The firing behavior of 51 non-eye movement related central vestibular neurons that were sensitive to passive head rotation in the plane of the horizontal semicircular canal was studied in three squirrel monkeys whose heads were free to move in the horizontal plane. Unit sensitivity to active head movements during spontaneous gaze saccades was compared with sensitivity to passive head rotation. Most units (29/35 tested) were activated at monosynaptic latencies following electrical stimulation of the ipsilateral vestibular nerve. Nine were vestibulo-spinal units that were antidromically activated following electrical stimulation of the ventromedial funiculi of the spinal cord at C1. All of the units were less sensitive to active head movements than to passive whole body rotation. In the majority of cells (37/51, 73%), including all nine identified vestibulo-spinal units, the vestibular signals related to active head movements were canceled. The remaining units (n = 14, 27%) were sensitive to active head movements, but their responses were attenuated by 20-75%. Most units were nearly as sensitive to passive head-on-trunk rotation as they were to whole body rotation; this suggests that vestibular signals related to active head movements were cancelled primarily by subtraction of a head movement efference copy signal. The sensitivity of most units to passive whole body rotation was unchanged during gaze saccades. A fundamental feature of sensory processing is the ability to distinguish between self-generated and externally induced sensory events. Our observations suggest that the distinction is made at an early stage of processing in the vestibular system.

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Maintaining balance after an external perturbation requires modification of ongoing motor plans and the selection of contextually appropriate muscle activation patterns that respect body and limb position. We have used the vestibular system to generate sensory-evoked transitions in motor programming. In the face of a rapid balance perturbation, the lateral vestibular nucleus (LVN) generates exclusive extensor muscle activation and selective early extension of the hindlimb, followed by the co-activation of extensor and flexor muscle groups. The temporal separation in EMG response to balance perturbation reflects two distinct cell types within the LVN that generate different phases of this motor program. Initially, an LVN population directs an extension movement that reflects connections with extensor, but not flexor, motor neurons. A distinct LVN population initiates muscle co-activation via the pontine reticular nucleus. Thus, distinct circuits within the LVN generate different elements of a motor program involved in the maintenance of balance.

A series of studies were carried out to investigate the role of the cerebellar flocculus and ventral paraflocculus in the ability to voluntarily cancel the vestibuloocular reflex (VOR). Squirrel monkeys were trained to pursue moving visual targets and to fixate a head stationary or earth stationary target during passive whole body rotation (WBR). The firing behavior of 187 horizontal eye movement-related Purkinje (Pk) cells in the flocculus region was recorded during smooth pursuit eye movements and during WBR. Half of the Pk cells encountered were eye velocity Pk cells whose firing rates were related to eye movements during smooth pursuit and WBR. Their sensitivity to eye velocity during WBR was reduced when a visual target was not present, and their response to unpredictable steps in WBR was delayed by 80-100 ms, which suggests that eye movement sensitivity depended on visual feedback. They were insensitive to WBR when the VOR was canceled. The other half of the Purkinje cells encountered were sensitive to eye velocity during pursuit and to head velocity during VOR cancellation. They resembled the gaze velocity Pk cells previously described in rhesus monkeys. The head velocity signal tended to be less than half as large as the eye velocity-related signal and was observable at a short ( approximately 40 ms) latency when the head was unpredictably accelerated during ongoing VOR cancellation. Gaze and eye velocity type Pk cells were found to be intermixed throughout the ventral paraflocculus and flocculus. Most gaze velocity Pk cells (76%) were sensitive to ipsilateral eye and head velocity, but nearly half (48%) of the eye velocity Pk cells were sensitive to contralateral eye velocity. Thus the output of flocculus region is modified in two ways during cancellation of the VOR. Signals related to both ipsilateral and contralateral eye velocity are removed, and in approximately half of the cells a relatively weak head velocity signal is added. Unilateral injections of muscimol into the flocculus region had little effect on the gain of the VOR evoked either in the presence or absence of visual targets. However, ocular pursuit velocity and the ability to suppress the VOR by fixating a head stationary target were reduced by approximately 50%. These observations suggest that the flocculus region is an essential part of the neural substrate for both visual feedback-dependent and nonvisual mechanisms for canceling the VOR during passive head movements.