Orienting Gaze Toward a Visual Target: Neurophysiological Synthesis with Epistemological Considerations

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 and by a slow eye movement if the target 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. Comparing the sole kinematic (or dynamic) numerical values with neurophysiological recordings carries the risk of believing that the activity of central neurons directly encodes gaze or head physical orientation rather than mediating changes in extraocular and neck muscle contraction, not to mention possible changes happening elsewhere (in posture, in the autonomous nervous system and more centrally). 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 cats and monkeys left a treasure of data allowing a synthesis, which illustrates the formidable complexity underlying the small changes in the orientations of the eyes and head. The aim of this synthesis is to serve as a new guide for further investigations or for comparison with other species.