Phase-locking patterns underlying effective communication in exact firing rate models of neural networks

PLoS Comput Biol. 2022 May 18;18(5):e1009342. doi: 10.1371/journal.pcbi.1009342. eCollection 2022 May.

Abstract

Macroscopic oscillations in the brain have been observed to be involved in many cognitive tasks but their role is not completely understood. One of the suggested functions of the oscillations is to dynamically modulate communication between neural circuits. The Communication Through Coherence (CTC) theory proposes that oscillations reflect rhythmic changes in excitability of the neuronal populations. Thus, populations need to be properly phase-locked so that input volleys arrive at the peaks of excitability of the receiving population to communicate effectively. Here, we present a modeling study to explore synchronization between neuronal circuits connected with unidirectional projections. We consider an Excitatory-Inhibitory (E-I) network of quadratic integrate-and-fire neurons modeling a Pyramidal-Interneuronal Network Gamma (PING) rhythm. The network receives an external periodic input from either one or two sources, simulating the inputs from other oscillating neural groups. We use recently developed mean-field models which provide an exact description of the macroscopic activity of the spiking network. This low-dimensional mean field model allows us to use tools from bifurcation theory to identify the phase-locked states between the input and the target population as a function of the amplitude, frequency and coherence of the inputs. We identify the conditions for optimal phase-locking and effective communication. We find that inputs with high coherence can entrain the network for a wider range of frequencies. Besides, faster oscillatory inputs than the intrinsic network gamma cycle show more effective communication than inputs with similar frequency. Our analysis further shows that the entrainment of the network by inputs with higher frequency is more robust to distractors, thus giving them an advantage to entrain the network and communicate effectively. Finally, we show that pulsatile inputs can switch between attended inputs in selective attention.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Communication
  • Models, Neurological*
  • Neural Networks, Computer*
  • Neurons / physiology

Grants and funding

Work produced with the support of a 2019 Leonardo Grant for Researchers and Cultural Creators, BBVA Foundation (DR, GH). GH also acknowledges support from the Spanish State Research Agency, through the MINECO-FEDER Grant PGC2018-098676-B-100 (AEI/FEDER/UE), the RyC grant RYC-2014-15866 and the Maria de Maeztu Award for Centers and Units of Excellence in R&D (CEX2020-001084-M). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.