMed
Kerns, J.G., & Berenbaum, H. (2002). Cognitive impairments associated with formal thought disorder in people with schizophrenia. Journal of Abnormal Psychology, 111(2), 211–224.Google Scholar
Kim, J.J., Kwon, J.S., Park, H.J., Youn, T., Kang, D.H., Kim, M.S., & Lee, M.C. (2003). Functional disconnection between the prefrontal and parietal cortices during working memory processing in schizophrenia: A [15(O)]H2O PET study. American Journal of Psychiatry, 160(5), 919–923.Google Scholar
Kircher, T.T., Liddle, P.F., Brammer, M.J., Williams, S.C., Murray, R.M., & McGuire, P.K. (2001). Neural correlates of formal thought disorder in schizophrenia: Preliminary findings from a functional magnetic resonance imaging study. Archives of General Psychiatry, 58(8), 769–774.Google Scholar
Levinson, D.F., Mowry, B.J., Escamilla, M.A., & Faraone, S.V. (2002). The Lifetime Dimensions of Psychosis Scale (LDPS): Description and interrater reliability. Schizophrenia Bulletin, 28(4), 683–695.Google Scholar
Martin, A.K., Mowry, B., Reutens, D., & Robinson, G.A. (2015). Executive functioning in schizophrenia: Unique and shared variance with measures of fluid intelligence. Brain and Cognition, 99, 57–67. doi:10.1016/j.bandc.2015.07.009 Google Scholar
Martin, A.K., Robinson, G., Reutens, D., & Mowry, B. (2014). Copy number deletion burden is associated with cognitive, structural, and resting-state network differences in patients with schizophrenia. Behavioural Brain Research, 272C, 324–334. doi:10.1016/j.bbr.2014.07.002 Google Scholar
Mathalon, D.H., & Ford, J.M. (2008). Divergent approaches converge on frontal lobe dysfunction in schizophrenia. The American Journal of Psychiatry, 165(8), 944–948. doi:10.1176/appi.ajp.2008.08050735 Google Scholar
Maxwell, M.E. (1992). Family Interview for Genetic Studies (FIGS): A manual for FIGS. Bethesda, MD: Clinical Neurogenetics Branch, Intramural Research Program, NIMH.Google Scholar
McIntosh, A.M., Whalley, H.C., McKirdy, J., Hall, J., Sussmann, J.E., Shankar, P., & Lawrie, S.M. (2008). Prefrontal function and activation in bipolar disorder and schizophrenia. American Journal of Psychiatry, 165(3), 378–384. doi:10.1176/appi.ajp.2007.07020365 Google Scholar
Miller, L.A., & Tippett, L.J. (1996). Effects of focal brain lesions on visual problem-solving. Neuropsychologia, 34(5), 387–398.CrossRefGoogle ScholarPubMed
Nathaniel-James, D.A., Fletcher, P., & Frith, C.D. (1997). The functional anatomy of verbal initiation and suppression using the Hayling Test. Neuropsychologia, 35(4), 559–566.Google Scholar
Nelson, H.E., & Willison, J.R. (1991). The revised national adult reading test - Test manual. Windsor: NFER-Nelson.Google Scholar
Nurnberger, J.I. Jr., Blehar, M.C., Kaufmann, C.A., York-Cooler, C., Simpson, S.G., Harkavy-Friedman, J., & Reich, T. (1994). Diagnostic interview for genetic studies. Rationale, unique features, and training. NIMH Genetics Initiative. Archives of General Psychiatry, 51(11), 849–859; discussion 863–864.Google Scholar
Rapp, A.M., & Steinhauser, A.E. (2013). Functional MRI of sentence-level language comprehension in schizophrenia: A coordinate-based analysis. Schizophrenia Research, 150(1), 107–113. doi:10.1016/j.schres.2013.07.019 CrossRefGoogle ScholarPubMed
