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.

Spatiotemporal transformations for gaze control

“…For example, the current review only touches on egocentric models; we have already started applying these methods to investigate the neural coding of allocentric landmarks in the gaze system (Bharmauria, Sajad, Li, et al, 2020a; Bharmauria, Sajad, Yan, Sajad, Yan, Wang, & Crawford, 2020b). We have also started using this method to differentiate gaze, head, and reach transformations in frontal cortex during coordinated eye‐head‐hand reaches (Arora et al., 2019; Nacher et al, 2019). There is no reason to not take this further afield, such as the analysis of activity in areas involved in spatial navigation and spatial memory, including the hippocampus and entorhinal cortex, against ego‐ and allocentric models during complex tasks such as natural viewing and free‐moving navigation (Gulli et al., 2020; Meister & Buffalo, 2018).…”

Coupling of head and hand movements during eye-head-hand coordination: there is more to reaching than meets eye

“…3, C and D) and this could account for the vertical head movement that occurred after the gaze shift ended, simultaneously with the hand movement. Adding further support to this interpreta-tion of Arora et al (2019) findings, very recent evidence by Berger et al (2020) has shown that in freely moving monkeys performing either reaches, or walk-to-reach movement sequences, the activity in frontal and parietal cortex was correlated not only with hand kinematics, but also with translational head movements. The experiments by Berger et al (2020) highlight the fact that the classic approach of constraining movement in a single or in a couple of joints that has been widely used in neurophysiological studies of motor control to facilitate data analysis and results interpretation should be revised and novel task paradigms using reaching movements under whole body motion in various behavioral constrains should be used.…”

“…Altogether, the results of Arora et al (2019) suggest a stronger coupling of head and arm with respect to the eye that seems rather unexpected. However, a significant number of older-but also some recent-human studies are in line with their findings.…”

“…This last finding could account for one of the main findings reported by Arora and colleagues (2019), i.e., that the major component of head movement during the reaching task occurred mostly along the vertical axis and was coincident with hand movement. In fact, although Arora et al (2019) did not mention it explicitly, it is evident that all reach trajectories in their study had a large upward component (see their Fig. 3, C and D) and this could account for the vertical head movement that occurred after the gaze shift ended, simultaneously with the hand movement.…”

“…What happens when all three effectors i.e., eye, head, and hand move simultaneously and need to be coordinated? Arora et al (2019) were the first to address this question in nonhuman primates. In their study, two macaque monkeys were seated in front of a touchscreen where a visual target was presented in one of eight peripheral locations that covered a large part of the visual field.…”