Motor control by precisely timed spike patterns

• 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
• Journal Title: Proceedings of the National Academy of Sciences
• Volume: Volume 114, Number 5
• Publisher: National Academy of Sciences | 2017-01-31, Pages 1171-1176
• Type of Work: Article | Final Publisher PDF
• Publisher DOI: http://doi.org/10.1073/pnas.1611734114
• Subjects: Biology, General; Engineering, Biomedical
• Keywords: motor systems; neurophysiology; computational neuroscience; information theory; songbird

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