Macroscopic phase resetting-curves determine oscillatory coherence and signal transfer in inter-coupled neural circuits

PLoS Comput Biol. 2019 May 9;15(5):e1007019. doi: 10.1371/journal.pcbi.1007019. eCollection 2019 May.


Macroscopic oscillations of different brain regions show multiple phase relationships that are persistent across time and have been implicated in routing information. While multiple cellular mechanisms influence the network oscillatory dynamics and structure the macroscopic firing motifs, one of the key questions is to identify the biophysical neuronal and synaptic properties that permit such motifs to arise. A second important issue is how the different neural activity coherence states determine the communication between the neural circuits. Here we analyse the emergence of phase-locking within bidirectionally delayed-coupled spiking circuits in which global gamma band oscillations arise from synaptic coupling among largely excitable neurons. We consider both the interneuronal (ING) and the pyramidal-interneuronal (PING) population gamma rhythms and the inter coupling targeting the pyramidal or the inhibitory neurons. Using a mean-field approach together with an exact reduction method, we reduce each spiking network to a low dimensional nonlinear system and derive the macroscopic phase resetting-curves (mPRCs) that determine how the phase of the global oscillation responds to incoming perturbations. This is made possible by the use of the quadratic integrate-and-fire model together with a Lorentzian distribution of the bias current. Depending on the type of gamma (PING vs. ING), we show that incoming excitatory inputs can either speed up the macroscopic oscillation (phase advance; type I PRC) or induce both a phase advance and a delay (type II PRC). From there we determine the structure of macroscopic coherence states (phase-locking) of two weakly synaptically-coupled networks. To do so we derive a phase equation for the coupled system which links the synaptic mechanisms to the coherence states of the system. We show that a synaptic transmission delay is a necessary condition for symmetry breaking, i.e. a non-symmetric phase lag between the macroscopic oscillations. This potentially provides an explanation to the experimentally observed variety of gamma phase-locking modes. Our analysis further shows that symmetry-broken coherence states can lead to a preferred direction of signal transfer between the oscillatory networks where this directionality also depends on the timing of the signal. Hence we suggest a causal theory for oscillatory modulation of functional connectivity between cortical circuits.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Brain / physiology
  • Computational Biology
  • Computer Simulation
  • Gamma Rhythm / physiology*
  • Humans
  • Interneurons / physiology
  • Models, Neurological*
  • Nerve Net / physiology*
  • Synaptic Transmission / physiology*

Grants and funding

GD was supported by the CNRS, INSERM, ANR-ERMUNDY and IDEX ANR-10-IDEX-0001-02 PSL*. BG was supported by Russian Science Foundation grant (Contract No. 17- 11-01273). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.