Abstract
Whether antisaccade errors in schizophrenia are due to defects in implementing saccadic inhibition or difficulty in generating novel responses is uncertain. We investigated whether antisaccade errors were related to difficulty in inhibiting saccades when subjects were asked to maintain steady fixation, a situation that does not require a novel response. We examined the ocular motor data of 15 schizophrenia subjects and 16 healthy subjects. We assessed fixation in two situations: first, during the period before target onset during each saccadic trial, and second, during fixation trials that were interspersed with saccadic trials. We found that schizophrenia subjects had higher rates of fixation losses than control subjects in both situations. Second, both in healthy and schizophrenia subjects, antisaccade error rate was positively correlated with the frequency of fixation losses in the preparatory period of saccadic trials, but not with the frequency of fixation losses during fixation trials. Third, antisaccade errors were more likely to occur in trials with unstable fixation than in trials with stable fixation. Last, antisaccade error rate was also correlated with prosaccade error rate. We conclude that antisaccade errors are related to difficulties with implementing inhibitory control in the saccadic system. However, the finding of a correlation between the error rates for antisaccades and prosaccades suggests that this is not specifically concerned with inhibiting the automatic prosaccade, but a more general deficit in implementing goal-oriented behavior.
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References
Amador X, Sackeim H, Mukherjee S, Halperin R, Neeley P, Maclin E, Schnur D (1991) Specificity of smooth pursuit eye movement and visual fixation abnormalities in schizophrenia. Comparison to mania and normal controls. Schizophr Res 5:135–144
Amador X, Malaspina D, Sackeim H, Coleman E, Kaufman C, Hasan A, Brown J (1995) Visual fixation and smooth pursuit eye movement abnormalities in subjects with schizophrenia and their relatives. J Neuropsychiatr 7:197–206
Barton J, Raoof M, Jameel O, Manoach D (2006) Task-switching with antisaccades versus no-go trials: a comparison of inter-trial effects. Exp Brain Res 172:114–119
Blair J, Spreen O (1989) Predicting premorbid IQ: a revision of the national adult reading test. Clin Neuropsychol 3:129–136
Boudet C, Bocca M, Chabot B, Delamillieure P, Brazo P, Denise P, Dollfus S (2005) Are eye movement abnormalities indicators of genetic vulnerability to schizophrenia? Eur Psychiatry 20:339–345
Broerse A, Crawford T, den Boer J (2001) Parsing cognition in schizophrenia using saccadic eye movements: a selective overview. Neuropsychologia 39:742–756
Calkins M, Iacono W, Curtis C (2003) Smooth pursuit and antisaccade performance evidence trait stability in schizophrenia subjects and their relatives. Int J Psychophysiol 49:139–146
Calkins M, Curtis C, Iacono W, Grove W (2004) Antisaccade performance is impaired in medically and psychiatrically healthy biological relatives of schizophrenia subjects. Schizophr Res 71:167–178
Clementz B, McDowell J, Zisook S (1994) Saccadic system functioning among schizophrenia subjects and their first-degree biological relatives. J Abnorm Psychol 103:277–287
Crawford T, Haeger B, Kennard C, Reveley M, Henderson L (1995) Saccadic abnormalities in psychotic subjects. I. Neuroleptic-free psychotic subjects. Psychol Med 25:461–471
Crawford TJ, Puri BK, Nijran KS, Jones B, Kennard C, Lewis SW (1996) Abnormal saccadic distractibility in subjects with schizophrenia: a 99mTc-HMPAO SPET study. Psychol Med 26:265–277
Curtis C, Calkins M, Iacono W (2001) Saccadic disinhibition in schizophrenia subjects and their first-degree biological relatives. A parametric study of the effects of increasing inhibitory load. Exp Brain Res 137:228–236
De Jong R, Coles M, Logan G, Gratton G (1990) In search of the point of no return: the control of response processes. J Exp Psychol Hum Percept Perform 16:164–182
De Jong R, Coles M, Logan G (1995) Strategies and mechanisms in nonselective and selective inhibitory motor control. J Exp Psychol Hum Percept Perform 21:498–511
