Orienting gaze toward a visual target: Neurophysiological synthesis with epistemological considerations

TL;DR

This paper critically examines the neurophysiological basis of gaze orientation, emphasizing the complexity of neural and muscular interactions beyond simple physical measurements, and offers a synthesis to guide future research across species.

Contribution

It provides a neurophysiological synthesis of gaze orienting mechanisms, challenging simplistic one-to-one mappings between physical orientation and neuronal activity, and highlights the complexity of visuomotor control.

Findings

Gaze movements involve complex intrinsic processes restoring poly-equilibrium.

Physical measurements may not directly reflect neuronal activity.

The synthesis aids future cross-species investigations.

Abstract

The appearance of an object triggers an orienting gaze movement toward its location. The movement consists of a rapid rotation of the eyes, the saccade, which is accompanied by a head rotation if the target eccentricity exceeds the oculomotor range, by a slow eye movement if it moves. Completing a previous report, we explain the numerous points that lead to questioning the validity of a one-to-one correspondence relation between measured physical values of gaze or head orientation and neuronal activity. Conflating kinematic (or dynamic) numerical values with neurophysiological recordings carries the risk of believing that central neuron activity directly encodes gaze or head orientation rather than mediating changes in extraocular and neck muscle contraction. Rather than reducing mismatches between extrinsic physical parameters (such as position or velocity errors), eye and head movements are behavioral expressions of intrinsic processes that restore a poly-equilibrium, i.e., balances of activities opposing antagonistic visuomotor channels. Past results obtained in the cat and monkey left a treasure allowing a synthesis, which illustrates the tremendous complexity underlying the changes in the orientations of the eyes and head. Its aim is to serve as a guide for further investigations in marmosets or for comparison with other species.