Abstract

Cerebellar climbing fiber activity encodes performance errors during many motor learning tasks, but the role of these error signals in learning has been controversial. We compared two motor learning paradigms that elicited equally robust putative error signals in the same climbing fibers: learned increases and decreases in the gain of the vestibulo-ocular reflex (VOR). During VOR-increase training, climbing fiber activity on one trial predicted changes in cerebellar output on the next trial, and optogenetic activation of climbing fibers to mimic their encoding of performance errors was sufficient to implant a motor memory. In contrast, during VOR-decrease training, there was no trial-by-trial correlation between climbing fiber activity and changes in cerebellar output, and climbing fiber activation did not induce VOR-decrease learning. Our data suggest that the ability of climbing fibers to induce plasticity can be dynamically gated in vivo, even under conditions where climbing fibers are robustly activated by performance errors. DOI: http://dx.doi.org/10.7554/eLife.02076.001.

Highlights

  • OverviewThe cerebellum is thought to implement a supervised learning algorithm, with the climbing fiber input to the cerebellum providing error signals that induce learning

  • We describe a second level of regulation in animals undergoing learning: even when climbing fibers are robustly activated by performance errors, the ability of that climbing fiber activity to trigger plasticity can be regulated by the state of the cerebellar circuit

  • An extracellular recording from a Purkinje cell provides simultaneous access to two distinct physiological signals: complex spikes, which provide a one-to-one readout of spikes in the single climbing fiber innervating the Purkinje cell (Eccles et al, 1966); and simple spikes, which reflect the impact of all excitatory and inhibitory inputs as well as the intrinsic excitability of the Purkinje cell (Figure 1)

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Summary

Introduction

The cerebellum is thought to implement a supervised learning algorithm, with the climbing fiber input to the cerebellum providing error signals that induce learning. According to this model, performance errors activate neurons in the inferior olive and their climbing fiber axons, which in turn trigger the induction of plasticity in the cerebellar cortex to produce adaptive changes in behavior (Marr, 1969; Albus, 1971). We describe a second level of regulation in animals undergoing learning: even when climbing fibers are robustly activated by performance errors, the ability of that climbing fiber activity to trigger plasticity can be regulated by the state of the cerebellar circuit. Climbing fiber activity as the trigger of cerebellar learning: conflicting evidence The cerebellum is not a slave to its climbing fiber ‘teachers’, but rather plays an active role in determining whether it will adapt in response to the error signals it receives from the climbing fibers.

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