Journal of Neurophysiology, Vol 62, Issue 6 1360-1374, Copyright © 1989 by APS

ARTICLES

Does an extraocular proprioceptive signal reach the superior colliculus?

J. S. Nelson, M. A. Meredith and B. E. Stein
Neurobiology Research Center, University of Alabama, Birmingham 35294.

1. The primary functions of the superior colliculus (SC) are thought to include both the spatial localization of sensory stimuli and the initiation of an orienting response. It has been hypothesized that, in cat, both of these SC functions may be influenced by feedback from the extraocular muscles. The present investigation was initiated to determine which SC cells receive this extraocular muscle feedback and how this feedback influences the discharge properties of SC cells and their ability to integrate input from other sensory modalities. These questions were addressed in cats prepared with various anesthetic agents. 2. During the course of these experiments it became apparent that responses of SC cells to extraocular muscle stimulation could be elicited only under very specific conditions, and these observations questioned the existence of functional extraocular inputs to SC cells. 3. Rotating the eye or stretching the extraocular muscles was never found to be effective in activating SC cells unless the drug chloralose was used in the experimental preparation. In these chloralose-anesthetized animals, responses to eye rotation or muscle stretch were long and variable in latency, the discharge did not reflect the metrics of the stimulus, and the velocity and amplitude thresholds of these cells usually exceeded the cat's oculomotor range. Responses usually consisted of one to three impulses and, in appropriate conditions, could be inhibited by responses to visual or auditory stimuli. 4. The origin of this SC response to eye rotation/extraocular-muscle stretch could not be localized to the extraocular muscles. Responses to passive stretch of extraocular muscles were not eliminated by anesthetizing the muscles with injections of lidocaine. Active contraction of the extraocular muscles induced by electrical stimulation of the oculomotor nerve was never observed to evoke SC responses. Furthermore, transection of the muscle nerves, which isolated the extraocular-muscle receptors from the CNS, did not affect the response initiated by stretching the extraocular muscles. However, in the absence of intact muscle nerves, pulling the periorbital tissue elicited responses very much like those produced by stretching the muscles in the intact preparation, suggesting the periorbita as the source of responses in intact preparations as well. 5. These data are not consistent with the hypothesis that feedback from extraocular-muscle receptors influences the activity of SC cells.

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