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Working Memory and Attention Influence Antisaccade Error Rate in Schizophrenia

Published online by Cambridge University Press:  18 December 2018

Elizabeth H.X. Thomas*
Affiliation:
Monash Alfred Psychiatry Research Centre (MAPrc), The Alfred Hospital and Central Clinical School, Monash University, Melbourne, Australia
Susan L. Rossell
Affiliation:
Centre for Mental Health, Faculty of Health, Arts and Design, School of Health Sciences, Swinburne University, Melbourne, Australia St Vincent’s Mental Health, St Vincent’s Hospital, Melbourne, Australia
Jessica B. Myles
Affiliation:
Monash Alfred Psychiatry Research Centre (MAPrc), The Alfred Hospital and Central Clinical School, Monash University, Melbourne, Australia
Eric J. Tan
Affiliation:
Centre for Mental Health, Faculty of Health, Arts and Design, School of Health Sciences, Swinburne University, Melbourne, Australia St Vincent’s Mental Health, St Vincent’s Hospital, Melbourne, Australia
Erica Neill
Affiliation:
St Vincent’s Mental Health, St Vincent’s Hospital, Melbourne, Australia Melbourne Neuropsychiatry Centre, Department of Psychiatry, University of Melbourne and Melbourne Health, Melbourne, Australia
Sean P. Carruthers
Affiliation:
Centre for Mental Health, Faculty of Health, Arts and Design, School of Health Sciences, Swinburne University, Melbourne, Australia
Philip J. Sumner
Affiliation:
Centre for Mental Health, Faculty of Health, Arts and Design, School of Health Sciences, Swinburne University, Melbourne, Australia
Kiymet Bozaoglu
Affiliation:
Bruce Lefroy Centre for Genetic Health Research, Murdoch Children’s Research Institute, Melbourne, Australia Department of Paediatrics, University of Melbourne, Melbourne, Australia
Caroline Gurvich
Affiliation:
Monash Alfred Psychiatry Research Centre (MAPrc), The Alfred Hospital and Central Clinical School, Monash University, Melbourne, Australia
*
Correspondence and reprint requests to: Elizabeth H.X. Thomas, Monash Alfred Psychiatry Research Centre, Level 4, 607 St Kilda Road, Melbourne, VIC 3004, Australia. E-mail: elizabeth.thomas@monash.edu

Abstract

Objectives: Antisaccade error rate has been proposed to be one of the most promising endophenotypes for schizophrenia. Increased error rate in patients has been associated with working memory, attention and other executive function impairments. The relationship between antisaccade error rate and other neuropsychological processes in patients compared to healthy controls has not been explored in depth. This study aimed to replicate the finding of heightened antisaccade error rate in patients and determine which cognitive processes were most strongly associated with antisaccade error rate in both patients and controls. In addition, the study investigated whether different antisaccade task paradigms engage different cognitive processes. Methods: One hundred and ninety-one participants (54 patients with schizophrenia/schizoaffective disorder and 137 controls) completed the antisaccade task, which included both gap and step task parameters. Neuropsychological measures were obtained using the MCCB and the Stroop task. Results: The current study replicated a pronounced antisaccade error rate deficit in patients. In patients, working memory variance was most significantly associated with antisaccade errors made during the step condition, while attentional processes were most associated with errors made during the gap condition. In controls, overall global cognitive performance was most associated with antisaccade rates for both gap and step conditions. Conclusions: The current study demonstrates that in schizophrenia patients, but not controls, elevated antisaccade error rate is associated with attention and working memory, but not with global cognitive impairment or psychopathological processes. Our novel findings demonstrate that the gap and step conditions of the antisaccade task engage different cognitive processes. (JINS, 2019, 25, 174–183)

Type
Regular Research
Copyright
Copyright © The International Neuropsychological Society 2018 

