Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-02T21:21:08.373Z Has data issue: false hasContentIssue false

Visuospatial encoding deficits and compensatory strategies in schizophrenia revealed by eye movement analysis during a working memory task

Published online by Cambridge University Press:  24 June 2014

Luca Cocchi*
Affiliation:
Melbourne Neuropsychiatry Centre, University of Melbourne, c/o National Neuroscience Facility, Melbourne, Australia Institute of Psychology, University of Lausanne, Switzerland Center for Psychiatric Neuroscience (CNP), Prilly, Switzerland Institute of Sport Science and Physical Education (ISSEP), University of Lausanne, Switzerland
Francesca Bosisio
Affiliation:
Institute of Psychology, University of Lausanne, Switzerland
André Berchtold
Affiliation:
Institute of Applied Mathematics (IMA), University of Lausanne, Switzerland
Alina Orita
Affiliation:
University Psychiatric Adult Department of Lausanne (DUPA), Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland
Martin Debbané
Affiliation:
Service Médico-Pédagogique, University of Geneva School of Medicine, Geneva, Switzerland
Stephen J. Wood
Affiliation:
Melbourne Neuropsychiatry Centre, University of Melbourne, c/o National Neuroscience Facility, Melbourne, Australia
Françoise Schenk
Affiliation:
Institute of Psychology, University of Lausanne, Switzerland Center for Psychiatric Neuroscience (CNP), Prilly, Switzerland Department of Physiology, University of Lausanne, Switzerland
*
Dr Luca Cocchi, Melbourne Neuropsychiatry Centre, The University of Melbourne, c/o National Neuroscience Facility, 161 Barry Street, Carlton South 3053, Australia. Tel: (+61 3) 8344 1861; Fax: (+61 3) 9348 0469; E-mail: [email protected]

Abstract

Objective:

To investigate scanpath abnormalities during the encoding of static stimuli in schizophrenia and their interaction with visuospatial working memory (VSWM) dysfunction.

Methods:

Outpatients with schizophrenia and control subjects were asked to encode a static pattern for subsequent recognition after a short delay. We measured the number of correct and incorrect choices. We also assessed the number and the distribution of fixations, the scanning time in specific regions of interest (ROIs) and the head movements during the encoding of the stimuli. The distributions of fixations and scanning time in definite ROIs during the discrimination of the correct pattern from the foils were also measured.

Results:

Patients recognised fewer correct patterns than controls. Correct trials in patients were characterised by a specific exploration of the central part of the stimulus during its presentation, whereas this feature was absent in incorrect trials. However, the scanning time and the numbers of fixations and head movements during encoding were similar in both groups and unrelated to recognition accuracy. In both groups, correct trials were associated with a selective exploration of the correct pattern amongst the six possibilities during recognition. Furthermore, patients gave more attention to incorrect patterns with a leftmost element identical to that of the correct response and also those approximating its global structure.

Conclusion:

Patients showed a VSWM deficit independent of oculomotor dysfunctions and head movements during encoding. Patients’ correct trials were related to specific scanning during encoding and discrimination phases. Analysis of these patterns suggests that patients try to compensate for reduced VSWM ability by using specific encoding strategies.

