A Behavioral Receptive Field for Ocular Following in Monkeys: Spatial Summation and Its Spatial Frequency Tuning

Abstract

In human and nonhuman primates, reflexive tracking eye movements can be initiated at very short latency in response to a rapid shift of the image. Previous studies in humans have shown that only a part of the central visual field is optimal for driving ocular following responses. Herein, we have investigated spatial summation of motion information, across a wide range of spatial frequencies and speeds of drifting gratings by recording short-latency ocular following responses in macaque monkeys. We show that the optimal stimulus size for driving ocular responses cover a small (diameter, <20°), central part of the visual field that shrinks with higher spatial frequency. This signature of linear motion integration remains invariant with speed and temporal frequency. For low and medium spatial frequencies, we found a strong suppressive influence from surround motion, evidenced by a decrease of response amplitude for stimulus sizes larger than optimal. Such suppression disappears with gratings at high frequencies. The contribution of peripheral motion was investigated by presenting grating annuli of increasing eccentricity. We observed an exponential decay of response amplitude with grating eccentricity, the decrease being faster for higher spatial frequencies. Weaker surround suppression can thus be explained by sparser eccentric inputs at high frequencies. A difference-of-Gaussians model best renders the antagonistic contributions of peripheral and central motions. Its best-fit parameters coincide with several, well known spatial properties of area MT neuronal populations. These results describe the mechanism by which central motion information is automatically integrated in a context-dependent manner to drive ocular responses.