The Journal of Neurophysiology Vol. 77 No. 5 May 1997, pp. 2328-2348
Copyright ©1997 The American Physiological Society

Eye-Head Coordination During Head-Unrestrained Gaze Shifts in Rhesus Monkeys

Edward G. Freedman¹ and David L. Sparks^{1, 2}

¹ Institute of Neurological Sciences and ² Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6196

Freedman, Edward G. and David L. Sparks. Eye-head coordination during head-unrestrained gaze shifts in rhesus monkeys. J. Neurophysiol. 77: 2328-2348, 1997. We analyzed gaze shifts made by trained rhesus monkeys with completely unrestrained heads during performance of a delayed gaze shift task. Subjects made horizontal, vertical, and oblique gaze shifts to visual targets. We found that coordinated eye-head movements are characterized by a set of lawful relationships, and that the initial position of the eyes in the orbits and the direction of the gaze shift are two factors that influence these relationships. Head movements did not contribute to the change in gaze position during small gaze shifts (<20°) directed along the horizontal meridian, when the eyes were initially centered in the orbits. For larger gaze shifts (25-90°), the head contribution to the gaze shift increased linearly with increasing gaze shift amplitude, and eye movement amplitude saturated at an asymptotic amplitude of ~35°. When the eyes began deviated in the orbits contralateral to the direction of the ensuing gaze shift, the head contributed less and the eyes more to amplitude-matched gaze shifts. The relative timing of eye and head movements was altered by initial eye position; head latency relative to gaze onset increased as the eyes began in more contralateral initial positions. The direction of the gaze shift also affected the relative amplitudes of eye and head movements; as gaze shifts were made in progressively more vertical directions, eye amplitude increased and head contribution declined systematically. Eye velocity was a saturating function of gaze amplitude for movements without a head contribution (gaze amplitude <20°). As head contribution increased with increasing gaze amplitude (20-60°), peak eye velocity declined by >200°/s and head velocity increased by 100°/s. For constant-amplitude eye movements (~30°), eye velocity declined as the velocity of the concurrent head movement increased. On the basis of these relationships, it is possible to accurately predict gaze amplitude, the amplitudes of the eye and head components of the gaze shift, and gaze, eye, and head velocities, durations and latencies if the two-dimensional displacement of the target and the initial position of the eyes in the orbits are known. These data indicate that signals related to the initial positions of the eyes in the orbits and the direction of the gaze shift influence separate eye and head movement commands. The hypothesis that this divergence of eye and head commands occurs downstream from the superior colliculus is supported by recent electrical stimulation and single-unit recording data.

This article has been cited by other articles:

				S. Rezvani and B. D. Corneil Recruitment of a Head-Turning Synergy by Low-Frequency Activity in the Primate Superior Colliculus J Neurophysiol, July 1, 2008; 100(1): 397 - 411. [Abstract] [Full Text] [PDF]

				M. M. G. Walton, B. Bechara, and N. J. Gandhi Effect of Reversible Inactivation of Superior Colliculus on Head Movements J Neurophysiol, May 1, 2008; 99(5): 2479 - 2495. [Abstract] [Full Text] [PDF]

				E. M. Klier, B. J. M. Hess, and D. E. Angelaki Human Visuospatial Updating After Passive Translations in Three-Dimensional Space J Neurophysiol, April 1, 2008; 99(4): 1799 - 1809. [Abstract] [Full Text] [PDF]

				J. Quinet and L. Goffart Head-Unrestrained Gaze Shifts After Muscimol Injection in the Caudal Fastigial Nucleus of the Monkey J Neurophysiol, December 1, 2007; 98(6): 3269 - 3283. [Abstract] [Full Text] [PDF]

				M. M. G. Walton, B. Bechara, and N. J. Gandhi Role of the Primate Superior Colliculus in the Control of Head Movements J Neurophysiol, October 1, 2007; 98(4): 2022 - 2037. [Abstract] [Full Text] [PDF]

				V. Stuphorn New Functions for an Old Structure: Superior Colliculus and Head-Only Movements. Focus on "The Role of Primate Superior Colliculus in the Control of Head Movements" J Neurophysiol, October 1, 2007; 98(4): 1847 - 1848. [Full Text] [PDF]

