Abstract

The responses of single units in the vestibular nuclei, nucleus praepositus hypoglossi and in the brainstem, deep and posterior to the abducens nucleus, were studied in anaesthetized, paralysed cats. Natural vestibular stimulation was provided by horizontal, sinusoidal oscillation of the animal and extraocular muscle afferents of the ipsilateral eye were activated either by passive eye-movement or by electrical stimulation of the inferior oblique branch of the oculomotor nerve in the orbit. Unit responses to vestibular and/or orbital stimuli were examined in sets of peristimulus time histograms interleaved in time.Of 127 units exposed to both types of stimulus, 40 (32%) responded only to vestibular input; 46 (32%) were affected only by the orbital afferent signal and 19 (15%) received both signals; the remaining 22 units (17%) were discarded because they had polymodal (usually somaesthetic) input. Of the 93 units whose recording sites were determined histologically, 24 were in the medial vestibular nucleus, 16 in the n. praepositus hypoglossi and 45 in the magnocellular nucleus of the reticular formation posterior and deep to the abducens nucleus. In these three nuclei 19 units in total were found which carried the orbital proprioceptive afferent signal and also responded to horizontal vestibular stimulation. The input from the eye muscles proved able to modify the vestibular response by adding excitation or inhibition or both. Effects of the orbital signal were generally phasic. About half of the units which responded to passive eye-movement showed statistically significant differences between their responses to horizontal and to vertical eye-movement.We have shown previously that signals from extraocular muscle proprioceptors reach the vestibulooculomotor system in an amphibian and a bony fish; the present experiments show that this is the case in a mammal also. The fact that the visual and visuomotor behaviour of these three species is very different suggests that the proprioceptive signal may play some rather fundamental role in the vestibulo-ocular system.The principal interest of the present results is that they demonstrate that units in the central vestibular system of the cat, in structures which are known to be concerned in oculomotor control, and particularly in the organization of horizontal eye-movement, receive an afferent signal from the eye muscles during passive eye-movement. These brainstem nuclei are known to receive various combinations of input from the vestibular and visual systems and of signals which represent neck movement and eye position and velocity. The latter signals are generally attributed to a “corollary discharge” and it has been suggested that this signal may be elaborated in the n. praepositus hypoglossi. Our results give no information on this putative “corollary discharge” but they do show that these parts of the vestibulo-oculomotor system also receive a proprioceptive signal which should be present during at least some natural eye-movements.Thus, we believe that the results in this paper add weight to the hypothesis that a proprioceptive signal from receptors in the extrinsic ocular muscles is likely to play a part in the control of eye-movement by the vestibulo-ocular system.

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