Inputs from the ipsilateral and contralateral vestibular apparatus to behaviorally characterized abducens neurons in rhesus monkeys

Abstract

1. We made extracellular recordings from neurons in the abducens nuclei of alert rhesus monkeys during electrical stimulation of the vestibular labyrinths with brief current pulses and during smooth pursuit, steady fixation, and the vestibuloocular reflex (VOR) evoked by passive head turns. The responses to electrical stimuli were compared with quantitative measures of the sensitivity of each neuron to eye position and eye velocity. We also compared the strengths of the vestibular inputs from the labyrinths ipsilateral and contralateral to the side of recording. 2. Abducens neurons showed transient excitation after a current pulse was applied to the contralateral labyrinth and transient inhibition after stimulation of the ipsilateral labyrinth. The latency of excitation had a mean value of 1.7 ms and a median value of 1.5 ms. Latency was unimodally distributed with little variation among neurons. Neurons with large responses showed a second phase of excitation that started 2.5 ms after the stimulus. 3. In two of three monkeys, the excitatory responses of abducens neurons to electrical stimulation of the contralateral labyrinth were approximately 3 times as large as their inhibitory responses to stimulation of the ipsilateral labyrinth. The difference in response size was not observed in the third monkey. The asymmetry in the size of the electrically evoked inputs from the two labyrinths was associated with a smaller asymmetry in responses of abducens neurons during the VOR evoked by passive head turns. The increase in firing rate during head rotation away from the side of the recording was almost always larger than the decrease in firing rate during head rotation toward the side of the recording. 4. The size of the neuronal response to electrical stimulation was correlated with the magnitude of the change in discharge rate during eye movements. Single or multiple regression of measures of response amplitude against eye position threshold, sensitivity to eye position, sensitivity to eye velocity, and baseline discharge rate yielded correlation coefficients that ranged from 0.26 to 0.92 in different monkeys. The existence of positive correlations is consistent with a role of the intrinsic properties of abducens neurons in determining recruitment order. However, the existence of large amounts of variability within most of the samples suggests that the recruitment order of abducens neurons also depends on the discharge properties of the afferents to each abducens neuron.