Neural Correlates of Motor Learning in the Vestibulo-Ocular Reflex: Dynamic Regulation of Multimodal Integration in the Macaque Vestibular System

Motor learning is required for the reacquisition of skills that have been compromised as a result of brain lesion or disease, as well as for the acquisition of new skills. Behaviors with well characterized anatomy and physiology are required to yield significant insight into changes that occur in the brain during motor learning. The vestibulo-ocular reflex (VOR) is well suited to establish connections between neurons, neural circuits, and motor performance during learning. Here, we examined the linkage between neuronal and behavioral VOR responses in alert behaving monkeys (Macaca mulatta) during the impressive recovery that occurs after unilateral vestibular loss. We show, for the first time, that motor learning is characterized by the dynamic reweighting of inputs from different modalities (i.e., vestibular vs extravestibular) at the level of the single neurons that constitute the first central stage of vestibular processing. Specifically, two types of information, which did not influence neuronal responses before the lesion, had an important role during compensation. First, unmasked neck proprioceptive inputs played a critical role in the early stages of this process demonstrated by faster and more substantial recovery of vestibular responses in proprioceptive sensitive neurons. Second, neuronal and VOR responses were significantly enhanced during active relative to passive head motion later in the compensation process (> 3 weeks). Together, our findings provide evidence linking the dynamic regulation of multimodal integration at the level of single neurons and behavioral recovery, suggesting a role for homeostatic mechanisms in VOR motor learning.