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Neuron. 2018 Feb 21;97(4):953-966.e8. doi: 10.1016/j.neuron.2018.01.004. Epub 2018 Feb 1.

Motor Cortex Embeds Muscle-like Commands in an Untangled Population Response.

Author information

1
Department of Neuroscience, Columbia University Medical Center, New York, NY 10032, USA; Zuckerman Institute, Columbia University, New York, NY 10027, USA.
2
Zuckerman Institute, Columbia University, New York, NY 10027, USA; Department of Biomedical Engineering, Columbia University, New York, NY 10027, USA.
3
SeatGeek, New York, NY 10003, USA.
4
Department of Neuroscience, Columbia University Medical Center, New York, NY 10032, USA; Zuckerman Institute, Columbia University, New York, NY 10027, USA; Departments of Biochemistry and Molecular Biophysics, Columbia University Medical Center, New York, NY 10032, USA.
5
Department of Ophthalmology and Visual Sciences, Dominick Purpura Department of Neuroscience, Albert Einstein College of Medicine, Yeshiva University, Bronx, NY 10461, USA.
6
Department of Neuroscience, Columbia University Medical Center, New York, NY 10032, USA; Zuckerman Institute, Columbia University, New York, NY 10027, USA; Kavli Institute for Brain Science, Columbia University Medical Center, New York, NY 10032, USA; Howard Hughes Medical Institute, Columbia University, New York, NY 10032, USA; Departments of Biochemistry and Molecular Biophysics, Columbia University Medical Center, New York, NY 10032, USA.
7
Department of Neuroscience, Columbia University Medical Center, New York, NY 10032, USA; Zuckerman Institute, Columbia University, New York, NY 10027, USA; Kavli Institute for Brain Science, Columbia University Medical Center, New York, NY 10032, USA; Department of Physiology and Cellular Biophysics, Columbia University Medical Center, New York, NY 10032, USA; Center for Theoretical Neuroscience, Columbia University Medical Center, New York, NY 10032, USA.
8
Zuckerman Institute, Columbia University, New York, NY 10027, USA; Grossman Center for the Statistics of Mind, Columbia University, New York, NY 10027, USA; Center for Theoretical Neuroscience, Columbia University Medical Center, New York, NY 10032, USA; Department of Statistics, Columbia University, New York, NY 10027, USA.
9
Department of Neuroscience, Columbia University Medical Center, New York, NY 10032, USA; Zuckerman Institute, Columbia University, New York, NY 10027, USA; Kavli Institute for Brain Science, Columbia University Medical Center, New York, NY 10032, USA; Grossman Center for the Statistics of Mind, Columbia University, New York, NY 10027, USA. Electronic address: mc3502@columbia.edu.

Abstract

Primate motor cortex projects to spinal interneurons and motoneurons, suggesting that motor cortex activity may be dominated by muscle-like commands. Observations during reaching lend support to this view, but evidence remains ambiguous and much debated. To provide a different perspective, we employed a novel behavioral paradigm that facilitates comparison between time-evolving neural and muscle activity. We found that single motor cortex neurons displayed many muscle-like properties, but the structure of population activity was not muscle-like. Unlike muscle activity, neural activity was structured to avoid "tangling": moments where similar activity patterns led to dissimilar future patterns. Avoidance of tangling was present across tasks and species. Network models revealed a potential reason for this consistent feature: low tangling confers noise robustness. Finally, we were able to predict motor cortex activity from muscle activity by leveraging the hypothesis that muscle-like commands are embedded in additional structure that yields low tangling.

KEYWORDS:

motor control; motor cortex; movement generation; neural dynamics; neural network; pattern generation; rhythmic movement

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