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

Studies have found that motion perception is impaired in patients with schizophrenia and that higher motion perception thresholds are significantly correlated with poor eye tracking or smooth pursuit eye movement (SPEM) (1-4). These findings are generally interpreted as evidence of a motion-processing deficit causing the SPEM abnormality in schizophrenia. Many studies (3,5-10), including those from our own (11), have shown abnormal smooth pursuit onset in schizophrenia. Because response to initial target motion is a response to retinal motion before eye movement feedback occurs (12-14), abnormal initiation response suggests a motion perception impairment. However, this conflicts with studies that report normal or even faster onset latencies as well as accurate saccades and SPEMs in response to initial target motion in schizophrenia patients (10,14-18). Using unexpected target changes during smooth pursuit, we found that patients made more accurate response to unexpected target direction changes than healthy subjects, suggesting unimpaired motion processing during SPEM in schizophrenia patients (19). One possible explanation for the inconsistent findings on initiation responses could be the role of anticipation. We recently examined the effect of anticipation on pursuit initiation and found that when anticipation of pursuit onset was removed, schizophrenia patients and healthy subjects showed similar pursuit initiation; when anticipation was introduced, schizophrenia patients showed impaired pursuit onset (18). Based on these data, we hypothesize that motion processing per se is unimpaired and not the cause of eye-tracking abnormality observed in schizophrenia. If true, then how does one explain the findings of impaired speed discrimination in schizophrenia patients? Eye movements are known to closely interact with motion perception (20,21). A critical methodological weakness of previous motion perception studies in schizophrenia was that no attempts were made to monitor eye movements. One cannot rule out the possibility that the observed motion perception problem in schizophrenia may be a consequence rather than the source of the patients’ known SPEM difficulty. Smooth pursuit eye movements occur frequently in motion perception tasks because humans have difficulty holding their eyes still when presented with moving images (22). Smooth pursuit eye movement is initiated in response to retinal motion, a moving image across the retina. The motor command to move the eye is considered a source of extraretinal motion information (21,23). The extraretinal motion signal is critical for normal motion perception (20,21). Data suggest that retinal motion and reafferent stimuli, i.e., the motion of the target image resulting from the eye movement, interact with the motor command to form an accurate motion perception (24,25). Traditional speed discrimination studies use motion of objects that are presented for a duration of 200 msec or longer, which is sufficient time to initiate SPEM and to generate a motor command that can be incorporated into the motion perception. Schizophrenia patients have specific problems in processing extraretinal motion information (26-28). Their poor motion perception could be derived from deficits in extraretinal rather than retinal motion processing, if the normal process of integrating the oculomotor command into motion perception (29) is impaired. This hypothesis can be studied by simultaneously examining motion perception and eye movements. A behavioral study that pinpoints whether the primary deficit is motion perception or SPEM has important implications for understanding the pathophysiology of schizophrenia, since these two visual functions are distinct in many brain areas. Motion perception involves the early visual pathway from lateral geniculate nucleus to primary visual cortex to middle temporal (MT) cortex, while SPEM pathway involves signals from this early visual pathway and also medio-superior temporal (MST), frontal, parietal, and cerebellar mechanisms (30-32). In this study, we hypothesized that speed discrimination deficit in schizophrenia patients described in previous studies may be affected by their eye-tracking difficulties. This hypothesis was tested in two contrasting experiments. In experiment 1, motion stimulus was presented for 150 msec duration, so the stimulus ended before the SPEM initiation, which generally occurs within 150 msec to 180 msec of target motion onset. Thus, the 150 msec condition should limit the influence of feedback information from eye movement during motion perception testing by minimizing the induction of eye movements (20). In consequence, we expected speed discrimination thresholds would not differ between schizophrenia patients and control subjects. In experiment 2, the motion stimulus was presented for 300 msec, intended to replicate the previous finding of speed discrimination deficit in schizophrenia patients. Eye movements were monitored in both experiments to determine whether or not individuals maintained fixation during motion perception testing and if they did not, to what extent eye movements contributed to the speed discrimination thresholds. A third experiment was performed to examine regular smooth pursuit and to determine whether subjects’ eye movements during speed discrimination are related to their capacity to pursue a moving target when they were instructed to do so.