Physical Review X (Mar 2020)

Noise-Induced Synchronization and Antiresonance in Interacting Excitable Systems: Applications to Deep Brain Stimulation in Parkinson’s Disease

  • Jonathan D. Touboul,
  • Charlotte Piette,
  • Laurent Venance,
  • G. Bard Ermentrout

DOI
https://doi.org/10.1103/PhysRevX.10.011073
Journal volume & issue
Vol. 10, no. 1
p. 011073

Abstract

Read online Read online

We study the nonlinear dynamics of a surprising phenomenon arising in large networks of excitable elements in response to noise: while at low noise, solutions remain in the vicinity of the resting state and large-noise solutions show asynchronous activity, the network displays orderly, perfectly synchronized periodic responses at intermediate levels of noise. This noise-induced synchronization, distinct from classical stochastic resonance, is fundamentally collective in nature. Indeed, we show that, for noise and coupling within specific ranges, an asymmetry in the transition rates between a resting and an excited regime progressively builds up, leading to an increase in the fraction of excited neurons eventually triggering a chain reaction associated with a macroscopic synchronized excursion and a collective return to rest where this process starts afresh, thus yielding the observed periodic synchronized oscillations. We further uncover a novel antiresonance phenomenon in this regime: noise-induced synchronized oscillations disappear when the system is driven by periodic stimulation with frequency within a specific range (high relative to the spontaneous activity). In that antiresonance regime, the system is optimal for measures of information transmission. This observation provides a new hypothesis accounting for the efficiency of high-frequency stimulation therapies, known as deep brain stimulation, in Parkinson’s disease, a neurodegenerative disease characterized by an increased synchronization of brain motor circuits. We further discuss the universality of these phenomena in the class of stochastic networks of excitable elements with specific coupling and illustrate this universality by analyzing various classical models of neuronal networks. Altogether, these results uncover some universal mechanisms supporting a regularizing impact of noise in excitable systems, reveal a novel antiresonance phenomenon in these systems, and propose a new hypothesis for the efficiency of high-frequency stimulation in Parkinson’s disease.