Editors' ChoiceNeuroscience

Learning to expect the unexpected: Updating the cerebellum during voluntary movement

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Science Translational Medicine  16 Sep 2015:
Vol. 7, Issue 305, pp. 305ec156
DOI: 10.1126/scitranslmed.aad3612

To guide our muscles precisely and carefully, we must quickly refine the neural commands to muscles and limbs, whether we are responding to unexpected forces or making routine movements. The cerebellum, a region at the lower back of the brain, participates by constructing an estimate of where our body is in space, but there is only theoretical evidence of where and how this estimate is refined during movement. The prevailing theory is that the brain compares a predicted measure of motor output with actual sensory feedback. This difference, the sensory prediction error, is fundamental to refining motor commands. Brooks et al. recently revealed the elegant computation performed by the cerebellum, which compares expected and unexpected sensory inputs to fine-tune behavior during motor learning.

To examine the learning process, the team investigated a well-organized and straightforward sensory-motor pathway in the monkey cerebral cortex that sends information to structures involved in postural control, such as the spinal cord and vestibular system. While monkeys made voluntary head movements, the authors applied an unexpected load to the head and recorded activity from single neurons in the cerebellar nucleus. Their key finding was that neurons displayed responses consistent with the initial introduction of a sensory prediction error, as well as its subsequent decline, throughout motor learning. Further corroborating their findings, they observed corresponding parallel changes in the responses of neurons downstream in the vestibular nucleus. This substantiated a direct link between the observed changes in the cerebellar commands with voluntary head motion.

This team has now demonstrated the existence of an explicit neural representation of motor learning in the cerebellum. The changes in head movement were consistently linked to changes in neural responses whereby the neurons increased sensitivity upon application of an expected and unexpected load. This is an important contribution to our understanding of motor learning and how it contributes to health and disease.

J. X. Brooks et al., Learning to expect the unexpected: Rapid updating in primate cerebellum during voluntary self-motion. Nat. Neurosci. 18, 1310–1317 (2015). [Abstract]

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