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Research Article

Motor control by precisely timed spike patterns

Kyle H. Srivastava, Caroline M. Holmes, Michiel Vellema, Andrea R. Pack, Coen P. H. Elemans, Ilya Nemenman, and Samuel J. Sober
  1. aBiomedical Engineering Doctoral Program, Georgia Institute of Technology and Emory University, Atlanta, GA 30322;
  2. bDepartment of Physics, Emory University, Atlanta, GA 30322;
  3. cDepartment of Biology, Emory University, Atlanta, GA 30322;
  4. dDepartment of Biology, University of Southern Denmark, DK-5230 Odense, Denmark;
  5. eNeuroscience Doctoral Program, Emory University, Atlanta, GA 30322

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PNAS January 31, 2017 114 (5) 1171-1176; first published January 18, 2017; https://doi.org/10.1073/pnas.1611734114
Kyle H. Srivastava
aBiomedical Engineering Doctoral Program, Georgia Institute of Technology and Emory University, Atlanta, GA 30322;
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Caroline M. Holmes
bDepartment of Physics, Emory University, Atlanta, GA 30322;
cDepartment of Biology, Emory University, Atlanta, GA 30322;
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Michiel Vellema
dDepartment of Biology, University of Southern Denmark, DK-5230 Odense, Denmark;
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Andrea R. Pack
cDepartment of Biology, Emory University, Atlanta, GA 30322;
eNeuroscience Doctoral Program, Emory University, Atlanta, GA 30322
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Coen P. H. Elemans
dDepartment of Biology, University of Southern Denmark, DK-5230 Odense, Denmark;
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Ilya Nemenman
bDepartment of Physics, Emory University, Atlanta, GA 30322;
cDepartment of Biology, Emory University, Atlanta, GA 30322;
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Samuel J. Sober
cDepartment of Biology, Emory University, Atlanta, GA 30322;
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  • For correspondence: samuel.j.sober@emory.edu
  1. Edited by William Bialek, Princeton University, Princeton, NJ, and approved December 5, 2016 (received for review July 17, 2016)

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Significance

A crucial problem in neuroscience is understanding how neural activity (sequences of action potentials or “spikes”) controls muscles, and hence motor behaviors. Traditional theories of brain function assume that information from the nervous system to the muscles is conveyed by the total number of spikes fired within a particular time interval. Here, we combine physiological, behavioral, and computational techniques to show that, at least in one relatively simple behavior—respiration in songbirds—the precise timing of spikes, rather than just their number, plays a crucial role in predicting and causally controlling behavior. These findings suggest that basic assumptions about neural motor control require revision and may have significant implications for designing neural prosthetics and brain–machine interfaces.

Abstract

A fundamental problem in neuroscience is understanding how sequences of action potentials (“spikes”) encode information about sensory signals and motor outputs. Although traditional theories assume that this information is conveyed by the total number of spikes fired within a specified time interval (spike rate), recent studies have shown that additional information is carried by the millisecond-scale timing patterns of action potentials (spike timing). However, it is unknown whether or how subtle differences in spike timing drive differences in perception or behavior, leaving it unclear whether the information in spike timing actually plays a role in brain function. By examining the activity of individual motor units (the muscle fibers innervated by a single motor neuron) and manipulating patterns of activation of these neurons, we provide both correlative and causal evidence that the nervous system uses millisecond-scale variations in the timing of spikes within multispike patterns to control a vertebrate behavior—namely, respiration in the Bengalese finch, a songbird. These findings suggest that a fundamental assumption of current theories of motor coding requires revision.

  • motor systems
  • neurophysiology
  • computational neuroscience
  • information theory
  • songbird

Footnotes

  • ↵1K.H.S. and C.M.H. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: samuel.j.sober{at}emory.edu.
  • Author contributions: K.H.S., C.M.H., C.P.H.E., I.N., and S.J.S. designed research; K.H.S., C.M.H., M.V., and A.R.P. performed research; K.H.S., C.M.H., M.V., A.R.P., C.P.H.E., I.N., and S.J.S. analyzed data; and K.H.S., C.M.H., C.P.H.E., I.N., and S.J.S. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The data reported in this paper are available via https://figshare.com (DOI: 10.6084/m9.figshare.4546486).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1611734114/-/DCSupplemental.

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Motor control by precisely timed spike patterns
Kyle H. Srivastava, Caroline M. Holmes, Michiel Vellema, Andrea R. Pack, Coen P. H. Elemans, Ilya Nemenman, Samuel J. Sober
Proceedings of the National Academy of Sciences Jan 2017, 114 (5) 1171-1176; DOI: 10.1073/pnas.1611734114

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Motor control by precisely timed spike patterns
Kyle H. Srivastava, Caroline M. Holmes, Michiel Vellema, Andrea R. Pack, Coen P. H. Elemans, Ilya Nemenman, Samuel J. Sober
Proceedings of the National Academy of Sciences Jan 2017, 114 (5) 1171-1176; DOI: 10.1073/pnas.1611734114
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  • Neuroscience
Proceedings of the National Academy of Sciences: 114 (5)
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