Corticostriatal dynamics encode the refinement of specific behavioral variability during skill learning

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Abstract

Learning to perform a complex motor task requires the optimization of specific behavioral features to cope with task constraints. We show that when mice learn a novel motor paradigm they differentially refine specific behavioral features. Animals trained to perform progressively faster sequences of lever presses to obtain reinforcement reduced variability in sequence frequency, but increased variability in an orthogonal feature (sequence duration). Trial-to-trial variability of the activity of motor cortex and striatal projection neurons was higher early in training and subsequently decreased with learning, without changes in average firing rate. As training progressed, variability in corticostriatal activity became progressively more correlated with behavioral variability, but specifically with variability in frequency. Corticostriatal plasticity was required for the reduction in frequency variability, but not for variability in sequence duration. These data suggest that during motor learning corticostriatal dynamics encode the refinement of specific behavioral features that change the probability of obtaining outcomes.

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Fernando J Santos

Champalimaud Neuroscience Programme, Fundação Champalimaud, Lisbon, Portugal

Competing interests
No competing interests declared.
Rodrigo F Oliveira

Champalimaud Neuroscience Programme, Fundação Champalimaud, Lisbon, Portugal

Competing interests
No competing interests declared.
Xin Jin

Molecular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, United States

Competing interests
No competing interests declared.
Rui M Costa

Champalimaud Neuroscience Programme, Fundação Champalimaud, Lisbon, Portugal

For correspondence
rui.costa@neuro.fchampalimaud.org

Competing interests
Rui M Costa, Reviewing editor, eLife.

Ethics

Animal experimentation: All experimental procedures were carried in accordance to the ethics committee guidelines of the Champalimaud Foundation and Instituto Gulbenkian de Ciência, and with approval of the Portuguese DGAV (ref 0421).

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.