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References

REFERENCES

Barton, J.J., Pandita, M., Thakkar, K., Goff, D.C., & Manoach, D.S. (2008). The relation between antisaccade errors, fixation stability and prosaccade errors in schizophrenia. Experimental Brain Research, 186(2), 273282.Google Scholar
Bittencourt, J., Velasques, B., Teixeira, S., Basile, L.F., Salles, J.I., Nardi, A.E., … Ribeiro, P. (2013). Saccadic eye movement applications for psychiatric disorders. Neuropsychiatric Disease and Treatment, 9, 1393.Google Scholar
Calkins, M.E., Curtis, C.E., Iacono, W.G., & Grove, W.M. (2004). Antisaccade performance is impaired in medically and psychiatrically healthy biological relatives of schizophrenia patients. Schizophrenia Research, 71(1), 167178.Google Scholar
Calkins, M.E., Iacono, W.G., & Curtis, C.E. (2003). Smooth pursuit and antisaccade performance evidence trait stability in schizophrenia patients and their relatives. International Journal of Psychophysiology, 49(2), 139146.Google Scholar
Cornblatt, B.A., Risch, N.J., Faris, G., Friedman, D., & Erlenmeyer-Kimling, L. (1988). The Continuous Performance Test, identical pairs version (CPT-IP): I. New findings about sustained attention in normal families. Psychiatry Research, 26(2), 223238.Google Scholar
Curtis, C.E., & D’Esposito, M. (2003). Persistent activity in the prefrontal cortex during working memory. Trends in Cognitive Sciences, 7(9), 415423.Google Scholar
Davidson, M., Galderisi, S., Weiser, M., Werbeloff, N., Fleischhacker, W.W., Keefe, R.S., … Rybakowski, J.K. (2009). Cognitive effects of antipsychotic drugs in first-episode schizophrenia and schizophreniform disorder: A randomized, open-label clinical trial (EUFEST). American Journal of Psychiatry, 166(6), 675682.Google Scholar
Delis, D.C., Kaplan, E., & Kramer, J.H. (2001). Delis-Kaplan executive function system (D-KEFS). San Antonio, TX: Psychological Corporation.Google Scholar
Dennis, M., Francis, D.J., Cirino, P.T., Schachar, R., Barnes, M.A., & Fletcher, J.M. (2009). Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. Journal of the International Neuropsychological Society, 15(03), 331343.Google Scholar
Dickinson, D., Ragland, J.D., Gold, J.M., & Gur, R.C. (2008). General and specific cognitive deficits in schizophrenia: Goliath defeats David? Biological Psychiatry, 64(9), 823827.Google Scholar
Donohoe, G., Reilly, R., Clarke, S., Meredith, S., Green, B., Morris, D., … Robertson, I.H. (2006). Do antisaccade deficits in schizophrenia provide evidence of a specific inhibitory function? Journal of the International Neuropsychological Society, 12(6), 901906.Google Scholar
Doricchi, F., Perani, D., Incoccia, C., Grassi, F., Cappa, S.F., Bettinardi, V., … Fazio, F. (1997). Neural control of fast-regular saccades and antisaccades: An investigation using positron emission tomography. Experimental Brain Research, 116(1), 5062.Google Scholar
Dorris, M.C., & Munoz, D.P. (1995). A neural correlate for the gap effect on saccadic reaction times in monkey. Journal of Neurophysiology, 73(6), 25582562.Google Scholar
Ettinger, U., Kumari, V., Crawford, T.J., Davis, R.E., Sharma, T., & Corr, P.J. (2003). Reliability of smooth pursuit, fixation, and saccadic eye movements. Psychophysiology, 40(4), 620628.Google Scholar
Gooding, D.C., & Basso, M.A. (2008). The tell-tale tasks: A review of saccadic research in psychiatric patient populations. Brain and Cognition, 68(3), 371390.Google Scholar
Gooding, D.C., Mohapatra, L., & Shea, H. (2004). Temporal stability of saccadic task performance in schizophrenia and bipolar patients. Psychological Medicine, 34(5), 921932.Google Scholar
Gooding, D.C., & Tallent, K.A. (2001). The association between antisaccade task and working memory task performance in schizophrenia and bipolar disorder. The Journal of Nervous and Mental Disease, 189(1), 816.Google Scholar
Greenwood, T.A., Braff, D.L., Light, G.A., Cadenhead, K.S., Calkins, M.E., Dobie, D.J., … Gur, R.C. (2007). Initial heritability analyses of endophenotypic measures for schizophrenia: The consortium on the genetics of schizophrenia. Archives of General Psychiatry, 64(11), 12421250.Google Scholar
Hallett, P. (1978). Primary and secondary saccades to goals defined by instructions. Vision Research, 18(10), 12791296.Google Scholar