Donohoe G, Reilly R, Clarke S, Meredith S, Green B, Morris D, Gill M, Corvin A, Garavan H, Robertson I (2006) Do antisaccade deficits in schizophrenia provide evidence of a specific inhibitory function? J Int Neuropsychol Soc 12:901–906
Doricchi F, Perani D, Incoccia C, Grassi F, Cappa SF, Bettinardi V, Galati G, Pizzamiglio L, Fazio F (1997) Neural control of fast-regular saccades and antisaccade: an investigation using positron emission tomography. Exp Brain Res 116:50–62
Everling S, Munoz DP (2000) Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. J Neurosci 20:387–400
Everling S, Dorris MC, Klein RM, Munoz DP (1999) Role of primate superior colliculus in preparation and execution of anti-saccades and pro-saccades. J Neurosci 19:2740–2754
First M, Spitzer R, Gibbon M, Williams J (1997) Structured clinical interview for DSM-IV axis I disorders, research version, subject edition with psychotic screen (SCID-I/P W/PSY SCREEN). Biometrics Research, New York State Psychiatric Institute, New York
Fischer B, Breitmeyer B (1987) Mechanisms of visual attention revealed by saccadic eye movements. Neuropsychologia 25:73–83
Fukushima J, Morita N, Fukushima K, Chiba T, Tanaka S, Yamashita I (1990a) Voluntary control of saccadic eye movements in subjects with schizophrenic and affective disorders. J Psychiatr Res 24:9–24
Fukushima J, Fukushima K, Morita N, Yamashita I (1990b) Further analysis of the control of voluntary saccadic eye movements in schizophrenic subjects. Biol Psychiatry 28:943–958
Fukushima J, Fukushima K, Miyasaka K, Yamashita I (1994) Voluntary control of saccadic eye movement in subjects with frontal cortical lesions and parkinsonian subjects in comparison with that in schizophrenics. Biol Psychiatry 36:21–30
Gooding D, Tallent K (2001) The association between antisaccade task and working memory task performance in schizophrenia and bipolar disorder. J Nerv Ment Dis 189:8–16
Gooding D, Grabowski J, Hendershot C (2000) Fixation stability in schizophrenia, bipolar, and control subjects. Psychiatry Res 97:119–128
Gooding D, Mohapatra L, Shea H (2004) Temporal stability of saccadic task performance in schizophrenia and bipolar subjects. Psychol Med 34:921–932
Gottesman I, Gould T (2003) The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry 160:636–645
Hallett P, Adams B (1980) The predictability of saccadic latency in a novel voluntary oculomotor task. Vis Res 20:329–339
Hollingshead A (1965) Two factor index of social position. Yale University Press, New Haven
Hutton S, Ettinger U (2006) The antisaccade task as a research tool in psychopathology: a critical review. Psychophysiology 43:302–313
Hutton S, Kennard C (1998) Oculomotor abnormalities in schizophrenia. A critical review. Neurology 50:604–609
Hutton S, Joyce E, Barnes T, Kennard C (2002) Saccadic distractibility in first-episode schizophrenia. Neuropsychologia 40:1729–1736
Kay S, Fiszbein A, Opler L (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13:261–276
Kissler J, Clementz B (1998) Fixation stability among schizophrenia subjects. Neuropsychobiology 38:57–62
Levy D, Mendell N, LaVancher C et al (1998) Disinhibition in antisaccade performance in schizophrenia. In: Lenzenweger M, Dworkin R (eds) Origins and development of schizophrenia. American Psychological Association, Washington DC, pp 185–210
Levy D, O’Driscoll G, Matthysse S, Cook S, Holzman P, Mendell N (2004) Antisaccade performance in biological relatives of schizophrenia subjects: a meta-analysis. Schizophr Res 71:113–125
Manoach DS, Lindgren KA, Cherkasova MV, Goff DC, Halpern EF, Intriligator J, Barton JJS (2002) Schizophrenic subjects show deficient inhibition but intact task-switching on saccadic tasks. Biol Psychiatry 51:816–825
Maruff P, Danckert J, Pantelis C, Currie J (1998) Saccadic and attentional abnormalities in subjects with schizophrenia. Psychol Med 28:1091–1100
Matsue Y, Okuma T, Saito H, Aneha S, Ueno T, Chiba H, Matsuoka H (1986) Saccadic eye movements in tracking, fixation, and rest in schizophrenic and normal subjects. Biol Psychiatry 21:382–389
McDowell J, Brown G, Paulus M, Martinez A, Stewart S, Dubowitz D, Braff D (2002) Neural correlates of refixation saccades and antisaccades in normal and schizophrenia subjects. Biol Psychiatry 51:216–223
