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 cerebellar cortex. A visual input to the cerebellum was investigated by measuring spike responses evoked by stimulation of drifting visual patterns imaged onto the contralateral retinal eyecup. A vestibular input was assessed by extracellular field potentials following brief current pulses through monopolar suction electrodes holding the eighth cranial nerve (nVIII). 2. The cortical topography of visual and vestibular inputs was first examined. Visual units and vestibular fields show considerable topographic overlap in the rostrolateral quadrant of the cerebellum. In addition, granule layer units were isolated that responded to current stimulation of nVIII (60-150 muA monopolar). In some cases, spikes occurred at short and fixed latency after each current pulse for stimulus frequencies of 1 00 Hz. The responses of these units suggest a direct path between the stimulating and recording electrodes without intervening synapses. Alternatively, extracellular units were also encountered that responded with longer, more variable latencies but only for low stimulation frequencies (less-than-or-equal-to 20 Hz). Of the units that responded to nVIII stimulation, three units also responded to visual stimuli, yet those units all failed to follow high-frequency stimulation of nVIII. This cortical area may then be a site for convergence of visual and vestibular signals on postsynaptic cells. 3. The cellular identity of the visual units in the granule layer and the visual pathways leading there were next investigated. Extracellular spike responses were elicited by single current pulses (30-150 muA) to bipolar stimulating electrodes in the basal optic nucleus (BON). Such responses were also recorded after a transection of the ventral brain stem at 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 the BON bipolar stimulating electrode could be verified by recording visual activity through one pole of the stimulating electrode. Thus it appears that at least some of the visually responsive units in the granule layer are recordings from mossy fibers originating in the BON. 4. The BON receives direct input from direction-sensitive retinal ganglion cells. From these inputs, the BON derives retinal slip information that it transmits directly to the cerebellar cortex. These results thus provide electrophysiological evidence of the bisynaptic retinocerebellar pathway described anatomically by Reiner and Karten in 1978. The proximity of nVIII input and this visual input to the cerebellar cortex may be important for visual-vestibular integration necessary for rapid oculomotor reflexes.