Motor control by precisely timed spike patterns

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 T he brain uses sequences of spikes to encode sensory and motor signals. In principle, neurons can encode this information via their firing rates, the precise timing of their spikes, or both (1, 2). Although many studies have shown that spike timing contains information beyond that in the rate in sensory codes (3-5), these studies could not verify whether precise timing affects perception or behavior. In motor systems, rate coding approaches dominate (6, 7), but we recently showed that precise spike timing in motor cortex can predict upcoming behavior better than spike rates (8), showing that spike timing carries information in motor as well as sensory cortex. However, as in sensory systems, it remains unknown whether spike timing in motor systems actually controls variations in behavior (9, 10). Resolving this question, therefore, requires examining the spike code used by the neurons that innervate the muscles, because discovering an apparent spike timing code in any brain area upstream of motor neurons is subject to the same ambiguity about whether spike timing patterns actually affect behavior.A spike timing-based theory of motor production predicts that millisecond-scale fluctuations in spike timing, holding other spike train features constant, will causally influence behavior. We tested this prediction by analyzing the activity of single motor units (that is, the muscle fibers innervated by a single motor neuron), focusing largely on the minimal patterns that have variable spike timing but fixed firing rate, burst onset, and burst duration: sequences of three spikes ("triplets"), where the third spike is a fixed latency after the first, but the timing of the middle spike varies. We examined timing codes in songbirds by focusing on respiration, ...

Degeneracy in hippocampal physiology and plasticity

“…With reference to neural codes for features of the external environment, the coding of spatial location of animal in the hippocampus is an ideal instance of hybrid encoding schema that expresses degeneracy. Unlike the argument for rate versus temporal coding that seems to drive the narrative otherwise Fries et al, 2007;Gallistel, 2017;Jaramillo & Kempter, 2017;London et al, 2010;Panzeri et al, 2017;Shadlen & Newsome, 1994;Shadlen & Newsome, 1995;Shadlen & Newsome, 1998;Singer et al, 1997;Softky, 1994;Softky, 1995;Srivastava et al, 2017), hippocampal physiologists have concurred on the existence of dual/hybrid encoding schema for place-specific encoding. Specifically, place cells in the hippocampus elicit higher rates of firing when the animal enters a specific place field.…”

Unsupervised Bayesian Ising Approximation for revealing the neural dictionary in songbirds

“…While the identified codewords are statistically significant, and we show that they can predict the behavior better than larger, but non-specific features of the neural activity, a crucial future test of our findings will be in establishing their causal rather than merely correlative nature by means of stimulating neurons with patterns of pulses mimicking the identified codewords 36 . This will be facilitated by the speed of our method, which can reconstruct dictionaries in real time on a laptop computer.…”

“…For many different experimental systems, it has been possible to measure the information content of spike trains [34][35][36] , but the question of decoding -which spike patterns carry this information? -has turned out to be a harder one.…”

Temporal pattern of electrical stimulation is a new dimension of therapeutic innovation

“…In addition to a demonstrated role in sensory coding and perception, the precise temporal pattern of activity plays a key role in motor control, as well. For example, shuffling or jittering the timing of spikes in motor neurons reduced the information content of the spike train and the precise timing of spikes in motor neurons predicted respiratory air pressure, while the shuffled patterns did not [•Srivastava et al 2017]. …”