Brain Research, 102 (1976) 181-184 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands

181

Somatosensory representation in the vestibulocerebellum

DIETRICH W. F. SCHWARZ AND A. CRAIG MILNE Departments of Otolaryngology and Physiology, University of Toronto, Toronto (Canada)

(Accepted October 8th, 1975)

A prominent somatosensory input has been documented for the vestibular nucleia0,~3, v~. The spinal afferents originate from the spinocerebellar system and, to a smaller extent, from the anterolateral funiculi (spinothalamic tract)7,12. Modalities represented are proprioception from joint 10, and muscle 13 receptors for those nuclei under the influence of the uvula and nodulus (descending and medial nucleus) 1. Neurons receiving proprioceptive in addition to vestibular input have been shown to project to the spinal cord 14, presumably participating in vestibulomotor regulation. If the role of the cerebellum in this extremely short neuron circuit for vestibulomotor control is to be understood, knowledge about somatosensory representation in the vestibulocerebellum 4 is a prerequisite. Uvula and nodulus were investigated with glass micropipettes penetrating the posterior lobe vermis at an angle of 30° posteriorly (Fig. IA). Recordings of field potentials and unit activity were obtained under N20 analgesia and gallamine triethiodide paralysis after surgical halothane anesthesia was discontinued. Bipolar electrodes were implanted to sciatic nerves, common radial nerves and nerves supplying the splenius muscles in the neck, as well as onto the anterior branches of the vestibular nerves bilaterally, for electrical stimulation. A stroboscopic flash presented in a dimly lit room provided visual stimulation which was ineffective for all units with somatosensory input described here. Field potentials in response to these stimuli were averaged, usually for 32 stimulus presentations, and unit responses were displayed as poststimulus time histograms for 64 or 128 presentations. Receptive fields were mapped manually. The location of the electrode tip in the vermal vestibulocerebellum could be recognized by the presence of a typical short latency vestibular field potential. Laminar field analysis revealed that a single shock mossy fiber (MF) excitation caused the greater portion of these potential shifts 9. This indicates that primary vestibular MF afferents are largely responsible for this response. Latencies were, as originally reported 6, 4-5 msec for the N2 potential 9, being fractions of a millisecond shorter ipsilaterally than for the midline or contralateral side of the vermis. Histological examination of specimens with electrodes remaining in situ verified that these potentials could be

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Fig. 1. Converging vestibular and somatosensory input in the lateral uvula. A: a typical electrode track. Field potentials in B are recorded at locations a, b and c. B : averagedfield potentials in molecular (a) and granular (c) layers in response to vestibular and contralateral neck nerve stimulation. C: amplitudes of the N2 potentials in response to a neck nerve stimulus conditioned by a vestibular nerve stimulus (open circles) and vice verszl (crosses). See text for details.

recorded only in uvula and nodulus; more superficial folia of Iobules V I I - V I I i occasionally yielded smaller vestibular field potentials with longer latencies. Within the lateral portion of the uvula field potentials characteristic for a mossy fiber input were also recorded following neck and limb nerve stimuli. The electrode track of Fig. 1A is directed to this region. Transition from molecular (Fig. 1B, a) to granular (Fig. IB, c) layer exhibits similar laminar field patterns for both vestibular and neck nerve impulses at identical microelectrode positions. When one of these two stimuli followed the other, at intervals ranging from 10 to 50 msec, interaction patterns for the N2 waves were observed, as shown in Fig. 1C. Apparently neck afferents suppress granule and/or Golgi cell activation s by vestibular afferents for more than 50 msec, whereas a vestibular impulse is able to enhance the activity of such cells in response to neck afferent input after a brief initial period of suppression lasting about 15 msec. A variety of such interaction patterns was observed indicating that vestibular and somatosensory inputs share common neuron groups within the cerebellar cortex. This was shown to be true by means of unitary recordings. Virtually all cells (57 studied thus far) in the lateral uvula responded to stimulation of at least one nerve apart from the vestibular nerves. A somatotopic organization could not be demonstrated; usually a combination of afferents from different body portions converges onto a cell, such as observed at other stations of the central vestibular systemt°,H,~ L The Purkinje cell, illustrated in Fig. 2, responds to stimulation of neck, forelimb (FL) and hindlimb (HL) nerves, in addition to both vestibular nerves (VN). The strongest vestibular activation originated from the left labyrinth, ipsilateral to the recording electrode, whereas the greater somatosensory responses originated from the contra-

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