Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex. I. Secondary vestibular neurons

1. The single-unit activity of vestibular neurons was recorded in alert squirrel monkeys. The monkeys had been trained to track a small visual target by generating smooth pursuit eye movements and to cancel their vestibuloocular reflex (VOR) by fixating a head stationary target. The monkeys were seated on a vestibular turntable, and their heads were held in the plane of the horizontal semicircular canals. The responses of 45 type I vestibular neurons whose activity was related to ipsilateral horizontal head movements were recorded. In 19 of 30 cells tested, electrical stimulation (0.1-ms monophasic pulses, ≤800 μA) of the ipsilateral vestibular nerve evoked a spike at a monosynaptic latency (0.7-1.3 ms). 2. The spiking behavior of each cell was recorded during several behavioral paradigms: 1) spontaneous eye movements, 2) horizontal smooth pursuit of a target that was moved sinusoidally ±20°/s at 0.5 Hz, 3) horizontal VOR during 0.5-Hz sinusoidal turntable rotations ± 40°/s (VOR(s)), and 4) voluntary cancellation of the sinusoidal VOR by fixation of a head-stationary target during 0.5-Hz sinusoidal turntable rotation at ±40°/s in the light (VORC(s)). 3. The response of most (34) of the units was recorded during unpredictable 100-ms steps in head acceleration (400°/s²) that were generated while the monkey was fixating a target light. The acceleration steps were generated either when the monkey was stationary (VOR(t) paradigm) or when the turntable was already rotating, and the monkey was canceling its VOR (VORC(t) paradigm). Smaller eye movements were evoked when the acceleration step was generated during VOR cancellation. 4. Type I vestibular units were grouped into two classes on the basis of the relationship of their firing rate to eye movements. The discharge rate of 20 'pure vestibular' units was not clearly related to eye movements. The remaining 25 units were classified as position-vestibular-pause (PVP) neurons. PVP neurons increased their firing rate during contralateral eye movements and during ipsilateral turntable rotations, and paused during saccadic eye movements. 5. Most (17/20) pure vestibular neurons generated the same response to vestibular stimuli when the monkeys canceled their VOR as they did during the VOR in both the sinusoidal and acceleration step paradigms. 6. The head velocity sensitivity of most (19/24) PVP neurons was reduced by 20-60% during VORC(s), compared with their response during the VOR(s). The PVP neurons whose sensitivity of head movements was reduced during VORC(s) also exhibited a reduced vestibular sensitivity during VORC(t). The reduction in sensitivity during VORC₁ was apparent at a short latency (<30 ms) after the initiation of the head acceleration step. On the other hand, the earliest change in firing rate that could be observed when the target was accelerated instead of the turntable was ≃80 ms, which suggests that visual signals were not responsible for the reduction in head movement sensitivity. The response of PVPs during VORC(t) could be modeled by subtracting a low-pass filtered head velocity signal with a gain of 0.5 from their VOR(t) response. 7. The reduction in vestibular sensitivity of PVPs was positively but poorly correlated with the smooth pursuit eye velocity sensitivity in individual units. In fact, several of the cells that showed a reduction in vestibular sensitivity during VORC(s) and VORC(t) were not sensitive to eye velocity during smooth pursuit. Thus it is unlikely that their reduced vestibular sensitivity during VOR cancellation was solely due to eye movement-related inputs. 8. Because previous studies have shown that PVP neurons are secondary vestibular neurons that project to extraocular motor neurons and presumably mediate the vestibuloocular reflex, it is likely that the reduction in head movement sensitivity observed in these cells during VORC contributes to their ability to voluntarily cancel their VOR. We suggest that the reduction in the head movement sensitivity of secondary vestibuloocular reflex pathways is part of a nonvisual mechanism that can be utilized to voluntarily suppress the VOR.