Passive activation of neck proprioceptive inputs does not influence the discharge patterns of vestibular nuclei neurons.

Position-vestibular-pause (PVP) neurons and vestibular only (VO) neurons are thought to mediate the vestibulo-ocular and vestibulo-collic reflexes, respectively. Both neuron classes are much less sensitive to head motion during active gaze shifts than during passive whole-body rotation (pWBR).1–5 The mechanism that underlies this differential processing of vestibular information is not known. Neck muscle proprioceptive inputs have been proposed to contribute to the observed attenuation. While experiments in decerebrate animals have shown that neck proprioception can modulate the responses of vestibular neurons,6,7 studies in alert monkeys have reported varying degrees of influence.3,8–10 However, these latter studies assumed that the monkey did not generate a neck motor command during the paradigms used to evaluate neck proprioceptive inputs. Since a coincident neck efference command could effect neuron discharges, in this study we measured the torque produced during passive rotation of the body relative to a stationary head, thereby allowing us to dissociate the effect of neck proprioception from efference commands. The discharge activity of vestibular neurons in three rhesus monkeys was initially recorded during voluntary eye movements and pWBR with the monkeys in the headrestrained condition. After a neuron was fully characterized, the monkey’s head was slowly and carefully released, allowing free rotation of its head through its natural range of motion. The response of the same neuron was then recorded during the voluntary head movements made during combined eye-head gaze shifts (15° to 65°). In agreement with previous studies, the head velocity sensitivities of PVP (n = 17) and VO (n = 40) neurons were significantly attenuated during gaze shifts as compared to those estimated during pWBR (mean sensitivity (± SEM) = 0.37± 0.17 vs. 1.31± 0.13 (spk/s)/(deg/s), and 0.17± 0.03 vs. 0.53± 0.04 (spk/s)/(deg/s), for PVP and VO neurons, respectively; FIG. 1E and F, compare white and gray-shaded columns). The influence of neck proprioceptive inputs on vestibular neurons was first tested by passively rotating the monkeys’ bodies while their heads were held earth-station-