Interaction of plasticity and circuit organization during the acquisition of cerebellum-dependent motor learning

Abstract

Motor learning occurs through interactions between the cerebellar circuit and cellular plasticity at different sites. Previous work has established plasticity in brain slices and suggested plausible sites of behavioral learning. We now reveal what actually happens in the cerebellum during short-term learning. We monitor the expression of plasticity in the simple-spike firing of cerebellar Purkinje cells during trial-over-trial learning in smooth pursuit eye movements of monkeys. Our findings imply that: 1) a single complex-spike response driven by one instruction for learning causes short-term plasticity in a Purkinje cell’s mossy fiber/parallel-fiber input pathways; 2) complex-spike responses and simple-spike firing rate are correlated across the Purkinje cell population; and 3) simple-spike firing rate at the time of an instruction for learning modulates the probability of a complex-spike response, possibly through a disynaptic feedback pathway to the inferior olive. These mechanisms may participate in long-term motor learning.DOI: http://dx.doi.org/10.7554/eLife.01574.001

The Errors of Our Ways: Understanding Error Representations in Cerebellar-Dependent Motor Learning

“…At the population level, complex spike synchrony is modulated by simple spike activity [153]. During smooth pursuit learning, simple spike firing increase also increases the probability of complex spike discharge, which in turn decreases the simple spike response on the subsequent trial [154]. The finding that simple spike firing modulates complex spike discharge suggests that rather than providing an error signal driven by sensory feedback, climbing fiber input may reflect the appropriateness of the cerebellar cortex’s response to specific behaviors.…”

Trial-by-Trial Motor Cortical Correlates of a Rapidly Adapting Visuomotor Internal Model

“…We believe this to be the first such report of motor cortical adaptation during arm reaching at the level of single trials. This result is evocative of behavioral and cerebellar changes that depend on the previous trial's error signals during oculomotor tasks (Medina and Lisberger, 2008;Yang and Lisberger, 2013;Kimpo et al, 2014) and, indeed, the cerebellum is a prime candidate for instructing these changes in motor cortex. The ability to observe internal model changes with single-trial resolution has utility for motor neural prostheses (Golub et al, 2015) and for studying the interaction of internal models, movements, and errors on the single-trial timescales at which these computations ultimately play out (Albert and Shadmehr, 2016).…”

Depressed by Learning—Heterogeneity of the Plasticity Rules at Parallel Fiber Synapses onto Purkinje Cells

“…Since then, the idea that the cerebellum learns by sculpting away synapses that cause errors through this anti-Hebbian form of synaptic plasticity has had a powerful influence on the cerebellar field. LTD and its links to cerebellum-dependent learning have been extensively investigated, yet there is still much disagreement about whether and how LTD at parallel fiber-to-Purkinje cell synapses contributes to learning [6,7,16–25,8,26–30,9–15]. Here, we review findings that suggest a path toward a Clearer and more sophisticated understanding of the contribution of LTD to cerebellum-dependent learning.…”