Gating of neural error signals during motor learning

TL;DR

This study investigates how cerebellar climbing fiber error signals influence motor learning, revealing that their ability to induce plasticity is dynamically gated by circuit state, differing between VOR-increase and VOR-decrease paradigms.

Contribution

It demonstrates that climbing fiber signals can be selectively effective or ineffective in driving plasticity depending on circuit conditions during different motor learning tasks.

Findings

Climbing fiber activity predicts cerebellar output changes during VOR-increase training.

Optogenetic activation of climbing fibers can induce VOR-increase learning.

Climbing fiber signals do not predict or induce VOR-decrease learning.

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. Comparison of the two training paradigms suggests that the ability of climbing fibers to induce plasticity can be dynamically gated in vivo by the state of the cerebellar circuit, even under conditions where the climbing fibers are robustly activated by performance errors.