Is Motion Perception Deficit in Schizophrenia a Consequence of Eye-Tracking Abnormality?

BACKGROUND Studies have shown that schizophrenia patients have motion perception deficit, which was thought to cause eye-tracking abnormality in schizophrenia. However, eye movement closely interacts with motion perception. The known eye-tracking difficulties in schizophrenia patients may interact with their motion perception. METHODS Two speed discrimination experiments were conducted in a within-subject design. In experiment 1, the stimulus duration was 150 msec to minimize the chance of eye-tracking occurrence. In experiment 2, the duration was increased to 300 msec, increasing the possibility of eye movement intrusion. Regular eye-tracking performance was evaluated in a third experiment. RESULTS At 150 msec, speed discrimination thresholds did not differ between schizophrenia patients (n = 38) and control subjects (n = 33). At 300 msec, patients had significantly higher thresholds than control subjects (p = .03). Furthermore, frequencies of eye tracking during the 300 msec stimulus were significantly correlated with speed discrimination in control subjects (p = .01) but not in patients, suggesting that eye-tracking initiation may benefit control subjects but not patients. The frequency of eye tracking during speed discrimination was not significantly related to regular eye-tracking performance. CONCLUSIONS Speed discrimination, per se, is not impaired in schizophrenia patients. The observed abnormality appears to be a consequence of impairment in generating or integrating the feedback information from eye movements. This study introduces a novel approach to motion perception studies and highlights the importance of concurrently measuring eye movements to understand interactions between these two systems; the results argue for a conceptual revision regarding motion perception abnormality in schizophrenia.

[1]  N. Swerdlow,et al.  Characteristics of open- and closed-loop smooth pursuit responses among obsessive-compulsive disorder, schizophrenia, and nonpsychiatric individuals. , 1997, Psychophysiology.

[2]  D. Hommer,et al.  Early expression of smooth-pursuit eye movement abnormalities in children of schizophrenic parents. , 1996, Journal of the American Academy of Child and Adolescent Psychiatry.

[3]  A. Crawley,et al.  Functional MRI of lateral occipitotemporal cortex during pursuit and motion perception , 1996, Annals of neurology.

[4]  J. Jesberger,et al.  The relationship between smooth pursuit performance, motion perception and sustained visual attention in patients with schizophrenia and normal controls , 1997, Psychological Medicine.

[5]  W. Slaghuis,et al.  Eye movement and visual motion perception in schizophrenia II: global coherent motion as a function of target velocity and stimulus density , 2007, Experimental Brain Research.

[6]  Martin S. Banks,et al.  Perceived head-centric speed is affected by both extra-retinal and retinal errors , 1998, Vision Research.

[7]  A. Radant,et al.  Relationships between Neuropsychological and Oculomotor Measures in Schizophrenia Patients and Normal Controls , 1997, Biological Psychiatry.

[8]  J. Poulet,et al.  New insights into corollary discharges mediated by identified neural pathways , 2007, Trends in Neurosciences.

[9]  B. Clementz,et al.  Abnormality of smooth pursuit eye movement initiation: specificity to the schizophrenia spectrum? , 1995, Psychophysiology.

[10]  D R Medoff,et al.  Smooth pursuit eye movements to extraretinal motion signals: deficits in relatives of patients with schizophrenia. , 1998, Archives of general psychiatry.

[11]  E. J. Morris,et al.  Different responses to small visual errors during initiation and maintenance of smooth-pursuit eye movements in monkeys. , 1987, Journal of neurophysiology.

[12]  C. Rashbass,et al.  The relationship between saccadic and smooth tracking eye movements , 1961, The Journal of physiology.

[13]  Brian J. Murphy,et al.  Slow oculomotor control in the presence of moving backgrounds , 1975, Vision Research.

[14]  E. L. Keller,et al.  Generation of smooth-pursuit eye movements: neuronal mechanisms and pathways , 1991, Neuroscience Research.

[15]  P. Thier,et al.  Impaired analysis of moving objects due to deficient smooth pursuit eye movements. , 1999, Brain : a journal of neurology.

