Eye proprioception and visual localization in humans: Influence of ocular dominance and visual context

It has been previously established that the application of low amplitude mechanical vibrations to the inferior rectus muscle of human subjects results in an illusory upward movement of a luminous spot fixated in total darkness, and in a corresponding overshooting of the target when the subject is asked to point to this spot. In the first experiment described here, we compared the effects of applying vibrations to each eye separately and to both eyes simultaneously, under monocular and binocular viewing conditions, in left- and right-eyed subjects. The results confirmed that proprioceptive signals arising from both eyes are involved in egocentric visual localization. A proprioceptive dominance was observed however since vibration of the dominant eye gave rise to larger pointing displacements. In addition, whichever eye was stimulated, the pointing shift induced by vibrating a covered eye was of smaller amplitude than that which occurred when vibrations were applied to the viewing eye. The second experiment showed that both the vibration induced illusions and the pointing shifts disappeared in a structured visual context, which suggests that the processes involved when the target is viewed in darkness might differ from those occurring in structured surroundings.

[1]  Ian P. Howard,et al.  Human visual orientation , 1982 .

[2]  B. Bridgeman,et al.  Relation between cognitive and motor-oriented systems of visual position perception. , 1979, Journal of experimental psychology. Human perception and performance.

[3]  E. Campos,et al.  Abnormal spatial localization in patients with herpes zoster ophthalmicus. Evidence for the presence of proprioceptive information. , 1986, Archives of ophthalmology.

[4]  J. Stevens,et al.  Oculoparalytic illusion: visual-field dependent spatial mislocalizations by humans partially paralyzed with curare. , 1982, Science.

[6]  J. Paillard,et al.  Cognitive Versus Sensorimotor Encoding of Spatial Information , 1987 .

[7]  D. Sparks,et al.  Corollary discharge provides accurate eye position information to the oculomotor system. , 1983, Science.

[8]  L. Stark,et al.  Ocular proprioception and efference copy in registering visual direction , 1991, Vision Research.

[9]  R Lal,et al.  Effect of passive eye position changes on retinogeniculate transmission in the cat. , 1990, Journal of neurophysiology.

[10]  Robert E. Bannon,et al.  SPATIAL SENSE AND MOVEMENTS OF THE EYE , 1948 .

[11]  M. Steinbach.  Proprioceptive knowledge of eye position , 1987, Vision Research.

[12]  I. Donaldson,et al.  Interactions between extraocular proprioceptive and visual signals in the superior colliculus of the cat. , 1980, The Journal of physiology.

[13]  D. Burke,et al.  The responses of human muscle spindle endings to vibration of non‐contracting muscles. , 1976, The Journal of physiology.

[14]  G. Lennerstrand.  Motor and Sensory Functions of Normal and Strabismic Extraocular Muscle , 1988 .

[15]  M J Steinbach,et al.  Spatial localization after strabismus surgery: evidence for inflow. , 1981, Science.

[16]  W. Shebilske,et al.  Induced esophoric shifts in eye convergence and illusory distance in reduced and structured viewing conditions. , 1983, Journal of experimental psychology. Human perception and performance.

[17]  J. Roll,et al.  KINAESTHETIC AND MOTOR EFFECTS OF EXTRAOCULAR MUSCLE VIBRATION IN MAN , 1987 .

[18]  J. C. Kattah,et al.  Monocular rotary nystagmus. , 1983, Journal of clinical neuro-ophthalmology.

[19]  J. A. Graziano,et al.  Effect of context and efference copy on visual straight ahead , 1989, Vision Research.

[20]  Elke U. Weber,et al.  Nonveridical visual direction produced by monocular viewing , 1981 .

[21]  S. Coren,et al.  The dominant eye. , 1976, Psychological bulletin.

[22]  L. Stark,et al.  Role of corollary discharge in space constancy , 1983, Perception & psychophysics.

[23]  J. Vercher,et al.  The role of ocular muscle proprioception in visual localization of targets. , 1990, Science.

[24]  M. Steinbach,et al.  Extraocular Muscle Proprioception and Visual Function: Psychophysical Aspects , 1988 .

[25]  Blake Crider,et al.  A Battery of Tests for the Dominant Eye , 1944 .

[26]  G. L. Walls.  A theory of ocular dominance. , 1951, A.M.A. archives of ophthalmology.

[27]  Otmar Bock,et al.  Visual localization after strabismus surgery is compatible with the “outflow” theory , 1986, Vision Research.

[28]  D. McCloskey,et al.  The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. , 1972, Brain : a journal of neurology.