ELECTROPHYSIOLOGICAL EVIDENCE FOR A BISYNAPTIC RETINOCEREBELLAR PATHWAY

1. Electrical microstimulation was applied to an in vitro turtle brain preparation while recording extracellular activity from the cerebella r cortex. A visual input to the cerebellum was investigated by measuri ng spike responses evoked by stimulation of drifting visual patterns i maged onto the contralateral retinal eyecup. A vestibular input was as sessed by extracellular field potentials following brief current pulse s through monopolar suction electrodes holding the eighth cranial nerv e (nVIII). 2. The cortical topography of visual and vestibular inputs was first examined. Visual units and vestibular fields show considerab le topographic overlap in the rostrolateral quadrant of the cerebellum . In addition, granule layer units were isolated that responded to cur rent stimulation of nVIII (60-150 muA monopolar). In some cases, spike s occurred at short and fixed latency after each current pulse for sti mulus frequencies of 1 00 Hz. The responses of these units suggest a d irect path between the stimulating and recording electrodes without in tervening synapses. Alternatively, extracellular units were also encou ntered that responded with longer, more variable latencies but only fo r low stimulation frequencies (less-than-or-equal-to 20 Hz). Of the un its that responded to nVIII stimulation, three units also responded to visual stimuli, yet those units all failed to follow high-frequency s timulation of nVIII. This cortical area may then be a site for converg ence of visual and vestibular signals on postsynaptic cells. 3. The ce llular identity of the visual units in the granule layer and the visua l pathways leading there were next investigated. Extracellular spike r esponses were elicited by single current pulses (30-150 muA) to bipola r stimulating electrodes in the basal optic nucleus (BON). Such respon ses were also recorded after a transection of the ventral brain stem a t the level of the cerebellar peduncles to remove pontine and olivary pathways to the cerebellum. Six of these units would also follow high frequency stimulation at fixed short latencies. The localization of th e BON bipolar stimulating electrode could be verified by recording vis ual activity through one pole of the stimulating electrode. Thus it ap pears that at least some of the visually responsive units in the granu le layer are recordings from mossy fibers originating in the BON. 4. T he BON receives direct input from direction-sensitive retinal ganglion cells. From these inputs, the BON derives retinal slip information th at it transmits directly to the cerebellar cortex. These results thus provide electrophysiological evidence of the bisynaptic retinocerebell ar pathway described anatomically by Reiner and Karten in 1978. The pr oximity of nVIII input and this visual input to the cerebellar cortex may be important for visual-vestibular integration necessary for rapid oculomotor reflexes.