Millisecond Spike Timing Codes for Motor Control

doi:10.1016/j.tins.2018.08.010

Trends in Neurosciences

Volume 41, Issue 10, October 2018, Pages 644-648

https://doi.org/10.1016/j.tins.2018.08.010 Get rights and content

Millisecond variations in spiking patterns can radically alter motor behavior, suggesting that traditional rate-based theories of motor control require revision. The importance of spike timing in sensorimotor control arises from dynamic interactions between the nervous system, muscles, and the body. New mechanisms, model systems, and theories are revealing how these interactions shape behavior.

Section snippets

When a Millisecond Matters: Correlative and Causal Evidence

Correlative evidence that millisecond spike timing differences affect behavior has been shown across a wide range of species and behaviors. Mammalian motor units regularly exhibit doublets and triplets with inter-spike intervals of 5–10 ms; occurrences increase as muscles fatigue, presumably to increase force via central mechanisms [3]. Recent examples show that spike timing correlates with variations in both fast and slow periodic behaviors, or with selection of different behavioral programs (

Why a Millisecond Matters: Motor Codes Interact with System Biomechanics

Intuitively, it would seem that a millisecond could hardly affect muscle force output, as a spike elicits a 40–100 ms force twitch in mammalian striated muscles [3]. Nonetheless, at least three classes of mechanisms enable small timing changes to profoundly alter motor output in vivo: (i) muscle properties, (ii) mechanical feedback, and (iii) biomechanical sensitivities (Figure 1B).

A number of intrinsic muscle force-generating properties (Figure 1B, i) allow small differences in spike timing and

A Diversity, Not a Dichotomy, of Spike Codes

Recent computational, experimental, and analytical innovations emphasize the diversity of motor codes beyond the classic dichotomy of rate versus timing (Figure 2A); both sensory and motor timing codes can differ across many dimensions (Figure 2D). One crucial issue is whether sensory or motor information is encoded by the timing of individual spikes (‘single-spike code’), the relative timing of two spikes (‘inter-spike-interval code’), or more spikes (‘pattern code’). Furthermore, both rate

New Directions in Timing and the Motor System

Our growing appreciation of timing codes raises as many questions as it answers. One challenge is completeness. Most neural recordings sample a (very) limited subset of the signals involved in motor processing, and often from a single anatomical structure. Questions of timing and rate, consistency, and redundancy would benefit from comprehensive recordings of the motor code, especially with spike level resolution, to capture a more complete picture of the motor program. Spiking datasets

Acknowledgements

This work was supported by NIH R01 NS084844 to SJS, NIH R01 EB022872 and NIH R01 NS099375 to SJS and IN, NIH R01 HD046922 and NIH R01 HD090642 to LHT, ARO W911NF-14-1-0396 and NSF CAREER PoLS 1554790 to SS. This work was done while LHT was visiting the Simons Institute for the Theory of Computing, and in part when SJS, SNS, and IN were visiting the Aspen Center for Physics.

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Citation Excerpt :
Thus, the full range of force and fo step sizes varies between 0.85 and 126 μN and 50 mHz and 7.4 Hz, respectively. Both suboptimal spike rates or timing codes35 and lateral force transmission52,53 result in lower force production by individual MFs compared to maximal stress during isometric activation. Therefore, the minimal force and vocal feature steps presented here can be considered conservative estimates and are likely even smaller during song.
The motor control resolution of any animal behavior is limited to the minimal force step available when activating muscles, which is set by the number and size distribution of motor units (MUs) and muscle-specific force. Birdsong is an excellent model system for understanding acquisition and maintenance of complex fine motor skills, but we know surprisingly little about how the motor pool controlling the syrinx is organized and how MU recruitment drives changes in vocal output. Here we developed an experimental paradigm to measure MU size distribution using spatiotemporal imaging of intracellular calcium concentration in cross-sections of living intact syrinx muscles. We combined these measurements with muscle stress and an in vitro syrinx preparation to determine the control resolution of fundamental frequency (f_o), a key vocal parameter, in zebra finches. We show that syringeal muscles have extremely small MUs, with 40%–50% innervating ≤3 and 13%–17% innervating a single muscle fiber. Combined with the lowest specific stress (5 mN/mm²) known to skeletal vertebrate muscle, small force steps by the major f_o controlling muscle provide control of 50-mHz to 7.3-Hz steps per MU. We show that the song system has the highest motor control resolution possible in the vertebrate nervous system and suggest this evolved due to strong selection on fine gradation of vocal output. Furthermore, we propose that high-resolution motor control was a key feature contributing to the radiation of songbirds that allowed diversification of song and speciation by vocal space expansion.
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Trends in Neurosciences

ForumSpecial Issue: Time in the BrainMillisecond Spike Timing Codes for Motor Control

Section snippets

When a Millisecond Matters: Correlative and Causal Evidence

Why a Millisecond Matters: Motor Codes Interact with System Biomechanics

A Diversity, Not a Dichotomy, of Spike Codes

New Directions in Timing and the Motor System

Acknowledgements

Curr. Opin. Neurobiol.

Cortical control of arm movements: a dynamical systems perspective

Annu. Rev. Neurosci.

Catchlike property of skeletal muscle: recent findings and clinical implications

Muscle Nerve

Chapter 12: Muscle, biomechanics, and implications for neural control

Abdicating power for control: a precision timing strategy to modulate function of flight power muscles

Proc. Biol. Sci.

Millisecond-scale motor encoding in a cortical vocal area

PLoS Biol.

Forum
Special Issue: Time in the Brain
Millisecond Spike Timing Codes for Motor Control