Holahan, A.-L.V., & O’Driscoll, G.A. (2005). Antisaccade and smooth pursuit performance in positive-and negative-symptom schizotypy. Schizophrenia Research, 76(1), 4354.Google Scholar
Hutton, S.B. (2008). Cognitive control of saccadic eye movements. Brain and Cognition, 68(3), 327340.Google Scholar
Hutton, S.B., Huddy, V., Barnes, T.R., Robbins, T.W., Crawford, T.J., Kennard, C., & Joyce, E.M. (2004). The relationship between antisaccades, smooth pursuit, and executive dysfunction in first-episode schizophrenia. Biological Psychiatry, 56(8), 553559.Google Scholar
Karoumi, B., Ventre-Dominey, J., & Dalery, J. (1998). Predictive saccade behavior is enhanced in schizophrenia. Cognition, 68(3), B81B91.Google Scholar
Kay, S.R., Fiszbein, A., & Opfer, L.A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13(2), 261.Google Scholar
Keefe, R.S., & Harvey, P.D. (2012). Cognitive impairment in schizophrenia Novel antischizophrenia treatments (pp. 1137). New York: Springer.Google Scholar
Kiehl, K.A., Smith, A.M., Hare, R.D., & Liddle, P.F. (2000). An event-related potential investigation of response inhibition in schizophrenia and psychopathy. Biological Psychiatry, 48(3), 210221.Google Scholar
Klein, C., Brügner, G., Foerster, F., Müller, W., & Schweickhardt, A. (2000). The gap effect in pro-saccades and anti-saccades in psychometric schizotypes. Biological Psychology, 55(1), 2539.Google Scholar
Kumari, V., Ettinger, U., Crawford, T.J., Zachariah, E., & Sharma, T. (2005). Lack of association between prepulse inhibition and antisaccadic deficits in chronic schizophrenia: Implications for identification of schizophrenia endophenotypes. Journal of Psychiatric Research, 39(3), 227240.Google Scholar
Larrison, A.L., Ferrante, C.F., Briand, K.A., & Sereno, A.B. (2000). Schizotypal traits, attention and eye movements. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 24(3), 357372.Google Scholar
Lecrubier, Y., Sheehan, D.V., Weiller, E., Amorim, P., Bonora, I., Sheehan, K.H., … Dunbar, G.C. (1997). The Mini International Neuropsychiatric Interview (MINI). A short diagnostic structured interview: Reliability and validity according to the CIDI. European Psychiatry, 12(5), 224231.Google Scholar
Lee, J., & Park, S. (2005). Working memory impairments in schizophrenia: A meta-analysis. Journal of Abnormal Psychology, 114(4), 599.Google Scholar
Leigh, R., & Kennard, C. (2004). Using saccades as a research tool in the clinical neurosciences. Brain, 127(3), 460477.Google Scholar
Levy, D.L., Mendell, N.R., LaVancher, C.A., Brownstein, J., Krastoshevsky, O., Teraspulsky, L., … Holzman, P.S. (1998). Disinhibition in antisaccade performance in schizophrenia. In M.F. Lenzenweger & R.H. Dworkin (Eds.), Origins and development of schizophrenia: Advances in experimental psychopathology (pp. 185210). Washington, DC: American Psychological Association.Google Scholar
Louchart-de la Chapelle, S., Nkam, I., Houy, E., Belmont, A., Ménard, J.-F., Roussignol, A.-C., … Fouldrin, G. (2005). A concordance study of three electrophysiological measures in schizophrenia. American Journal of Psychiatry, 162(3), 466474.Google Scholar
MacDonald, A.W. III, Carter, C.S., Flory, J.D., Ferrell, R.E., & Manuck, S.B. (2007). COMT val158Met and executive control: A test of the benefit of specific deficits to translational research. Journal of Abnormal Psychology, 116(2), 306.Google Scholar
Mackeben, M., & Nakayama, K. (1993). Express attentional shifts. Vision Research, 33(1), 8590.Google Scholar
Malone, S.M., & Iacono, W.G. (2002). Error rate on the antisaccade task: Heritability and developmental change in performance among preadolescent and late-adolescent female twin youth. Psychophysiology, 39(5), 664673.Google Scholar
Mazhari, S., Price, G., Dragović, M., Waters, F.A., Clissa, P., & Jablensky, A. (2011). Revisiting the suitability of antisaccade performance as an endophenotype in schizophrenia. Brain and Cognition, 77(2), 223230.Google Scholar
McDowell, J., & Clementz, B.A. (1997). The effect of fixation condition manipulations on antisaccade performance in schizophrenia: Studies of diagnostic specificity. Experimental Brain Research, 115(2), 333344.Google Scholar
Menard, S. (1995). Applied logistic regression analysis: Sage university series on quantitative applications in the social sciences. Thousand Oaks, CA: Sage.Google Scholar
