Stochastic resonance mediates the state-dependent effect of periodic stimulation on cortical alpha oscillations.

Jérémie Lefebvre,Axel Hutt,Flavio Frohlich

doi:10.7554/elife.32054

Abstract

Brain stimulation can be used to engage and modulate rhythmic activity in brain networks. However, the outcomes of brain stimulation are shaped by behavioral states and endogenous fluctuations in brain activity. To better understand how this intrinsic oscillatory activity controls the susceptibility of the brain to stimulation, we analyzed a computational model of the thalamo-cortical system in two distinct states (rest and task-engaged) to identify the mechanisms by which endogenous alpha oscillations (8Hz-12Hz) are modulated by periodic stimulation. Our analysis shows that the different responses to stimulation observed experimentally in these brain states can be explained by a passage through a bifurcation combined with stochastic resonance - a mechanism by which irregular fluctuations amplify the response of a nonlinear system to weak periodic signals. Indeed, our findings suggest that modulation of brain oscillations is best achieved in states of low endogenous rhythmic activity, and that irregular state-dependent fluctuations in thalamic inputs shape the susceptibility of cortical population to periodic stimulation.

Highlights

Periodic brain stimulation, such as repetitive transcranial magnetic stimulation and transcranial alternating current stimulation, can be used to engage cortical rhythms (Frohlich 2015)
Our findings suggest that modulating brain oscillations is best achieved in states of low endogenous rhythmic activity, and that irregular state-dependent fluctuations in thalamic inputs shape the susceptibility of cortical population to periodic stimulation
To understand how the efficacy of periodic stimulation could depend on brain state (Alagappan et al 2016) we examined the hypothesis that cortical susceptibility to entrainment is controlled by sub-cortical populations

Summary

Introduction

Periodic brain stimulation, such as repetitive transcranial magnetic stimulation (rTMS) and transcranial alternating current stimulation (tACS), can be used to engage cortical rhythms (Frohlich 2015) Such findings have raised the fascinating prospect of manipulating rhythmic brain activity in a controlled manner, engaging neural circuits at a functional level to manipulate cognition and treat disorders of the central nervous system (Cerere et al 2015, Frohlich 2014, Romei et al 2016). The rest state is characterized by strong endogenous oscillations that reflect internally driven brain processes (Pfurtscheller et al 1996, Klimesch 2012) To compensate for these state-dependent differences in population activity, it has been suggested that stimulation parameters should be calibrated in a closed-loop

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Conclusion