Investigations of behaviors with well-characterized circuitry are required to understand how the brain learns new motor skills and ensures existing behaviors remain appropriately calibrated over time. Accordingly, here we recorded from neurons within different sites of the vestibulo-spinal circuitry of behaving macaque monkeys during temporally precise activation of vestibular afferents. Behaviorally relevant patterns of vestibular nerve activation generated a rapid and substantial decrease in the monosynaptic responses recorded at the first central stage of processing from neurons receiving direct input from vestibular afferents within minutes, as well as a decrease in the compensatory reflex response that lasted up to 8 hours. In contrast, afferent responses to this same stimulation remained constant, indicating that plasticity was not induced at the level of the periphery but rather at the afferent-central neuron synapse. Strikingly, the responses of neurons within indirect brainstem pathways also remained constant, even though the efficacy of their central input was significantly reduced. Taken together, our results show that rapid plasticity at the first central stage of vestibulo-spinal pathways can guide changes in motor performance, and that complementary plasticity on the same millisecond time scale within inhibitory vestibular nuclei networks contributes to ensuring a relatively robust behavioral output.
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