[16]  L. Elliot Hong,et al.  Components of the smooth pursuit function in deficit and nondeficit schizophrenia , 2003, Schizophrenia Research.

[17]  K. Nakayama,et al.  Motion perception in schizophrenia. , 1999, Archives of general psychiatry.

[18]  L. Elliot Hong,et al.  Response to unexpected target changes during sustained visual tracking in schizophrenic patients , 2005, Experimental Brain Research.

[19]  L Elliot Hong,et al.  Role of anticipation in schizophrenia-related pursuit initiation deficits. , 2006, Journal of neurophysiology.

[20]  K. Dobkins,et al.  Compromised speed discrimination among schizophrenia patients when viewing smooth pursuit targets , 2007, Schizophrenia Research.

[21]  Kathleen A Turano,et al.  Eye movements affect the perceived speed of visual motion , 1999, Vision Research.

[22]  M. Leek Adaptive procedures in psychophysical research , 2001, Perception & psychophysics.

[23]  B. Clementz,et al.  Smooth pursuit in schizophrenia: abnormalities of open- and closed-loop responses. , 1994, Psychophysiology.

[24]  C. Schroeder,et al.  Dysfunction of early-stage visual processing in schizophrenia. , 2001, The American journal of psychiatry.

[25]  B. Clementz Saccades to moving targets in schizophrenia: evidence for normal posterior cortex functioning. , 1996, Psychophysiology.

[26]  Frans A. J. Verstraten,et al.  Visual motion and the human brain: what has neuroimaging told us? , 2001, Acta psychologica.

[27]  K. Nakayama,et al.  Psychophysical isolation of a motion-processing deficit in schizophrenics and their relatives and its association with impaired smooth pursuit. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[28]  S. Lisberger,et al.  Properties of visual inputs that initiate horizontal smooth pursuit eye movements in monkeys , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  Mark W Greenlee,et al.  Coherent motion pops out during smooth pursuit , 2002, Neuroreport.

[30]  L. Elliot Hong,et al.  Refining the Predictive Pursuit Endophenotype in Schizophrenia , 2008, Biological Psychiatry.

[31]  Chul E. Kim,et al.  Accuracies of saccades to moving targets: During pursuit initiation and maintenance , 1995, Schizophrenia Research.

[32]  Robert W. Massof,et al.  Nonlinear contribution of eye velocity to motion perception , 2001, Vision Research.

[33]  Robert H. Wurtz,et al.  Influence of the thalamus on spatial visual processing in frontal cortex , 2006, Nature.

[34]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. , 1988, Journal of neurophysiology.

[35]  Robert W. Buchanan,et al.  Smooth pursuit eye movements to extra-retinal motion signals: deficits in patients with schizophrenia , 1999, Psychiatry Research.

[36]  R. Gellman,et al.  Motion processing for saccadic eye movements in humans , 2004, Experimental Brain Research.

[37]  J. Sweeney,et al.  Abnormalities in visually guided saccades suggest corticofugal dysregulation in never-treated schizophrenia , 2005, Biological Psychiatry.

[38]  J. Sweeney,et al.  Eye tracking abnormalities in schizophrenia: evidence for dysfunction in the frontal eye fields , 1998, Biological Psychiatry.

[39]  Hermann von Helmholtz,et al.  Treatise on Physiological Optics , 1962 .

[40]  A Pentland,et al.  Maximum likelihood estimation: The best PEST , 1980, Perception & psychophysics.

[41]  Peter Thier,et al.  False perception of motion in a patient who cannot compensate for eye movements , 1997, Nature.

[42]  E. Keller,et al.  Velocity prediction in corrective saccades during smooth-pursuit eye movements in monkey , 2004, Experimental Brain Research.

[43]  Berthold Hedwig,et al.  The Cellular Basis of a Corollary Discharge , 2006, Science.

[44]  Summer Sheremata,et al.  Compromised late-stage motion processing in schizophrenia , 2004, Biological Psychiatry.