Reflexive tracking eye movements and motion perception: One or two neural populations?

Abstract

Motion-sensitive neurons in the middle temporal (MT) and medial superior temporal (MST) areas perform the sensory analysis required for both motion perception and controlling smooth eye movements. The perceptual and oculomotor systems are characterized by high variability, even when responding to identical stimulus repetitions. If a single population of neurons performs the motion analysis driving perception and eye movements, errors in perception and action might show similar direction-dependent biases, or their variability might be correlated across trials. However, previous studies have produced conflicting reports of the presence of significant single-trial correlations between motion perception and the velocity of smooth pursuit, a volitional tracking eye movement. We studied ocular following, a reflexive tracking eye movement, simultaneously measuring eye movement direction and perceived direction of a moving random dot field. Oculomotor errors were largest for near-cardinal directions, providing the first evidence for cardinal repulsion in reflexive eye movements. Biases in perceptual and oculomotor errors were correlated across test directions, but not across single trials with the same direction. Based on the similar direction-dependent anisotropies in eye movements and perception, there is reason to believe that partially overlapping populations of sensory neurons underlie motion perception and oculomotor behaviors, with independent downstream sources of noise masking trial-by-trial correlations between perception and action.