Dissociating Self-Generated from Passively Applied Head Motion: Neural Mechanisms in the Vestibular Nuclei

Abstract

The ability to distinguish sensory inputs that are a consequence of our own actions from those that result from changes in the external world is essential for perceptual stability and accurate motor control. To accomplish this, it has been proposed that an internal prediction of the consequences of our actions is compared with the actual sensory input to cancel the resultant self-generated activation. Here, we provide evidence for this hypothesis at an early stage of processing in the vestibular system. Previous studies have shown that neurons in the vestibular nucleus, which receive direct inputs from vestibular afferent fibers, are responsive to passively applied head movements. However, these same neurons do not reliably encode head velocity resulting from self-generated movements of the head on the body. In this study, we examined the mechanism that underlies the selective elimination of vestibular sensitivity to active head-on-body rotations. Individual neurons were recorded in monkeys making active head movements. The correspondence between intended and actual head movement was experimentally controlled. We found that a cancellation signal was gated into the vestibular nuclei only in conditions in which the activation of neckproprioceptorsmatchedthatexpectedonthebasisoftheneckmotorcommand.Thisfindingsuggeststhatvestibularsignalsthatarisefrom self-generated head movements are inhibited by a mechanism that compares the internal prediction of the sensory consequences by the brain to the actual resultant sensory feedback. Because self-generated vestibular inputs are selectively cancelled early in processing, we propose that this gating is important for the computation of spatial orientation and control of posture by higher-order structures.

The thalamocortical vestibular system in animals and humans

“…At the level of vestibular nuclei neurons, electrophysiological recordings in monkeys revealed strongly modulated (decreased) responses during active and voluntary head movements as compared to passive head movements, although primary vestibular afferents reliably code for active head movements (Angelaki and Cullen, 2008;Cullen et al, 2003;McCrea et al, 1999;Roy and Cullen, 2004). These observations indicated that such vestibular nuclei signals are strongly modulated depending on the context of the movement and that efference copy signals can cancel the response of vestibular nuclei neurons during active motion (Angelaki and Cullen, 2008;Cullen et al, 2003).…”

Right–Left Asymmetries in the Whisking Behavior of Rats Anticipate Head Movements

“…The VCR stabilizes the head in space through activation of neck muscles, but the reflex is modulated depending on whether head movement is active or passive (Cullen, 2004;Roy and Cullen, 2004). When the goal of head movement is perceptual stabilization, the VCR exactly accommodates for head movements.…”

“…When the goal of movement is to change the region of space actively being searched, the reflex is suppressed. Neurophysiological recordings have shown that a cancellation signal is present only when the activation of neck proprioceptors matches the motor-generated expectation during active head movements Roy and Cullen, 2004).…”

Separate Areas for Mirror Responses and Agency within the Parietal Operculum

“…In addition, when the sensory consequences of a selfgenerated event are predictable, responses to reafferent feedback are suppressed. This sensory gating (Blakemore et al, 1998;Roy and Cullen, 2004) is thought to depend on an interaction between cerebral and cerebellar cortical areas (Blakemore et al, 1999).…”