1. Vestibular and prepositus hypoglossi (PH) neurones projecting to the abducens (ABD) nucleus were recorded in the alert cat. Their discharge characteristics were analysed to ascertain the origin of the horizontal eye position signal present in ABD neurones. 2. Neurones were classified according to: their location with respect to the ABD nucleus; their antidromic activation from the ABD nucleus; the synaptic field potential they induced in the ABD nucleus with the spike-triggered averaging technique; and their activity during spontaneous and vestibularly induced eye movements. 3. Vestibular neurones projecting to the ABD nucleus were located in the rostral medial vestibular nucleus. They were excitatory on the contralateral and inhibitory on the ipsilateral ABD neurones. Both types of premotor vestibular neurone showed a firing rate weakly related to eye position, increasing for eye fixations in the contralateral on-direction, and decreasing with ipsilateral fixation. Position sensitivity during eye fixations was (means +/- S.D.) 1.8 +/- 0.9 spikes s-1 deg-1 for excitatory neurones and 2.2 +/- 1.3 spikes s-1 deg-1 for inhibitory neurones, Firing rate exhibited a high variability during eye fixations. Their responses during saccades in the off-direction were characterized by a pause that, although less defined, was occasionally present during saccades in the on-direction. Eve velocity sensitivity during spontaneous saccades in the on-direction was 0.17 +/- 6.15 spikes s-1 deg-1 s-1 for excitatory neurones and 0.15 +/- 0.07 spikes s-1 deg-1 s-1 for inhibitory vestibular neurones. During sinusoidal head stimulation at 0.2 Hz, vestibular neurones showed a type 1 discharge rate with a phase lead over eye position of 86.0 +/- 14.1 deg for excitatory and 80.2 +/- 12.5 deg for inhibitory neurones. Position sensitivity during vestibular stimulation did not differ significantly from values obtained for spontaneous eye movements. However. the velocity sensitivity of premotor vestibular neurones during head rotation was significantly higher (1.6 +/- 0.2 spikes s-1 deg-1 s-1 for excitatory and 1.5 +/- 0.3 spikes s-1 deg-1 s-1 for inhibitory neurones) than during spontaneous eve movements. 4. PH neurones projecting to the ABD nucleus were located in the rostral one-third third of the nucleus. These neurones were excitatory on the ipsilateral and inhibitory on the contralateral ABD nucleus. Their firing rates were correlated mainly with eye position, increasing for abducting eye positions of the ipsilateral eye and decreasing with adduction movements. Eye position sensitivities were 8.2 +/- 2.9 and 7.9 +/- 2.9 spikes s-1 deg-1 for excitatory and inhibitory neurones, respectively. Variability of the firing rate during eye fixations was lower than that shown by promoter vestibular neurones. During saccades, premotor PH neurones showed low eye velocity sensitivity (0.15 +/- 0.21 for the excitatory and 0.32 +/- 0.28 spikes s-1 deg-1 s-1 for the inhibitory group) with low coefficients of correlation. During vestibular sinusoidal stimulation these neurones were type II and showed phase leads of 11.3 +/- 4.1 and 13.0 +/- 4.5 deg, respectively at 0.2 Hz. Eve position sensitivity during vestibular sinusoidal stimulation was similar to that shown during spontaneous eye movements. Their velocity sensitivities during vestibular stimulation were 1.0 +/- 0.7 and 0.8 +/- 0.3 spikes s-1 dec-1 s-1 for excitatory and inhibitory neurones, respectively. 5. It is proposed that the PH nucleus is responsible for the generation of the eve position signal present in ABD motoneurones and internuclear neurones. Furthermore. the weak position signal present in vestibular neurones is probably the result of a corollary discharge not directly related to eye position signal generation. A suggestion of how eve position signal is generated in the PH nucleus is also presented.