Miller, G.A., & Chapman, J.P. (2001). Misunderstanding analysis of covariance. Journal of Abnormal Psychology, 110(1), 40.Google Scholar
Minzenberg, M.J., Laird, A.R., Thelen, S., Carter, C.S., & Glahn, D.C. (2009). Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Archives of General Psychiatry, 66(8), 811822.Google Scholar
Mitchell, J.P., Macrae, C.N., & Gilchrist, I.D. (2002). Working memory and the suppression of reflexive saccades. Journal of Cognitive Neuroscience, 14(1), 95103.Google Scholar
Murman, D.L. (2015). The impact of age on cognition . Paper presented at the Seminars in Hearing. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4906299/ Google Scholar
Myles, J.B., Rossell, S.L., Phillipou, A., Thomas, E., & Gurvich, C. (2017). Insights to the schizophrenia continuum: A systematic review of saccadic eye movements in schizotypy and biological relatives of schizophrenia patients. Neuroscience & Biobehavioral Reviews, 72, 278300.Google Scholar
Nieman, D., Bour, L., Linszen, D., Goede, J., Koelman, J., Gersons, B., & de Visser, B.O. (2000). Neuropsychological and clinical correlates of antisaccade task performance in schizophrenia. Neurology, 54(4), 866871.Google Scholar
Nuechterlein, K.H., Green, M.F., Kern, R.S., Baade, L.E., Barch, D.M., Cohen, J.D., … Gold, J.M. (2008). The MATRICS Consensus Cognitive Battery, part 1: Test selection, reliability, and validity. American Journal of Psychiatry, 165(2), 203213.Google Scholar
Park, S., & Gooding, D.C. (2014). Working memory impairment as an endophenotypic marker of a schizophrenia diathesis. Schizophrenia Research: Cognition, 1(3), 127136.Google Scholar
Pierrot-Deseilligny, C., Rivaud, S., Gaymard, B., & Agid, Y. (1991). Cortical control of reflexive visually-guided saccades. Brain, 114(3), 14731485.Google Scholar
Radant, A.D., Millard, S.P., Braff, D.L., Calkins, M.E., Dobie, D.J., Freedman, R., … Gur, R.C. (2015). Robust differences in antisaccade performance exist between COGS schizophrenia cases and controls regardless of recruitment strategies. Schizophrenia Research, 163(1), 4752.Google Scholar
Reilly, J.L., Frankovich, K., Hill, S., Gershon, E.S., Keefe, R.S., Keshavan, M.S., … Sweeney, J.A. (2013). Elevated antisaccade error rate as an intermediate phenotype for psychosis across diagnostic categories. Schizophrenia Bulletin, 40(5), 10111021.Google Scholar
Reilly, J.L., Harris, M.S., Khine, T.T., Keshavan, M.S., & Sweeney, J.A. (2008). Reduced attentional engagement contributes to deficits in prefrontal inhibitory control in schizophrenia. Biological Psychiatry, 63(8), 776783.Google Scholar
Reuter, B., & Kathmann, N. (2004). Using saccade tasks as a tool to analyze executive dysfunctions in schizophrenia. Acta Psychologica, 115(2), 255269.Google Scholar
Roberts, R.J., Hager, L.D., & Heron, C. (1994). Prefrontal cognitive processes: Working memory and inhibition in the antisaccade task. Journal of Experimental Psychology: General, 123(4), 374.Google Scholar
Salvucci, D.D., & Goldberg, J.H. (2000). Identifying fixations and saccades in eye-tracking protocols . Paper presented at the Proceedings of the 2000 symposium on Eye tracking research & applications.Google Scholar
Sweeney, J., Mintun, M., Kwee, S., Wiseman, M., Brown, D., Rosenberg, D., & Carl, J. (1996). Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. Journal of Neurophysiology, 75(1), 454468.Google Scholar
Wechsler, D. (1997). WAIS-III: Administration and scoring manual: Wechsler adult intelligence scale. New York: Psychological Corporation.Google Scholar
Weickert, T.W., Goldberg, T.E., Gold, J.M., Bigelow, L.B., Egan, M.F., & Weinberger, D.R. (2000). Cognitive impairments in patients with schizophrenia displaying preserved and compromised intellect. Archives of General Psychiatry, 57(9), 907913.Google Scholar
World Medical Association. (2013). World medical association declaration of helsinki: Ethical principles for medical research involving human subjects. JAMA, 310(20), 21912194. doi:10.1001/jama.2013.281053Google Scholar
Zanelli, J., MacCabe, J., Toulopoulou, T., Walshe, M., McDonald, C., & Murray, R. (2009). Neuropsychological correlates of eye movement abnormalities in schizophrenic patients and their unaffected relatives. Psychiatry Research, 168(3), 193197.Google Scholar