				B. Razavi, W. E. O'Neill, and G. D. Paige Auditory Spatial Perception Dynamically Realigns with Changing Eye Position J. Neurosci., September 19, 2007; 27(38): 10249 - 10258. [Abstract] [Full Text] [PDF]

				N. J. Gandhi and D. L. Sparks Dissociation of Eye and Head Components of Gaze Shifts by Stimulation of the Omnipause Neuron Region J Neurophysiol, July 1, 2007; 98(1): 360 - 373. [Abstract] [Full Text] [PDF]

				M. K. McCluskey and K. E. Cullen Eye, Head, and Body Coordination During Large Gaze Shifts in Rhesus Monkeys: Movement Kinematics and the Influence of Posture J Neurophysiol, April 1, 2007; 97(4): 2976 - 2991. [Abstract] [Full Text] [PDF]

				F. Farshadmanesh, E. M. Klier, P. Chang, H. Wang, and J. D. Crawford Three-Dimensional Eye-Head Coordination After Injection of Muscimol Into the Interstitial Nucleus of Cajal (INC) J Neurophysiol, March 1, 2007; 97(3): 2322 - 2338. [Abstract] [Full Text] [PDF]

				M. Prsa and H. L. Galiana Visual-Vestibular Interaction Hypothesis for the Control of Orienting Gaze Shifts by Brain Stem Omnipause Neurons J Neurophysiol, February 1, 2007; 97(2): 1149 - 1162. [Abstract] [Full Text] [PDF]

				T. A. Knight and A. F. Fuchs Contribution of the Frontal Eye Field to Gaze Shifts in the Head-Unrestrained Monkey: Effects of Microstimulation J Neurophysiol, January 1, 2007; 97(1): 618 - 634. [Abstract] [Full Text] [PDF]

				E. M. Klier, H. Wang, and J. D. Crawford Interstitial Nucleus of Cajal Encodes Three-Dimensional Head Orientations in Fick-Like Coordinates J Neurophysiol, January 1, 2007; 97(1): 604 - 617. [Abstract] [Full Text] [PDF]

				B. D. Corneil, D. P. Munoz, and E. Olivier Priming of Head Premotor Circuits During Oculomotor Preparation J Neurophysiol, January 1, 2007; 97(1): 701 - 714. [Abstract] [Full Text] [PDF]

				A. Guillaume and D. Pelisson Kinematics and eye-head coordination of gaze shifts evoked from different sites in the superior colliculus of the cat J. Physiol., December 15, 2006; 577(3): 779 - 794. [Abstract] [Full Text] [PDF]

				P. A. Sylvestre and K. E. Cullen Premotor correlates of integrated feedback control for eye-head gaze shifts. J. Neurosci., May 3, 2006; 26(18): 4922 - 4929. [Abstract] [Full Text] [PDF]

				K. K. Porter, R. R. Metzger, and J. M. Groh Representation of Eye Position in Primate Inferior Colliculus J Neurophysiol, March 1, 2006; 95(3): 1826 - 1842. [Abstract] [Full Text] [PDF]

				A. F. Fuchs, L. Ling, and J. O. Phillips Behavior of the Position Vestibular Pause (PVP) Interneurons of the Vestibuloocular Reflex During Head-Free Gaze Shifts in the Monkey J Neurophysiol, December 1, 2005; 94(6): 4481 - 4490. [Abstract] [Full Text] [PDF]

				R. J. Krauzlis The Control of Voluntary Eye Movements: New Perspectives Neuroscientist, April 1, 2005; 11(2): 124 - 137. [Abstract] [PDF]

				K. E. Cullen, M. Huterer, D. A. Braidwood, and P. A. Sylvestre Time Course of Vestibuloocular Reflex Suppression During Gaze Shifts J Neurophysiol, December 1, 2004; 92(6): 3408 - 3422. [Abstract] [Full Text] [PDF]

				Y. Izawa, H. Suzuki, and Y. Shinoda Suppression of Visually and Memory-Guided Saccades Induced by Electrical Stimulation of the Monkey Frontal Eye Field. II. Suppression of Bilateral Saccades J Neurophysiol, October 1, 2004; 92(4): 2261 - 2273. [Abstract] [Full Text] [PDF]

