Efference copy failure during smooth pursuit eye movements in schizophrenia

Abstract

Abnormal smooth pursuit eye movements in patients with schizophrenia are often considered a consequence of impaired motion perception. Here we used a novel motion prediction task to assess the effects of abnormal pursuit on perception in human patients. Schizophrenia patients (n = 15) and healthy controls (n = 16) judged whether a briefly presented moving target ("ball") would hit/miss a stationary vertical line segment ("goal"). To relate prediction performance and pursuit directly, we manipulated eye movements: in half of the trials, observers smoothly tracked the ball; in the other half, they fixated on the goal. Strict quality criteria ensured that pursuit was initiated and that fixation was maintained. Controls were significantly better in trajectory prediction during pursuit than during fixation, their performance increased with presentation duration, and their pursuit gain and perceptual judgments were correlated. Such perceptual benefits during pursuit may be due to the use of extraretinal motion information estimated from an efference copy signal. With an overall lower performance in pursuit and perception, patients showed no such pursuit advantage and no correlation between pursuit gain and perception. Although patients' pursuit showed normal improvement with longer duration, their prediction performance failed to benefit from duration increases. This dissociation indicates relatively intact early visual motion processing, but a failure to use efference copy information. Impaired efference function in the sensory system may represent a general deficit in schizophrenia and thus contribute to symptoms and functional outcome impairments associated with the disorder.

Figure 1.

Trial sequence in eye soccer. A, Pursuit trial, step-ramp motion of target toward goal for 200 or 500 ms. B, Fixation trial, fixation on goal, ramp motion of ball toward fixation for 200 or 500 ms. For illustration purposes, eye position in each condition is indicated by red-dotted circles. C, Ball motion angles.

Figure 2.

Difference measures for pursuit versus fixation and long versus short presentation duration. A, Pursuit benefit calculated as performance in pursuit trials minus performance in fixation trials. B, Duration benefit calculated as performance in trials with long presentation duration minus performance with short duration. Black bars indicate results for controls and white bars indicate results for patients. Data are shown as means ± SE. Asterisks indicate results significantly different from zero in two-tailed t tests; *p < 0.05, **p < 0.01.

Figure 3.

Comparison of perceptual prediction performance between pursuit (squares, solid lines) and fixation (triangles, dashed lines) by group (filled symbols: controls, open symbols: patients) and presentation duration. For visibility purposes, results for the two groups are shown at an offset. A, Results for trials with correct pursuit/fixation in controls and patients. B, Results for trials with incorrect pursuit/fixation. Data are shown as means ± SE.

Figure 4.

Mean eye velocity traces. A, Controls (n = 16). B, Patients (n = 15). Solid red lines indicate eye movement responses for 200 ms presentation duration; solid blue lines are for 500 ms. Dashed red and blue lines mark stimulus offset at 200 and 500 ms, respectively. Shaded gray areas denote analysis intervals for open-loop measures (OL, light gray; smooth pursuit onset to 100 ms after pursuit onset) and closed-loop pursuit gain (CL, dark gray; 150–300 ms after pursuit onset). For demonstration purposes, the onset of the open-loop analysis window has been aligned with the group average pursuit onset (∼180 ms). Note that the pursuit analysis was done on a trial-by-trial basis relative to pursuit latency in each single trial.

Figure 5.

A, Gain versus perceptual judgments in controls. Colors denote presentation durations; solid lines are best-fit regression lines. Perceptual performance was significantly correlated with gain. B, Gain versus perceptual judgment in patients. Correlation was not significant.

Figure 6.

Mean eye position error. A, Results for controls. B, Results for patients. Pursuit data are indicated by solid lines; fixation data are dashed lines; trials with correct perceptual judgment (black) include hits and correct rejections, perceptual error trials (red) are misses and false alarms. Data are shown as means ± SE.