Spontaneous traveling waves naturally emerge from horizontal fiber time delays and travel through locally asynchronous-irregular states

Zachary W Davis,John H Reynolds,Terrence J Sejnowski,Lyle Muller,Charlee Fletterman,Christopher Steward,Gabriel B Benigno,Theo Desbordes

doi:10.1038/s41467-021-26175-1

Zachary W Davis, John H Reynolds + Show 6 more

Open Access

https://doi.org/10.1038/s41467-021-26175-1

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Abstract

Studies of sensory-evoked neuronal responses often focus on mean spike rates, with fluctuations treated as internally-generated noise. However, fluctuations of spontaneous activity, often organized as traveling waves, shape stimulus-evoked responses and perceptual sensitivity. The mechanisms underlying these waves are unknown. Further, it is unclear whether waves are consistent with the low rate and weakly correlated “asynchronous-irregular” dynamics observed in cortical recordings. Here, we describe a large-scale computational model with topographically-organized connectivity and conduction delays relevant to biological scales. We find that spontaneous traveling waves are a general property of these networks. The traveling waves that occur in the model are sparse, with only a small fraction of neurons participating in any individual wave. Consequently, they do not induce measurable spike correlations and remain consistent with locally asynchronous irregular states. Further, by modulating local network state, they can shape responses to incoming inputs as observed in vivo.

Highlights

Studies of sensory-evoked neuronal responses often focus on mean spike rates, with fluctuations treated as internally-generated noise
Previous work has shown that moment-by-moment fluctuations in synaptic input in the cortex can be on the same order of magnitude as during the sustained period of stimulus-evoked responses[6,22,23,24]
The model presented here shows that distance-dependent conduction delays in topographic, conductance-based spiking network models are sufficient to account for our results in vivo

Summary

Introduction

Studies of sensory-evoked neuronal responses often focus on mean spike rates, with fluctuations treated as internally-generated noise. The traveling waves that occur in the model are sparse, with only a small fraction of neurons participating in any individual wave They do not induce measurable spike correlations and remain consistent with locally asynchronous irregular states. Based on their speed of propagation, we hypothesize that these waves result from action potentials propagating along unmyelinated horizontal fibers To test this hypothesis, we studied a spiking network model across a range of biologically realistic neuronal densities, distance-dependent connection probabilities, excitatory/inhibitory balances, and synaptic conductance states. We studied a spiking network model across a range of biologically realistic neuronal densities, distance-dependent connection probabilities, excitatory/inhibitory balances, and synaptic conductance states This model incorporated axonal time delays from conduction along unmyelinated horizontal fibers, which shaped ongoing activity patterns into traveling waves consistent with those observed in vivo. Traveling waves can coexist with a locally asynchronous-irregular state, conferring their benefits while maintaining the computational advantages of this dynamical regime[20,21]

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