Multisensory integration and self-motion perception in primate vestibular cortex

Johns Hopkins University, Baltimore MD

Investigators

Abstract

Project Summary In vertebrate animals, the vestibular system (primarily known as the “balance system” of the brain) interprets head-movement and orientation signals to provide organisms with a sense of self-motion. The vital contribution of vestibular system to reflexive control of posture, gaze, and gait is well characterized; however, far less is known about the neural substrates underlying higher-order vestibular functions, such as the perception of self- motion and the awareness of one's orientation in space. These functions rely on the cortical integration of vestibular input with somatosensory and visual input. In non-human primates, the parieto-insular vestibular cortex (PIVC) is uniquely suited to perform this multisensory integration. Unlike other vestibular-sensitive cortical areas, PIVC has direct access to vestibular, somatosensory, and visual input from the thalamus; indeed, it is hypothesized that other vestibular cortical areas receive their vestibular input from PIVC, thus making it a nexus for higher-order vestibular function. Despite its hypothesized importance, extremely little is known about the neural mechanisms by which PIVC integrates vestibular and extra-vestibular input, and whether this integration is context dependent. For example, it is unclear whether PIVC neurons differentiate between vestibular input generated during passive vs. active movements; such differentiation is seen in the vestibular nuclei and thalamus and is thought to be essential for producing a sense of motor agency. To investigate these issues, I propose to conduct high-density neurophysiological recordings in behaving primates during both passive stimulation and actively generated head and whole-body movement. In Aim 1, I will investigate how PIVC integrates passively applied vestibular and somatosensory input (Aim 1.1) and then vestibular and visual input (Aim 1.2). In Aim 2, I will investigate whether PIVC differentially processes vestibular input during passive and active movement. Specifically, I will examine how PIVC processes vestibular input generated during natural self-motion (i.e., self- motion relying on sensorimotor input in the form of a head-turning task, Aim 2.1). I will then examine how PIVC processes vestibular input generated during a learned, cognitively demanding motor task (Aim 2.2). In both aims, I will determine how individual neurons in PIVC encode vestibular and extra-vestibular input, as well as how this information is represented at the population level. The proposed experiments will resolve two questions which are fundamental to understanding PIVC function: 1) How does PIVC integrate multisensory input to construct a percept of self-motion? and 2) Is the processing of self-motion by PIVC neurons consistent with that required to provide a sense of motor agency? Furthermore, the proposed experiments will determine how sensorimotor and cognitive percepts of self-motion are represented in PIVC. This research will provide new insights into cortical vestibular function and how it supports the higher-order processes that allow primates (both human and non- human) to successfully perceive and navigate their environments.