Type
Research Article
Copyright
Copyright © 2009 Blackwell Munksgaard

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

Pierrot-Deseilligny, C, Milea, D, Muri, RM.Eye movement control by the cerebral cortex. Curr Opin Neurol 2004;17:1725CrossRefGoogle ScholarPubMed
Pierrot-Deseilligny, C, Muri, RM, Nyffeler, T, Milea, D.The role of the human dorsolateral prefrontal cortex in ocular motor behavior. Ann N Y Acad Sci 2005;1039:239251CrossRefGoogle ScholarPubMed
Pierrot-Deseilligny, C, Muri, RM, Ploner, CJ, Gaymard, B, Demeret, S, Rivaud-Pechoux, S.Decisional role of the dorsolateral prefrontal cortex in ocular motor behaviour. Brain 2003;126:14601473CrossRefGoogle ScholarPubMed
Lee, J, Park, S.Working memory impairments in schizophrenia: a meta-analysis. J Abnorm Psychol 2005;114:599611CrossRefGoogle ScholarPubMed
Wood, SJ, Pantelis, C, Proffitt, Tet al. Spatial working memory ability is a marker of risk-for-psychosis. Psychol Med 2003;33:12391247CrossRefGoogle ScholarPubMed
Green, M, Williams, L, Hemsley, D.Cognitive theories of delusional formation: the contribution of visual scanpath research. Cognit Neuropsychiatry 2000;5:6374CrossRefGoogle Scholar
Phillips, ML, David, AS.Visual scan paths are abnormal in deluded schizophrenics. Neuropsychologia 1997;35:99105CrossRefGoogle ScholarPubMed
Phillips, ML, David, AS.Abnormal visual scan paths: a psychophysiological marker of delusions in schizophrenia. Schizophr Res 1998;29:235245CrossRefGoogle ScholarPubMed
Williams, LM, Loughland, CM, Gordon, E, Davidson, D.Visual scanpaths in schizophrenia: is there a deficit in face recognition? Schizophr Res 1999;40:189199CrossRefGoogle Scholar
Loughland, CM, Williams, LM, Gordon, E.Visual scanpaths to positive and negative facial emotions in an outpatient schizophrenia sample. Schizophr Res 2002;55:159170CrossRefGoogle Scholar
Kojima, T, Matsushima, E, Ando, Ket al. Exploratory eye movements and neuropsychological tests in schizophrenic patients. Schizophr Bull 1992;18:8594CrossRefGoogle ScholarPubMed
Loughland, CM, Williams, LM, Gordon, E.Schizophrenia and affective disorder show different visual scanning behavior for faces: a trait versus state-based distinction? Biol Psychiatry 2002;52:338348CrossRefGoogle ScholarPubMed
Minassian, A, Granholm, E, Verney, S, Perry, W.Visual scanning deficits in schizophrenia and their relationship to executive functioning impairment. Schizophr Res 2005;74:6979CrossRefGoogle ScholarPubMed
Nakayama, H, Morita, K, Mori, K, Hirai, S, Maeda, H.Improvement of exploratory eye movements in schizophrenic patients during recovery period. Psychiatry Clin Neurosci 2003;57:169176CrossRefGoogle ScholarPubMed
Obayashi, S, Matsushima, E, Ando, H, Ando, K, Kojima, T.Exploratory eye movements during the Benton Visual Retention Test: characteristics of visual behavior in schizophrenia. Psychiatry Clin Neurosci 2003;57:409415CrossRefGoogle ScholarPubMed
Manor, BR, Gordon, E, Williams, LMet al. Eye movements reflect impaired face processing in patients with schizophrenia. Biol Psychiatry 1999;46:963969CrossRefGoogle ScholarPubMed
Bestelmeyer, PE, Tatler, BW, Phillips, LH, Fraser, G, Benson, PJ, St Clair, D.Global visual scanning abnormalities in schizophrenia and bipolar disorder. Schizophr Res 2006;87:212222CrossRefGoogle ScholarPubMed
Hutton, SB, Huddy, V, Barnes, TRet al. The relationship between antisaccades, smooth pursuit, and executive dysfunction in first-episode schizophrenia. Biol Psychiatry 2004;56:553559CrossRefGoogle ScholarPubMed
Katsanis, J, Iacono, WG.Clinical, neuropsychological, and brain structural correlates of smooth-pursuit eye tracking performance in chronic schizophrenia. J Abnorm Psychol 1991;100:526534CrossRefGoogle ScholarPubMed
Litman, RE, Hommer, DW, Clem, T, Ornsteen, ML, Ollo, C, Pickar, D.Correlation of Wisconsin Card Sorting Test performance with eye tracking in schizophrenia. Am J Psychiatry 1991;148:15801582Google ScholarPubMed
Snitz, BE, Curtis, CE, Zald, DH, Katsanis, J, Iacono, WG.Neuropsychological and oculomotor correlates of spatial working memory performance in schizophrenia patients and controls. Schizophr Res 1999;38:3750CrossRefGoogle ScholarPubMed
