The visual motion detectors underlying ocular following responses in monkeys

Abstract

Psychophysical evidence indicates that visual motion can be sensed by low-level (energy-based) and high-level (feature-based) mechanisms. The present experiments were undertaken to determine which of these mechanisms mediates the initial ocular following response (OFR) that can be elicited at ultra-short latencies by sudden motion of large-field images. We used the methodology of Sheliga, Chen, Fitzgibbon, and Miles (Initial ocular following in humans: A response to first-order motion energy. Vision Research, 2005a), who studied the initial OFRs of humans, to study the initial OFRs of monkeys. Accordingly, we applied horizontal motion to: (1) vertical square-wave gratings lacking the fundamental (“missing fundamental stimulus”) and (2) vertical grating patterns consisting of the sum of two sinusoids of frequency 3 f and 4 f, which created a repeating pattern with beat frequency, f. Both visual stimuli share a critical property: when subject to 1/4-wavelength steps, their overall pattern (feature) shifts in the direction of the steps, whereas their major Fourier component shifts in the reverse direction (because of spatial aliasing). We found that the initial OFRs of monkeys to these stimuli, like those of humans, were always in the opposite direction to the 1/4-wavelength shifts, i.e., in the direction of the major Fourier component, consistent with detection by (low-level) oriented spatio-temporal filters as in the well-known energy model of motion analysis. Our data indicate that the motion detectors mediating the initial OFR have quantitatively similar properties in monkeys and humans, suggesting that monkeys provide a good animal model for the human OFR.