				A. G. Constantin, H. Wang, and J. D. Crawford Role of Superior Colliculus in Adaptive Eye-Head Coordination During Gaze Shifts J Neurophysiol, October 1, 2004; 92(4): 2168 - 2184. [Abstract] [Full Text] [PDF]

				J. C. Martinez-Trujillo, E. M. Klier, H. Wang, and J. D. Crawford Contribution of Head Movement to Gaze Command Coding in Monkey Frontal Cortex and Superior Colliculus J Neurophysiol, October 1, 2003; 90(4): 2770 - 2776. [Abstract] [Full Text] [PDF]

				J. QUINET and L. GOFFART Influence of Head Restraint on Visually Triggered Saccades in the Rhesus Monkey Ann. N.Y. Acad. Sci., October 1, 2003; 1004(1): 404 - 408. [Full Text] [PDF]

				J. C. Martinez-Trujillo, H. Wang, and J. D. Crawford Electrical Stimulation of the Supplementary Eye Fields in the Head-Free Macaque Evokes Kinematically Normal Gaze Shifts J Neurophysiol, June 1, 2003; 89(6): 2961 - 2974. [Abstract] [Full Text] [PDF]

				B. D. Corneil, E. Olivier, and D. P. Munoz Neck Muscle Responses to Stimulation of Monkey Superior Colliculus. I. Topography and Manipulation of Stimulation Parameters J Neurophysiol, October 1, 2002; 88(4): 1980 - 1999. [Abstract] [Full Text] [PDF]

				B. D. Corneil, E. Olivier, and D. P. Munoz Neck Muscle Responses to Stimulation of Monkey Superior Colliculus. II. Gaze Shift Initiation and Volitional Head Movements J Neurophysiol, October 1, 2002; 88(4): 2000 - 2018. [Abstract] [Full Text] [PDF]

				D. M. WAITZMAN, J. PATHMANATHAN, R. PRESNELL, A. AYERS, and S. DePALMA Contribution of the Superior Colliculus and the Mesencephalic Reticular Formation to Gaze Control Ann. N.Y. Acad. Sci., April 1, 2002; 956(1): 111 - 129. [Abstract] [Full Text] [PDF]

				L. C. POPULIN, D. J. TOLLIN, and J. M. WEINSTEIN Human Gaze Shifts to Acoustic and Visual Targets Ann. N.Y. Acad. Sci., April 1, 2002; 956(1): 468 - 473. [Full Text] [PDF]

				A. S. Dubrovsky and K. E. Cullen Gaze-, Eye-, and Head-Movement Dynamics During Closed- and Open-Loop Gaze Pursuit J Neurophysiol, February 1, 2002; 87(2): 859 - 875. [Abstract] [Full Text] [PDF]

				P. A. Sylvestre, H. L. Galiana, and K. E. Cullen Conjugate and Vergence Oscillations During Saccades and Gaze Shifts: Implications for Integrated Control of Binocular Movement J Neurophysiol, January 1, 2002; 87(1): 257 - 272. [Abstract] [Full Text] [PDF]

				F. J. R. Richmond, K. Singh, and B. D. Corneil Neck Muscles in the Rhesus Monkey. I. Muscle Morphometry and Histochemistry J Neurophysiol, October 1, 2001; 86(4): 1717 - 1728. [Abstract] [Full Text] [PDF]

				B. D. Corneil, E. Olivier, F. J. R. Richmond, G. E. Loeb, and D. P. Munoz Neck Muscles in the Rhesus Monkey. II. Electromyographic Patterns of Activation Underlying Postures and Movements J Neurophysiol, October 1, 2001; 86(4): 1729 - 1749. [Abstract] [Full Text] [PDF]

				C. Maurer, T. Mergner, C. H. Lucking, and W. Becker Adaptive changes of saccadic eye-head coordination resulting from altered head posture in torticollis spasmodicus Brain, February 1, 2001; 124(2): 413 - 426. [Abstract] [Full Text] [PDF]

				N. L. Port, M. A. Sommer, and R. H. Wurtz Multielectrode Evidence for Spreading Activity Across the Superior Colliculus Movement Map J Neurophysiol, July 1, 2000; 84(1): 344 - 357. [Abstract] [Full Text] [PDF]

