A Dynamical Moedl of Context Dependencies for the Vestibulo-Ocular Reflex

The vestibulo-ocular reflex (VOR) stabilizes images on the retina during rapid head motions. The gain of the VOR (the ratio of eye to head rotation velocity) is typically around -1 when the eyes are focused on a distant target. However, to stabilize images accurately, the VOR gain must vary with context (eye position, eye vergence and head translation). We first describe a kinematic model of the VOR which relies solely on sensory information available from the semicircular canals (head rotation), the otoliths (head translation), and neural correlates of eye position and vergence angle. We then propose a dynamical model and compare it to the eye velocity responses measured in monkeys. The dynamical model reproduces the observed amplitude and time course of the modulation of the VOR and suggests one way to combine the required neural signals within the cerebellum and the brain stem. It also makes predictions for the responses of neurons to multiple inputs (head rotation and translation, eye position, etc.) in the oculomotor system.

[1]  J. Goldberg,et al.  Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. II. Directional selectivity and force-response relations. , 1976, Journal of neurophysiology.

[2]  D A Robinson,et al.  The use of control systems analysis in the neurophysiology of eye movements. , 1981, Annual review of neuroscience.

[3]  D P Corey,et al.  Analysis of the microphonic potential of the bullfrog's sacculus , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  L. Mays Neural control of vergence eye movements: convergence and divergence neurons in midbrain. , 1984, Journal of neurophysiology.

[5]  J I Simpson,et al.  The selection of reference frames by nature and its investigators. , 1985, Reviews of oculomotor research.

[6]  L E Mays,et al.  Neural control of vergence eye movements: neurons encoding vergence velocity. , 1986, Journal of neurophysiology.

[7]  T Vilis,et al.  A reexamination of the gain of the vestibuloocular reflex. , 1986, Journal of neurophysiology.

[8]  S. Judge,et al.  Neurons in the monkey midbrain with activity related to vergence eye movement and accommodation. , 1986, Journal of neurophysiology.

[9]  D. Robinson,et al.  Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. , 1987, Journal of neurophysiology.

[10]  D Tweed,et al.  Implications of rotational kinematics for the oculomotor system in three dimensions. , 1987, Journal of neurophysiology.

[11]  F. Thorn,et al.  Compensatory eye movements during active head rotation for near targets: effects of imagination, rapid head oscillation and vergence , 1987, Vision Research.

[12]  G. Cheron,et al.  Disabling of the oculomotor neural integrator by kainic acid injections in the prepositus‐vestibular complex of the cat. , 1987, The Journal of physiology.

[13]  B. Peterson,et al.  Dependence of cat vestibulo-ocular reflex direction adaptation on animal orientation during adaptation and rotation in darkness , 1987, Brain Research.

[14]  W. P. Huebner,et al.  Performance of the human vestibuloocular reflex during locomotion. , 1989, Journal of neurophysiology.

[15]  G D Paige,et al.  Eye movement responses to linear head motion in the squirrel monkey. II. Visual-vestibular interactions and kinematic considerations. , 1991, Journal of neurophysiology.

[16]  G. Paige,et al.  Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics. , 1991, Journal of neurophysiology.

[17]  T. Vilis,et al.  Generation of torsional and vertical eye position signals by the interstitial nucleus of Cajal , 1991, Science.

[18]  W. M. King,et al.  Changes in vestibulo-ocular reflex (VOR) anticipate changes in vergence angle in monkey , 1992, Vision Research.

[19]  D. Robinson,et al.  Context-specific adaptation of the gain of the vestibulo-ocular reflex in humans. , 1992, Journal of vestibular research : equilibrium & orientation.

[20]  L. Snyder,et al.  Effect of viewing distance and location of the axis of head rotation on the monkey's vestibuloocular reflex. I. Eye movement responses. , 1992, Journal of neurophysiology.

[21]  D. Zee,et al.  Adaptation of the vestibulo-ocular reflex with the head in different orientations and positions relative to the axis of body rotation. , 1993, Journal of vestibular research : equilibrium & orientation.

[22]  D. Tweed,et al.  Testing models of the oculomotor velocity-to-position transformation. , 1994, Journal of neurophysiology.

[23]  S. Lisberger,et al.  Neural basis for motor learning in the vestibuloocular reflex of primates. II. Changes in the responses of horizontal gaze velocity Purkinje cells in the cerebellar flocculus and ventral paraflocculus. , 1994, Journal of neurophysiology.

[24]  R. Baker,et al.  Cerebellar role in adaptation of the goldfish vestibuloocular reflex. , 1994, Journal of neurophysiology.

[25]  B. Hess,et al.  Inertial representation of angular motion in the vestibular system of rhesus monkeys. II. Otolith-controlled transformation that depends on an intact cerebellar nodulus. , 1995, Journal of neurophysiology.

[26]  Tamar Flash,et al.  The Geometry of Eye Rotations and Listing's Law , 1995, NIPS.