Neurophysiology of visual tracking in primates: From kinematic analysis to the poly-equilibrium theory

Recent technological developments facilitated the recording and quantitative analysis of eye movements, to the point where these movements are now widely used to probe diverse kinds of cognition (spatial, temporal, mathematical, social etc.). This article provides a comprehensive review of the basic neurophysiological aspects underlying gaze direction changes during saccadic and pursuit eye movements, with a focus on primate studies that highlights overlooked but critical complexities. The primary analysis of eye movement kinematics reveals that in response to a moving target, the tracking is not smoothly continuous, but instead composed of saccadic and pursuit eye movements. These components reflect parallel outputs of multiple visuomotor channels, each with distinct neural substrates. By examining the muscles, the neural structures and circuits in the left and right parts of the brainstem and cerebellum, we discover systems underlying the generation of horizontal and vertical movements. The review challenges the assumption of symmetrical neuronal populations or identical spiking activity between the left and right hemispheres during eye movements. Instead, gaze stability emerges from a dynamic equilibrium between “commands” and “anti-commands” distributed across the brain networks. This perspective unravels the neuronal complexity underlying the control of gaze direction, a complexity that psychological and computational models must integrate when using eye movements as markers of cognitive processes or as evidence of computations within the brain.