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Primary motor cortex underlies multi-joint integration for fast feedback control

Abstract

A basic difficulty for the nervous system is integrating locally ambiguous sensory information to form accurate perceptions about the outside world1,2,3,4. This local-to-global problem is also fundamental to motor control of the arm, because complex mechanical interactions between shoulder and elbow allow a particular amount of motion at one joint to arise from an infinite combination of shoulder and elbow torques5. Here we show, in humans and rhesus monkeys, that a transcortical pathway through primary motor cortex (M1) resolves this ambiguity during fast feedback control. We demonstrate that single M1 neurons of behaving monkeys can integrate shoulder and elbow motion information into motor commands that appropriately counter the underlying torque within about 50 milliseconds of a mechanical perturbation. Moreover, we reveal a causal link between M1 processing and multi-joint integration in humans by showing that shoulder muscle responses occurring 50 milliseconds after pure elbow displacement can be potentiated by transcranial magnetic stimulation. Taken together, our results show that transcortical processing through M1 permits feedback responses to express a level of sophistication that rivals voluntary control; this provides neurophysiological support for influential theories positing that voluntary movement is generated by the intelligent manipulation of sensory feedback6,7.

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Figure 1: Experimental methods.
Figure 2: Neurons in primary motor cortex.
Figure 3: Population analysis of neurons and muscles.
Figure 4: TMS and perturbation evoked activity in human shoulder muscles.

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Acknowledgements

This work was supported by the Canadian Institutes of Health Research (CIHR) and the National Sciences and Engineering Research Council of Canada (NSERC). J.A.P., I.K. and M.O. received salary awards from CIHR. We thank K. Moore and J. Peterson for technical support, and G. Blohm, B. Edin, R. Flanagan, R. Johansson, A. Kahn and D. Munoz for comments on the manuscript.

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Authors and Affiliations

Authors

Contributions

J.A.P. collected and analysed the monkey data, helped design the experiments, interpreted the results and helped write the manuscript. I.K. collected and analysed the human data, helped design the experiments, interpreted the results and helped write the manuscript. J.Y.N. helped collect the human data. M.O. helped collect a subset of the monkey data. B.B. helped interpret the human data. S.H.S. helped design the experiments, interpreted the results and helped write the manuscript.

Corresponding author

Correspondence to Stephen H. Scott.

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Competing interests

S.H.S. is associated with BKIN Technologies, which commercializes the KINARM device used in this study.

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Pruszynski, J., Kurtzer, I., Nashed, J. et al. Primary motor cortex underlies multi-joint integration for fast feedback control. Nature 478, 387–390 (2011). https://doi.org/10.1038/nature10436

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