Robinson, G., Shallice, T., & Cipolotti, L. (2005). A failure of high level verbal response selection in progressive dynamic aphasia. Cognitive Neuropsychology, 22(6), 661–694. doi:10.1080/02643290442000239 Google Scholar
Robinson, G.A., Cipolotti, L., Walker, D.G., Biggs, V., Bozzali, M., & Shallice, T. (2015). Verbal suppression and strategy use: A role for the right lateral prefrontal cortex? Brain, 138(Pt 4), 1084–1096. doi:10.1093/brain/awv003 Google Scholar
Roca, M., Parr, A., Thompson, R., Woolgar, A., Torralva, T., Antoun, N., & Duncan, J. (2010). Executive function and fluid intelligence after frontal lobe lesions. Brain, 133(Pt 1), 234–247. doi:10.1093/brain/awp269 Google Scholar
Royer, A., Schneider, F.C., Grosselin, A., Pellet, J., Barral, F.G., Laurent, B., & Lang, F. (2009). Brain activation during executive processes in schizophrenia. Psychiatry Research, 173(3), 170–176. doi:10.1016/j.pscychresns.2009.02.009 Google Scholar
Salgado-Pineda, P., Caclin, A., Baeza, I., Junque, C., Bernardo, M., Blin, O., & Fonlupt, P. (2007). Schizophrenia and frontal cortex: Where does it fail? Schizophrenia Research, 91(1-3), 73–81. doi:10.1016/j.schres.2006.12.028 Google Scholar
Savage, S., Hsieh, S., Piguet, O., & Hodges, J.R. (2009). Distinguishing language profiles in Progressive Aphasia: Introducing the SYD-BAT. Brain Impairment, 10(1), 114.Google Scholar
Simon, M.A., Giacomini, V., Ferrero, F., & Mohr, S. (2003). Is executive function associated with symptom severity in schizophrenia? European Archives of Psychiatry and Clinical Neuroscience, 253(4), 216–218. doi:10.1007/s00406-003-0421-x Google Scholar
Stirling, J., Hellewell, J., Blakey, A., & Deakin, W. (2006). Thought disorder in schizophrenia is associated with both executive dysfunction and circumscribed impairments in semantic function. Psychological Medicine, 36(4), 475–484. doi:10.1017/S0033291705006884 CrossRefGoogle ScholarPubMed
Stuss, D.T., Alexander, M.P., Shallice, T., Picton, T.W., Binns, M.A., Macdonald, R., & Katz, D.I. (2005). Multiple frontal systems controlling response speed. Neuropsychologia, 43(3), 396–417. doi:10.1016/j.neuropsychologia.2004.06.010 Google Scholar
Swofford, C.D., Scheller-Gilkey, G., Miller, A.H., Woolwne, B., & Mance, R. (2000). Double jeopardy: Schizophrenia and substance abuse. American Journal of Drug and Alcohol Abuse, 26(3), 343–353.Google Scholar
Ventura, J., Thames, A.D., Wood, R.C., Guzik, L.H., & Hellemann, G.S. (2010). Disorganization and reality distortion in schizophrenia: A meta-analysis of the relationship between positive symptoms and neurocognitive deficits. Schizophrenia Research, 121(1-3), 1–14. doi:10.1016/j.schres.2010.05.033 Google Scholar
Volle, E., de Lacy Costello, A., Coates, L.M., McGuire, C., Towgood, K., Gilbert, S., & Burgess, P.W. (2012). Dissociation between verbal response initiation and suppression after prefrontal lesions. Cerebral Cortex, 22(10), 2428–2440. doi:10.1093/cercor/bhr322 Google Scholar
Weinstein, S., Werker, J.F., Vouloumanos, A., Woodward, T.S., & Ngan, E.T. (2006). Do you hear what I hear? Neural correlates of thought disorder during listening to speech in schizophrenia. Schizophrenia Research, 86(1-3), 130–137. doi:10.1016/j.schres.2006.05.011 Google Scholar
Weschler, D. (1991). Weschler Abbreviated Scale of Intelligence (WASI). San Antonio: Pearson.Google Scholar