Thaker, GK, Avila, MT, Hong, EL, Medoff, DR, Ross, DE, Adami, HM.A model of smooth pursuit eye movement deficit associated with the schizophrenia phenotype. Psychophysiology 2003;40:277284CrossRefGoogle Scholar
Cocchi, L, Schenk, F, Volken, H, Bovet, P, Parnas, J, Vianin, P.Visuo-spatial processing in a dynamic and a static working memory paradigm in schizophrenia. Psychiatry Res 2007;152:129142CrossRefGoogle Scholar
Uhlhaas, PJ, Silverstein, SM.Perceptual organization in schizophrenia spectrum disorders: empirical research and theoretical implications. Psychol Bull 2005;131:618632CrossRefGoogle ScholarPubMed
Butler, PD, Javitt, DC.Early-stage visual processing deficits in schizophrenia. Curr Opin Psychiatry 2005;18:151157CrossRefGoogle ScholarPubMed
Haenschel, C, Bittner, RA, Haertling, Fet al. Contribution of impaired early-stage visual processing to working memory dysfunction in adolescents with schizophrenia: a study with event-related potentials and functional magnetic resonance imaging. Arch Gen Psychiatry 2007;64:12291240CrossRefGoogle ScholarPubMed
Kurylo, DD, Pasternak, R, Silipo, G, Javitt, DC, Butler, PD.Perceptual organization by proximity and similarity in schizophrenia. Schizophr Res 2007;95:205214CrossRefGoogle ScholarPubMed
de Fockert, JW, Rees, G, Frith, CD, Lavie, N.The role of working memory in visual selective attention. Science 2001;291:18031806CrossRefGoogle ScholarPubMed
Gazzaley, A, Clapp, W, Kelley, J, McEvoy, K, Knight, RT, D'Esposito, M.Age-related top-down suppression deficit in the early stages of cortical visual memory processing. Proc Natl Acad Sci U S A 2008;105:1312213126CrossRefGoogle ScholarPubMed
Sheehan, DV, Lecrubier, Y, Sheehan, KHet al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 1998;59(Suppl. 20):2233; quiz 34–57Google ScholarPubMed
Woods, SW.Chlorpromazine equivalent doses for the newer atypical antipsychotics. J Clin Psychiatry 2003;64:663667CrossRefGoogle ScholarPubMed
Leucht, S, Wahlbeck, K, Hamann, J, Kissling, W.New generation antipsychotics versus low-potency conventional antipsychotics: a systematic review and meta-analysis. Lancet 2003;361:15811589CrossRefGoogle ScholarPubMed
Gitelman, DR.ILAB: a program for postexperimental eye movement analysis. Behav Res Methods Instrum Comput 2002;34:605612CrossRefGoogle ScholarPubMed
Liversedge, SP, Findlay, JM.Saccadic eye movements and cognition. Trends Cogn Sci 2000;4:614CrossRefGoogle ScholarPubMed
Altmann, CF, Bulthoff, HH, Kourtzi, Z.Perceptual organization of local elements into global shapes in the human visual cortex. Curr Biol 2003;13:342349CrossRefGoogle ScholarPubMed
Gazzaley, A, Cooney, JW, Rissman, J, D'Esposito, M.Top-down suppression deficit underlies working memory impairment in normal aging. Nat Neurosci 2005;8:12981300CrossRefGoogle ScholarPubMed
Gazzaley, A, D'Esposito, M.Top-down modulation and normal aging. Ann N Y Acad Sci 2007;1097:6783CrossRefGoogle ScholarPubMed
Nishiura, S, Morita, K, Kurakake, K, Igimi, H, Maeda, H.Characteristics of left and right scanning in schizophrenia patients using exploratory eye movements: comparison with healthy subjects. Psychiatry Clin Neurosci 2007;61:487494CrossRefGoogle ScholarPubMed
Gaebel, W, Ulrich, G, Frick, K.Visuomotor performance of schizophrenic patients and normal controls in a picture viewing task. Biol Psychiatry 1987;22:12271237CrossRefGoogle Scholar
Butler, PD, Harkavy-Friedman, JM, Amador, XF, Gorman, JM.Backward masking in schizophrenia: relationship to medication status, neuropsychological functioning, and dopamine metabolism. Biol Psychiatry 1996;40:295298CrossRefGoogle ScholarPubMed
Daban, C, Amado, I, Bourdel, MCet al. Cognitive dysfunctions in medicated and unmedicated patients with recent-onset schizophrenia. J Psychiatr Res 2005;39:391398CrossRefGoogle ScholarPubMed
Cocchi, L, Bosisio, F, Carter, O, Wood, SJ, Berchtold, F, Conus, P, Orita, A, Debanné, M, Schenk, F.Visuospatial working memory deficits and visual pursuit impairments are not directly related in schizophrenia. Aust New Zeal J Psychiatr in pressGoogle Scholar