Meehl P (1970) Nuisance variables and the ex post facto design. In: Radner M, Winokur S (eds) Minnesota studies in the philosophy of science. University of Minnesota Press, Minneapolis, pp 373–402
Mialet J, Pichot P (1981) Eye-tracking patterns in schizophrenia. Arch Gen Psychiatry 38:183–186
Müller N, Riedel M, Eggert T, Straube A (1999) Internally and externally guided voluntary saccades in unmedicated and medicated schizophrenic subjects. Part II. Saccadic latency, gain, and fixation suppression errors. Eur Arch Psychiatry Clin Neurosci 249:7–14
Munoz D, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5:218–228
Nieman D, Bour L, Linszen D, Goede J, Koelman J, Gersons B, Ongerboer de Visser B (2000) Neuropsychological and clinical correlates of antisaccade task performance in szchizophrenia. Neurology 54:866–871
Nieuwenhuis S, Broerse A, Nielen M, de Jong R (2004) A goal activation approach to the study of executive function: an application to antisaccade tasks. Brain Cogn 56:198–214
Overall J, Gorham D (1962) The brief psychiatric rating scale. Psychol Rep 10:799–812
Paus T (1991) Two modes of central gaze fixation maintenance and oculomotor distractibility in schizophrenics. Schizophr Res 5:145–152
Radant A, Claypoole K, Wingerson D, Cowley D, Roy-Byrne P (1997) Relationships between neuropsychological and oculomotor measures in schizophrenia subjects and normal controls. Biol Psychiatry 42:797–805
Radant A, Dobie D, Calkins M, Olincy A, Braff D, Cadenhead K, Freedman R, Green M, Greenwood T, Gur R, Light G, Meichle S, Mintz J, Nuechterlein K, Schork N, Seidman L, Siever L, Silverman J, Stone W, Swerdlow N, Tsuang M, Turetsky B, Tsuang D (2006) Successful multi-site measurement of antisaccade performance deficits in schizophrenia. Schizophr Res 89:320–329
Raemaekers M, Jansma J, Cahn W, Van der Geest J, van der Linden J, Kahn R, Ramsey N (2002) Neuronal substrate of the saccadic inhibition deficit in schizophrenia investigated with 3-dimensional event-related functional magnetic resonance imaging. Arch Gen Psychiatry 59:313–320
Reuter B, Kathmann N (2004) Using saccade tasks as a tool to analyze executive dysfunctions in schizophrenia. Acta Psychol (Amst) 115:255–269
Roberts R, Hager L, Heron C (1994) Prefrontal cognitive processes: working memory and inhibition in the antisaccade task. J Exp Psychol Gen 123:374–393
Ross D, Ochs A, Hill M, Goldberg S, Pandurangi A, Winfrey C (1988) Erratic eye tracking in schizophrenic subjects as revealed by high-resolution techniques. Biol Psychiatry 24:675–688
Rosse RB, Schwartz BL, Kim SY, Deutsch SI (1993) Correlation between antisaccades and Wisconsin card sorting test performance in schizophrenia. Am J Psychiatry 150:333–335
Seidman L, Buka S, Goldstein J, Tsuang M (2006) Intellectual decline in schizophrenia: evidence from a prospective birth cohort 28 year follow-up study. J Clin Exp Neuropsychol 28:225–242
Sereno A, Holzman P (1995) Antisaccades and smooth pursuit eye movements in schizophrenia. Biol Psychiatry 37:394–401
Straube A, Riedel M, Eggert T, Muller N (1999) Internally and externally guided voluntary saccades in unmedicated and medicated schizophrenic subjects. Part I. Saccadic velocity. Eur Arch Psychiatry Clin Neurosci 249:1–6
White K, Ashton R (1976) Handedness assessment inventory. Neuropsychologia 14:261–264
Acknowledgments
DSM was supported by the National Institute for Mental Health (R01 MH67720), National Center for Research Resources (P41-RR14075), and the Mental Illness and Neuroscience Discovery (MIND) Institute (DOE-DE-FG02-99ER62764). J. J. S. B. was supported by CIHR grant MOP-81270, a Canada Research Chair, and a Senior Scholar award from the Michael Smith Foundation for Health Research.
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Barton, J.J.S., Pandita, M., Thakkar, K. et al. The relation between antisaccade errors, fixation stability and prosaccade errors in schizophrenia. Exp Brain Res 186, 273–282 (2008). https://doi.org/10.1007/s00221-007-1235-2
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DOI: https://doi.org/10.1007/s00221-007-1235-2