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Multiple dynamic representations in the motor cortex during sensorimotor learning

Abstract

The mechanisms linking sensation and action during learning are poorly understood. Layer 2/3 neurons in the motor cortex might participate in sensorimotor integration and learning; they receive input from sensory cortex and excite deep layer neurons, which control movement. Here we imaged activity in the same set of layer 2/3 neurons in the motor cortex over weeks, while mice learned to detect objects with their whiskers and report detection with licking. Spatially intermingled neurons represented sensory (touch) and motor behaviours (whisker movements and licking). With learning, the population-level representation of task-related licking strengthened. In trained mice, population-level representations were redundant and stable, despite dynamism of single-neuron representations. The activity of a subpopulation of neurons was consistent with touch driving licking behaviour. Our results suggest that ensembles of motor cortex neurons couple sensory input to multiple, related motor programs during learning.

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Figure 1: Learning a whisker-based object-detection task under the microscope.
Figure 2: Imaging population activity across trials.
Figure 3: Population decoding of behavioural features.
Figure 4: Single neuron representations across learning.
Figure 5: Plasticity in task-related neuronal dynamics.
Figure 6: Stability in population decoding.

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Acknowledgements

We thank B. Ölveczky, L. Petreanu, N. Li, A. Hantman and S. Druckmann for critical comments on the manuscript; N. Clack, V. Iyer and J. Vogelstein for help with software; D. Flickinger for help with microscope design; J. Kim for tdTomato adeno-associated virus; N. Xu for suggestions regarding mouse behaviour; and T.-W. Chen and E. Schreiter for help with calibrating GCaMP3.

Author information

Affiliations

Authors

Contributions

D.H. and K.S. conceived the study. D.H. performed all behavioural and in vivo imaging experiments. J.S.W. performed the LTP experiments. D.H., D.A.G., S.P. and K.S. performed analysis. D.A.G., S.P. and D.H.O. provided software. L.T., T.G.O. and L.L.L. provided reagents. D.H., D.A.G. and K.S. wrote the paper with comments from all authors.

Corresponding author

Correspondence to K. Svoboda.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-17 and Supplementary Tables 1-2. (PDF 6271 kb)

Supplementary Movie 1

This movie shows a behaving mouse under the two-photon microscope. Sequence of trial types: Go (hit), No Go (correct rejection), Go (hit), Go (hit), No Go (false alarm). (MOV 7602 kb)

Supplementary Movie 2

This movie shows motion-corrected raw fluorescence images of L2/3 neurons in vibrissal motor cortex infected with AAV-GCaMP3. The white square indicates pole sampling period. (MOV 3419 kb)

Supplementary Movie 3

This movie shows in the left panel the original high-speed whisker movie (500Hz). In the right panel the decoded whisker position (center of gray wedge) and amplitude (gray wedge width) based on calcium imaging. The black line represents C2 whisker angle (after tracking). The red hue of the wedge indicates the magnitude of the decoded whisker curvature change. (MOV 1638 kb)

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Huber, D., Gutnisky, D., Peron, S. et al. Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484, 473–478 (2012). https://doi.org/10.1038/nature11039

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