Eye-head-hand coordination during visually guided reaches in head-unrestrained macaques

Abstract

Nonhuman primates have been used extensively to study eye-head coordination and eye-hand coordination, but the combination—eye-head-hand coordination—has not been studied. Our goal was to determine whether reaching influences eye-head coordination (and vice versa) in rhesus macaques. Eye, head, and hand motion were recorded in two animals with search coil and touch screen technology, respectively. Animals were seated in a customized “chair” that allowed unencumbered head motion and reaching in depth. In the reach condition, animals were trained to touch a central LED at waist level while maintaining central gaze and were then rewarded if they touched a target appearing at 1 of 15 locations in a 40° × 20° (visual angle) array. In other variants, initial hand or gaze position was varied in the horizontal plane. In similar control tasks, animals were rewarded for gaze accuracy in the absence of reach. In the Reach task, animals made eye-head gaze shifts toward the target followed by reaches that were accompanied by prolonged head motion toward the target. This resulted in significantly higher head velocities and amplitudes (and lower eye-in-head ranges) compared with the gaze control condition. Gaze shifts had shorter latencies and higher velocities and were more precise, despite the lack of gaze reward. Initial hand position did not influence gaze, but initial gaze position influenced reach latency. These results suggest that eye-head coordination is optimized for visually guided reach, first by quickly and accurately placing gaze at the target to guide reach transport and then by centering the eyes in the head, likely to improve depth vision as the hand approaches the target. NEW & NOTEWORTHY Eye-head and eye-hand coordination have been studied in nonhuman primates but not the combination of all three effectors. Here we examined the timing and kinematics of eye-head-hand coordination in rhesus macaques during a simple reach-to-touch task. Our most novel finding was that (compared with hand-restrained gaze shifts) reaching produced prolonged, increased head rotation toward the target, tending to center the binocular field of view on the target/hand.