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Learning to expect the unexpected: rapid updating in primate cerebellum during voluntary self-motion
Jessica X Brooks1,2, Jerome Carriot1,2 & Kathleen E Cullen1
There is considerable evidence that the cerebellum has a vital role in motor learning by constructing an estimate of the sensory consequences of movement. Theory suggests that this estimate is compared with the actual feedback to compute the sensory prediction error. However, direct proof for the existence of this comparison is lacking. We carried out a trial-by-trial analysis of cerebellar neurons during the execution and adaptation of voluntary head movements and found that neuronal sensitivities dynamically tracked the comparison of predictive and feedback signals. When the relationship between the motor command and resultant movement was altered, neurons robustly responded to sensory input as if the movement was externally generated. Neuronal sensitivities then declined with the same time course as the concurrent behavioral learning. These findings demonstrate the output of an elegant computation in which rapid updating of an internal model enables the motor system to learn to expect unexpected sensory inputs.
npg 201 5 Nature America, Inc. All rights reserved.
How does the brain allow us to acquire new skills and maintain mastered skills in response to changes in the external environment and our motor systems? There are many reasons to believe that it does this by computing a sensory prediction error signal that represents the difference between the expected and actual sensory consequences of a given motor command. First, the intrinsic delays of sensory feedback make it impossible for sensory signals alone to account for many aspects of motor learning15. Second, theoretical investigations have demonstrated that the computation of sensory prediction errors is essential for fine-tuning motor behavior, including its on-line control and motor adaptation6,7. Third, behavioral studies in humans suggest that errors induced by external perturbations are interpreted as sensory prediction errors8,9.
The cerebellum, a structure that is well-conserved across vertebrates, has a vital role in motor learning. Numerous studies have focused on understanding the information represented by the activity of cerebellar Purkinje cells, whose axons encode the output of the cerebellar cortex, during motor learning (reviewed in refs. 10,11). Although progress has been limited by the inherent challenge of systematically dissociating motor...