Our results demonstrate that the primate vestibular system can distinguish vestibular signals that arise from active self-motion of the head on the body, early in processing, at the level of the vestibular nuclei. This finding supports the proposal of von Holst and Mittelstaedt (1950) who suggested that afferent signals aris ing from an animal's own behaviour could be distinguished from afferent signals generated by external sources. They proposed that a copy of the motor command (i.e., a motor efference) is combined with the afferent signal to selectively remove the component caused by the motor behaviour. A similar mechanism has been reported in the electric fish, where an efference copy of the command to activate the electric organ converges centrally with electroreceptor afferent information, thereby reducing the response to self-generated electric fields (Bell, 1981; Zipser and Bennett, 1976).
Two important questions that arise from our studies of active head-on-body motion are: Do the vestibular nuclei lose track of vestibular information during active gaze shifts and gaze pursuit? And if they do, are we effectively operating as if we have a significant bilateral loss of labyrinth function during these self-generated behaviours? We addressed these points by utilizing a paradigm in which the monkey was able to generate voluntary head movements on its body (Figure 16.6a, dashed arrow in cartoon) while undergoing passive whole-body rotation (Figure 16.6a, solid arrow in cartoon). In this paradigm, head-in-space velocity is the sum of passive whole-body velocity and the voluntarily generated head-on-body velocity. Recall that VO neuron responses to the component of head-in-space motion arising from the monkey's voluntary head-on-body movements were relatively weak or negligible (Figure 16.6a). Yet, remarkably, neurons continued to respond robustly to the component of head-in-space motion produced by the passive rotation of the body. A summary of the population response is shown in Figure 16.9a. In contrast, when we tested PVP neurons during the same paradigm, their responses to both active and passive components of head-in-space motion were significantly reduced during combined eye-head gaze shifts. A summary of the population responses are shown in Figure 16.9b. Thus, during combined eye-head gaze shifts neither cell group reliably encoded the monkey's head-in-space motion (compare black and white bars, Figure 16.9). A similar trend was observed during gaze pursuit (not shown). Previous work in head-restrained animals has shown that passive horizontal head rotations are predominantly encoded at the level of the vestibular nuclei in the modulation of these two classes of neurons. However, since we have shown that neither cell type faithfully encodes head in space velocity under all conditions (Figure 16.10, pathway A), it appears that the vestibular nuclei actually do lose track of vestibular information that results from voluntary head motion during active gaze shifts and gaze pursuit.
The combined results of our studies of VO and PVP neuron discharges during active head-on-body motion also lead to a third important question: Does the brain have access to reliable vestibular sensory information during active gaze shifts and gaze pursuit via some route independent of the vestibular nuclei? Vestibular afferents project strongly to cerebellar regions involved in vestibular and eye movement control, namely, the nodulus/uvula, the flocullus, and the fastigial nucleus (reviewed in Voogd et al., 1996), as well as diffusely to other regions of the vestibulocerebellar vermis (Kotchabkakdi and Walberg, 1978). A reliable estimate of head-in-space motion may be encoded by these pathways during voluntary gaze shifts and gaze pursuit (Figure 16.10, pathway B). The projection to the
A. VO neurons
Was this article helpful?