Single-unit responses to natural vestibular stimuli and eye movements in deep cerebellar nuclei of the alert rhesus monkey

Abstract

To study the possible role of the cerebellum in the vestibular-ocular reflex, extracellular responses of cerebellar nuclear neurons were recorded in awake monkeys during natural vestibular stimulation; 115 neurons in the fastigial nucleus responded to horizontal sinusoidal accelerations applied to the head by means of whole-body rotation. More than 75% of these cells were located in a distinct layer, 500 mum thick, in the rostral part of the fastigial nucleus; they were excited by contralateral horizontal angular acceleration and inhibited by ipsilateral rotation (type IIf neurons). The remaining 25% of the population were scattered more caudally in the nucleus, and were excited by ipsilateral rotation and inhibited by contralateral rotation (type If). All showed fairly high resting discharges, averaging 50 spikes/s. Sinusoidal horizontal rotation (0.2--4.8 HZ) produced clear periodic modulation of the firing rate of fastigial neurons, which was approximately sinusoidal about the resting rate at low frequencies. As the frequency of oscillation (and the applied acceleration) increased, the sinusoidal modulation of unit firing increased in amplitude; at high stimulus frequencies the firing rate was usually driven to zero during the inhibitory part of stimulus cycle, but did not saturate in the excitatory half leading to an increase in the mean firing rate. The maximum firing rates of fastigial neurons were related to the peak acceleration by a power function. At all stimulus frequencies, the peak firing frequency of fastigial neurons lagged the input angular acceleration. Maximum firing of most units occurred just prior to the maximum velocity of the head. The gain and phase lag of the averaged unit discharge relative to head acceleration were calculated by Fourier analysis, using the fundamental as a first approximation of the response. Over a 20-fold stimulus range (0.2--4.0 HZ), mean phage lags of type IIf unit responses with respect to the applied acceleration remained relatively constant; the phase lag at 0.9 HZ measured 62 plus or minus 13 degrees. This phase lag is very similar to that recorded from vestibular nerve fibers (15), suggesting that type IIf fastigial neurons provide an excitatory signal to the ipsilateral vestibular nuclei which is in phase with direct vestibular afferent input, although functionally opposite in sign. Over the same frequency range, the gain decreased at minus- 18 dB/decade. Our data suggests that the majority of fastigial neurons work in parallel with flocculus Purkinje cells to functionally inhibit type Iv neurons in the ipsilateral vestibular nuclei.