Three-dimensional human eye movements are organized differently for the different oculomotor subsystems

Three-dimensional (3-D) eye movements during steady fixation, saccades and smooth pursuit are governed by a powerful strategy restricting eye position to 2 degrees of freedom by keeping the torsional component close to o (Listing's law). To test if Listing's law is also obeyed during optokinetic and vestibular stimulation, the study compares 3-D eye movements in humans during pursuit, optokinetic and vestibular activation using similar gaze trajectories. The optokinetic and vestibuloocular reflexes deviate from Listing's law showing a strategy lying about halfway between optimal full-field retinal image stabilization and Listing's law. The fact that for similar gaze trajectories the brain can choose between different 3-D movement strategies depending on the oculomotor subsystem currently in action (supposedly to optimize for the specific requirements of a particular oculomotor subsystem) suggests that Listing's law is due to a neurally-im-posed constraint on the oculomotor output.

[1]  T. Vilis,et al.  How do Motor Systems Deal with the Problems of Controlling Three-Dimensional Rotations? , 1995 .

[2]  T Vilis,et al.  Symmetry of oculomotor burst neuron coordinates about Listing's plane. , 1992, Journal of neurophysiology.

[3]  J. Dichgans,et al.  Three-dimensional properties of human pursuit eye movements , 1992, Vision Research.

[4]  T Haslwanter,et al.  Three‐Dimensional Transformations from Vestibular and Visual Input to Oculomotor Output a , 1992, Annals of the New York Academy of Sciences.

[5]  D. Tweed,et al.  Multidimensional Descriptions of the Optokinetic and Vestibuloocular Reflexes , 1992, Annals of the New York Academy of Sciences.

[6]  K. Fukushima,et al.  Involvement of the Interstitial Nucleus of Cajal in the Midbrain Reticular Formation in the Position-Related, Tonic Component of Vertical Eye Movement and Head Posture , 1992 .

[7]  Alain Berthoz,et al.  The Head-neck sensory motor system , 1992 .

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

[9]  K Hepp,et al.  Two- rather than three-dimensional representation of saccades in monkey superior colliculus. , 1991, Science.

[10]  T Vilis,et al.  Axes of eye rotation and Listing's law during rotations of the head. , 1991, Journal of neurophysiology.

[11]  T. Vilis,et al.  Geometric relations of eye position and velocity vectors during saccades , 1990, Vision Research.

[12]  T. Vilis,et al.  Computing three-dimensional eye position quaternions and eye velocity from search coil signals , 1990, Vision Research.

[13]  T Vilis,et al.  Rapid eye movement generation in the primate. Physiology, pathophysiology, and clinical implications. , 1989, Revue neurologique.

[14]  H. Collewijn,et al.  Human gaze stability in the horizontal, vertical and torsional direction during voluntary head movements, evaluated with a three-dimensional scleral induction coil technique , 1987, Vision Research.

[15]  H. Collewijn,et al.  A direct test of Listing's law—II. Human ocular torsion measured under dynamic conditions , 1987, Vision Research.

[16]  H. Collewijn,et al.  A direct test of Listing's law—I. Human ocular torsion measured in static tertiary positions , 1987, Vision Research.

[17]  A. Fuchs,et al.  Reticular control of vertical saccadic eye movements by mesencephalic burst neurons. , 1979, Journal of neurophysiology.

[18]  V. Henn,et al.  Vertical eye movement related unit activity in the rostral mesencephalic reticular formation of the alert monkey , 1977, Brain Research.

[19]  P. Bach-y-Rita,et al.  Basic Mechanisms of Ocular Motility and Their Clinical Implications , 1976 .

[20]  Ken Nakayama,et al.  Coordination of extraocular muscles , 1975 .