Abstract

In the idling brain, neuronal circuits transition between periods of sustained firing (UP state) and quiescence (DOWN state), a pattern the mechanisms of which remain unclear. Here we analyzed spontaneous cortical population activity from anesthetized rats and found that UP and DOWN durations were highly variable and that population rates showed no significant decay during UP periods. We built a network rate model with excitatory (E) and inhibitory (I) populations exhibiting a novel bistable regime between a quiescent and an inhibition-stabilized state of arbitrarily low rate. Fluctuations triggered state transitions, while adaptation in E cells paradoxically caused a marginal decay of E-rate but a marked decay of I-rate in UP periods, a prediction that we validated experimentally. A spiking network implementation further predicted that DOWN-to-UP transitions must be caused by synchronous high-amplitude events. Our findings provide evidence of bistable cortical networks that exhibit non-rhythmic state transitions when the brain rests.

Highlights

  • A ubiquitous pattern of spontaneous cortical activity during synchronized brain states consists of the alternation between periods of tonic firing (UP states) and periods of quiescence (DOWN states) (Luczak et al, 2007; Steriade et al, 1993a; Timofeev et al, 2001)

  • Our model provides the first EI network that exhibits stochastic transitions between a silent and a low rate inhibition-stabilized attractor matching the statistics of UP and DOWN periods and population rate time-courses observed in the cortex

  • Using cortical population recordings we have shown that UP and DOWN period durations are irregular and show positive serial correlation, but there is no significant decrease of population rate during UP periods

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Summary

Introduction

A ubiquitous pattern of spontaneous cortical activity during synchronized brain states consists of the alternation between periods of tonic firing (UP states) and periods of quiescence (DOWN states) (Luczak et al, 2007; Steriade et al, 1993a; Timofeev et al, 2001). During DOWN periods, in the absence of firing, the fatigue variables recover until the circuit becomes self-excitable and autonomously transitions into an UP state (Cunningham et al, 2006; Le Bon-Jego and Yuste, 2007; Poskanzer and Yuste, 2011; Sanchez-Vives and McCormick, 2000; Timofeev et al, 2000) This mechanism of activity dependent negative feedback causing oscillatory UP-DOWN dynamics has been implemented by several computational models

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