FIRING BEHAVIOR OF BRAIN-STEM NEURONS DURING VOLUNTARY CANCELLATION OF THE HORIZONTAL VESTIBULOOCULAR REFLEX .2. EYE-MOVEMENT RELATED NEURONS

1. The single-unit activity of neurons in the vestibular nucleus, the prepositus nucleus, and the abducens nucleus, whose activity was prima rily related to horizontal eye movements, was recorded in alert squirr el monkeys that were trained to track a small visual target by generat ing smooth pursuit eye movements and to cancel their horizontal vestib uloocular reflex (VOR) by fixating a head stationary target. 2. The sp iking behavior of each cell was recorded during 1) spontaneous eye mov ements, 2) horizontal smooth pursuit of a target that was moved sinuso idally +/- 20-degrees/s at 0.5 Hz, 3) horizontal VOR evoked by 0.5-Hz sinusoidal turntable rotations +/- 40-degrees/s (VOR(s)), and 4) volun tary cancellation of the VOR by fixation of a head-stationary target d uring 0.5-Hz sinusoidal turntable rotation at +/- 40-degrees/s (VORC(s )). The responses of most (28/42) of the units were recorded during un predictable 100-ms steps in head acceleration (400-degrees/S2) that we re generated while the monkey was fixating a target light. The acceler ation steps were generated either when the monkey was stationary or wh en the turntable was already rotating (VOR(t) trials), and the monkey was canceling its VOR (VORC(t) trials). 3. The firing behavior of all 12 of the abducens neurons recorded was closely related to horizontal eye position and eye velocity during all of the behavioral paradigms u sed, although there was a small but significant increase in the eye po sition sensitivity of many of these units when the eye was moving (smo oth pursuit) versus when the eye was stationary (fixation). 4. Many ne urons in the prepositus nucleus and the medial vestibular nucleus (n = 15) were similar to abducens neurons, in that their firing rate was r elated primarily to horizontal eye position and eye velocity, regardle ss of the behavioral paradigm used. These cells were, on average, more sensitive to eye position and smooth pursuit eye velocity than were a bducens neurons. 5. The firing rate of 15 other neurons in the preposi tus and medial vestibular nucleus was related primarily to horizontal smooth pursuit eye movements. The tonic firing rate of all of these sm ooth pursuit (SP) cells was related to horizontal eye position, and th e majority generated bursts of spikes during saccades in all direction s but their off direction. Six of the SP neurons fired in phase with i psilateral eye movements, whereas the remaining nine were sensitive to eye movements in the opposite direction. During VORC(s), the firing r ate of SP neurons was modulated in phase with head movements that were in the same direction as their eye movement sensitivity, although the ir depth of modulation was usually much less than their sensitivity to eye velocity during smooth pursuit. The response of SP(s) neurons dur ing the VOR(s) could not be explained in terms of the head and eye mov ement sensitivities estimated during VORC and SP paradigms, respective ly. These data suggested that the responses of SP neurons during VORC. were related to smooth pursuit eye movements rather than to head velo city. 6. When an unpredictable step in head acceleration was generated in their on direction, SP cells did not respond until 80 ms after the step was initiated during both VOR(t) and VORC(t) trials. The latter observation also suggested that the modulation of SP neurons during he ad movements was related to smooth pursuit eye movements, rather than to vestibular nerve activity. 7. We conclude that the firing behavior of abducens neurons during the VOR and VORC can be explained if it is assumed that they receive synaptic inputs from secondary vestibular po sition-vestibular-pause (PVP) neurons, burst tonic neurons, and SP neu rons. We suggest that the premotor inputs related to the nonvisual mec hanism for VORC are carried by PVP and burst tonic neurons, whereas pr emotor inputs related to smooth pursuit mechanism for VORC are carried by SP and burst tonic neurons.