Motor control by precisely timed spike patterns

• Type of Material: Article
• Authors: Kyle H. Srivastava, Georgia Institute of Technology; Caroline M. Holmes, Emory University; Michiel Vellema, University of Southern Denmark; Andrea R. Pack, Emory University; Coen P.H. Elemans, University of Southern Denmark; Ilya Nemenman, Emory University; Samuel Sober, Emory University
• Language: English
• Date: 2017-01-31
• Publisher: National Academy of Sciences
• Publication Version: Final Published Version
• Copyright Statement: © 2017 National Academy of Sciences.
• Final Published Version (URL): http://dx.doi.org/10.1073/pnas.1611734114
• Title of Journal or Parent Work: Proceedings of the National Academy of Sciences
• ISSN: 0027-8424
• Volume: 114
• Issue: 5
• Start Page: 1171
• End Page: 1176
• Grant/Funding Information: This work was supported by NIH Grants P30NS069250, R01NS084844, F31DC013753, and 5R90DA033462; National Science Foundation Grants 1208126 and 1456912; James S. McDonnell Foundation Grant 220020321; the Danish Research Council and Carlsberg Foundation; and the Woodruff Scholarship at Emory University.
• Keywords: computational neuroscience; songbird; neurophysiology; motor systems; information theory
• Research Categories: Engineering, Biomedical; Biology, General

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