Eye, Head, and Body Coordination During Large Gaze Shifts in Rhesus Monkeys: Movement Kinematics and the Influence of Posture

Abstract

McCluskey MK, Cullen KE. Eye, head, and body coordination during large gaze shifts in rhesus monkeys: movement kinematics and the influence of posture. J Neurophysiol 97: 2976 -2991, 2007. First published January 17, 2007 doi:10.1152/jn.00822.2006. Coordinated movements of the eye, head, and body are used to redirect the axis of gaze between objects of interest. However, previous studies of eyehead gaze shifts in head-unrestrained primates generally assumed the contribution of body movement to be negligible. Here we characterized eye-head-body coordination during horizontal gaze shifts made by trained rhesus monkeys to visual targets while they sat upright in a standard primate chair and assumed a more natural sitting posture in a custom-designed chair. In both postures, gaze shifts were characterized by the sequential onset of eye, head, and body movements, which could be described by predictable relationships. Body motion made a small but significant contribution to gaze shifts that were Ն40°i n amplitude. Furthermore, as gaze shift amplitude increased (40 -120°), body contribution and velocity increased systematically. In contrast, peak eye and head velocities plateaued at velocities of ϳ250 -300°/s, and the rotation of the eye-in-orbit and head-on-body remained well within the physical limits of ocular and neck motility during large gaze shifts, saturating at ϳ35 and 60°, respectively. Gaze shifts initiated with the eye more contralateral in the orbit were accompanied by smaller body as well as head movement amplitudes and velocities were greater when monkeys were seated in the more natural body posture. Taken together, our findings show that body movement makes a predictable contribution to gaze shifts that is systematically influenced by factors such as orbital position and posture. We conclude that body movements are part of a coordinated series of motor events that are used to voluntarily reorient gaze and that these movements can be significant even in a typical laboratory setting. Our results emphasize the need for caution in the interpretation of data from neurophysiological studies of the control of saccadic eye movements and/or eye-head gaze shifts because single neurons can code motor commands to move the body as well as the head and eyes.

Effect of Reversible Inactivation of Superior Colliculus on Head Movements

“…This animal often oriented itself in the chair at an angle (i.e., with the right shoulder forward). The relatively large head movements are, therefore attributable to the position of the head on the body at the time of gaze onset (McCluskey and Cullen 2007).…”

Gaze and Attention Management for Embodied Conversational Agents

“…Research in neurophysiology has studied how humans and other primates carry out gaze shifts in a tightly connected dynamic process by coordinating eye, head, and body movements [Zangemeister and Stark 1982;André-Deshays et al 1988;Barnes 1979;Freedman and Sparks 2000;Uemura et al 1980;McCluskey and Cullen 2007]. Researchers measured these movements in highly controlled experiments, obtaining numeric data about kinematic properties such as movement range [Guitton and Volle 1987] and eye and head velocities [Guitton and Volle 1987;Freedman and Sparks 2000;Barnes 1979;Uemura et al 1980].…”

“…In this work, we focus on modeling gaze shifts: coordinated movements of the eyes, head, and body toward objects and information in the environment [Zangemeister and Stark 1982;McCluskey and Cullen 2007]. Gaze shifts serve as fundamental units of gaze behavior, which itself plays a key role in human communication.…”

Symmetries of the Central Vestibular System: Forming Movements for Gravity and a Three-Dimensional World

“…Since optic flow and inertial sensation can provide similar motion information, they converge on many neurons-that is, they connect to many of the same neurons in such a way that their activity is combined [1,2]. However, the head movements can be passive or intentional and can arise from rotations about different body axes; to take these factors into account in action and perception, the central vestibular system (CVS) changes the origin of sensorimotor reference frames [3][4][5][6][7][8]. By actively and circumstantially combining the different sensory and motor information, the CVS facilitates the ability to grasp a motion experience with whatever sensory information is relevant and available.…”