Neural Computations Underlying Cancellation of the Vestibular Consequences of Voluntary Movement

Johns Hopkins University, Baltimore MD

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Abstract

Project Summary: This research program is motivated by three goals. First, we will establish the cerebellar mechanisms that underlie the brain's ability to estimate and cancel self-generated vestibular (inner ear balance) input during active movement Second, we will determine how the cerebellum encodes changes in the relationship between expected and actual sensory input when these predictions are learned, adapted, and flexibly implemented. Third, we will assess how cerebellum-mediated vestibular reafference suppression generalizes to another natural self-motion behavior, namely standing balance and its adaptation. The brain's ability to distinguish sensory stimuli that are the result of self-generated (Le., active) versus unexpected or externally generated (i.e., passive) stimulation is vital to ensuring perceptual stability and accurate motor control. Notably, in the vestibular system, the same central neurons that receive afferent input also send direct projections to motor centers to control posture via vestibular-spinal reflexes. These are essential for providing robust postural responses to unexpected vestibular stimuli yet counter-productive when the goal is to make active head movements. Accordingly, it is advantageous to suppress this pathway during active self-motion. Over the past two decades, we have made excellent progress toward identifying how the brain makes the distinction between active and passive vestibular signals - vestibular reafference vs. exafference, respectively. While vestibular afferents responses remain robust (and equivalent) regardless of whether stimulation is active or passive, neural responses at the next stage of processing in the vestibular nuclei are significantly attenuated during active stimulation. Further, this selective suppression of vestibular reafference only occurs when sensory feedback matches that expected based on motor command (e.g., during active movements). During the current grant period, we established that the cerebellum integrates sensory and motor inputs to make the required distinction between reafference and exafference. In the proposed research, we will address several fundamental questions that remain open. First, Aim 1 will establish how the cerebellum learns to interpret active motion as self-generated when the relationship between the actual and expected sensory feedback is altered. Aim 2 will determine how the vestibular cerebellum computes the expected consequences of self-motion when predictions must adapt to changes in the statistics of sensory feedback and/or be flexibly implemented across contexts. Finally, in Aim 3 we will determine whether and how cerebellum-mediated vestibular reafference suppression generalizes to another natural self-motion behavior: standing balance and its adaptation to perturbations. Combined, these studies will (1) advance our understanding of how the cerebellum computes the expected consequences of self-motion in everyday life when predictions are learned, adapted, and flexibly implemented, and (2) establish how the mechanisms underlying reafference suppression ensure postural stability.