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Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task

Abstract

When an animal learns to make movements in response to different stimuli, changes in activity in the motor cortex seem to accompany and underlie this learning1,2,3,4,5,6. The precise nature of modifications in cortical motor areas during the initial stages of motor learning, however, is largely unknown. Here we address this issue by chronically recording from neuronal ensembles located in the rat motor cortex, throughout the period required for rats to learn a reaction-time task. Motor learning was demonstrated by a decrease in the variance of the rats' reaction times and an increase in the time the animals were able to wait for a trigger stimulus. These behavioural changes were correlated with a significant increase in our ability to predict the correct or incorrect outcome of single trials based on three measures of neuronal ensemble activity: average firing rate, temporal patterns of firing, and correlated firing. This increase in prediction indicates that an association between sensory cues and movement emerged in the motor cortex as the task was learned. Such modifications in cortical ensemble activity may be critical for the initial learning of motor tasks.

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Figure 1: Improvements in behavioural performance parallelled increases in the neuronal predictions of trial outcomes.
Figure 2: Neuronal ensemble responses associated with correct and error trials.
Figure 3: Predictions of trial outcome were based on temporal patterns of firing and correlated activity.
Figure 4: Muscle activations and response kinematics were similar on correct and error trials.

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Acknowledgements

We thank P. Beck, D. Cohen, D. Katz, D. Krupa, M. Shuler and B. Storey-Laubach for comments on the manuscript. The work was supported by grants from the National Institute of Health (M.L. and M.A.L.N.), the National Science Foundation, the Defense Advanced Research Project Agency, the Office of Naval Research, and the Human Frontiers and Whitehall Foundations (M.A.L.N.). J.W. was supported by the Swedish Foundation for International Cooperation in Research and Higher Education and by the Swedish Medical Research Council.

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Laubach, M., Wessberg, J. & Nicolelis, M. Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task. Nature 405, 567–571 (2000). https://doi.org/10.1038/35014604

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