Article | Published:

Robust neuronal dynamics in premotor cortex during motor planning

Nature volume 532, pages 459464 (28 April 2016) | Download Citation

  • A Corrigendum to this article was published on 29 June 2016

Abstract

Neural activity maintains representations that bridge past and future events, often over many seconds. Network models can produce persistent and ramping activity, but the positive feedback that is critical for these slow dynamics can cause sensitivity to perturbations. Here we use electrophysiology and optogenetic perturbations in the mouse premotor cortex to probe the robustness of persistent neural representations during motor planning. We show that preparatory activity is remarkably robust to large-scale unilateral silencing: detailed neural dynamics that drive specific future movements were quickly and selectively restored by the network. Selectivity did not recover after bilateral silencing of the premotor cortex. Perturbations to one hemisphere are thus corrected by information from the other hemisphere. Corpus callosum bisections demonstrated that premotor cortex hemispheres can maintain preparatory activity independently. Redundancy across selectively coupled modules, as we observed in the premotor cortex, is a hallmark of robust control systems. Network models incorporating these principles show robustness that is consistent with data.

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Acknowledgements

We thank B. DePasquale, A. Finkelstein, D. Gutnisky, A. Hantman, H. Inagaki, V. Jayaraman, J. Magee, S. Peron, S. Romani and N. Spruston for comments on the manuscript and discussion, T. Pluntke for animal training, A. Hu for histology, T. Harris and B. Barbarits for silicon probe recording system. This work was funded by Howard Hughes Medical Institute. N.L. and K.D. are Helen Hay Whitney Foundation postdoctoral fellows.

Author information

Author notes

    • Nuo Li
    •  & Kayvon Daie

    These authors contributed equally to this work.

Affiliations

  1. Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia 20147, USA

    • Nuo Li
    • , Kayvon Daie
    • , Karel Svoboda
    •  & Shaul Druckmann

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Contributions

N.L., K.S. and S.D. conceived and designed the experiments. N.L. and K.D. performed behavioural experiments. N.L. performed electrophysiology and optogenetic experiments. K.D. and S.D. performed modeling. N.L., K.D., K.S. and S.D. analysed data and wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Karel Svoboda or Shaul Druckmann.

Data have been deposited at the CRCNS (https://crcns.org/) and can be accessed at http://dx.doi.org/10.6080/K0RB72JW.

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https://doi.org/10.1038/nature17643

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