				M. Ceylan, D. Y. P. Henriques, D. B. Tweed, and J. D. Crawford Task-Dependent Constraints in Motor Control: Pinhole Goggles Make the Head Move Like an Eye J. Neurosci., April 1, 2000; 20(7): 2719 - 2730. [Abstract] [Full Text] [PDF]

				L. Ling, A. F. Fuchs, J. O. Phillips, and E. G. Freedman Apparent Dissociation Between Saccadic Eye Movements and the Firing Patterns of Premotor Neurons and Motoneurons J Neurophysiol, November 1, 1999; 82(5): 2808 - 2811. [Abstract] [Full Text] [PDF]

				B. D. Corneil and D. P. Munoz Human Eye-Head Gaze Shifts in a Distractor Task. II. Reduced Threshold for Initiation of Early Head Movements J Neurophysiol, September 1, 1999; 82(3): 1406 - 1421. [Abstract] [Full Text] [PDF]

				S. D. Newlands, L. Ling, J. O. Phillips, C. Siebold, L. Duckert, and A. F. Fuchs Short- and Long-Term Consequences of Canal Plugging on Gaze Shifts in the Rhesus Monkey. I. Effects on Gaze Stabilization J Neurophysiol, May 1, 1999; 81(5): 2119 - 2130. [Abstract] [Full Text] [PDF]

				J. D. Crawford, M. Z. Ceylan, E. M. Klier, and D. Guitton Three-Dimensional Eye-Head Coordination During Gaze Saccades in the Primate J Neurophysiol, April 1, 1999; 81(4): 1760 - 1782. [Abstract] [Full Text] [PDF]

				J. O. Phillips, L. Ling, and A. F. Fuchs Action of the Brain Stem Saccade Generator During Horizontal Gaze Shifts. I. Discharge Patterns of Omnidirectional Pause Neurons J Neurophysiol, March 1, 1999; 81(3): 1284 - 1295. [Abstract] [Full Text] [PDF]

				M. A. Basso and R. H. Wurtz Modulation of Neuronal Activity in Superior Colliculus by Changes in Target Probability J. Neurosci., September 15, 1998; 18(18): 7519 - 7534. [Abstract] [Full Text] [PDF]

				D. Pelisson, L. Goffart, and A. Guillaume Contribution of the Rostral Fastigial Nucleus to the Control of Orienting Gaze Shifts in the Head-Unrestrained Cat J Neurophysiol, September 1, 1998; 80(3): 1180 - 1196. [Abstract] [Full Text] [PDF]

				L. Goffart, D. Pelisson, and A. Guillaume Orienting Gaze Shifts During Muscimol Inactivation of Caudal Fastigial Nucleus in the Cat. II. Dynamics and Eye-Head Coupling J Neurophysiol, April 1, 1998; 79(4): 1959 - 1976. [Abstract] [Full Text] [PDF]

				K. E. Cullen and D. Guitton Analysis of Primate IBN Spike Trains Using System Identification Techniques. III. Relationship to Motor Error During Head-Fixed Saccades and Head-Free Gaze Shifts J Neurophysiol, December 1, 1997; 78(6): 3307 - 3322. [Abstract] [Full Text] [PDF]

				J. D. Crawford and D. Guitton Primate Head-Free Saccade Generator Implements a Desired (Post-VOR) Eye Position Command by Anticipating Intended Head Motion J Neurophysiol, November 1, 1997; 78(5): 2811 - 2816. [Abstract] [Full Text] [PDF]

				J. O. Phillips, A. F. Fuchs, L. Ling, Y. Iwamoto, and S. Votaw Gain Adaptation of Eye and Head Movement Components of Simian Gaze Shifts J Neurophysiol, November 1, 1997; 78(5): 2817 - 2821. [Abstract] [Full Text] [PDF]

				E. G. Freedman and D. L. Sparks Activity of Cells in the Deeper Layers of the Superior Colliculus of the Rhesus Monkey: Evidence for a Gaze Displacement Command J Neurophysiol, September 1, 1997; 78(3): 1669 - 1690. [Abstract] [Full Text] [PDF]