Criticality enhances the multilevel reliability of stimulus responses in cortical neural networks

Junhao Liang, Changsong Zhou*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Cortical neural networks exhibit high internal variability in spontaneous dynamic activities and they can robustly and reliably respond to external stimuli with multilevel features–from microscopic irregular spiking of neurons to macroscopic oscillatory local field potential. A comprehensive study integrating these multilevel features in spontaneous and stimulus–evoked dynamics with seemingly distinct mechanisms is still lacking. Here, we study the stimulus–response dynamics of biologically plausible excitation–inhibition (E–I) balanced networks. We confirm that networks around critical synchronous transition states can maintain strong internal variability but are sensitive to external stimuli. In this dynamical region, applying a stimulus to the network can reduce the trial-to-trial variability and shift the network oscillatory frequency while preserving the dynamical criticality. These multilevel features widely observed in different experiments cannot simultaneously occur in non-critical dynamical states. Furthermore, the dynamical mechanisms underlying these multilevel features are revealed using a semi-analytical mean-field theory that derives the macroscopic network field equations from the microscopic neuronal networks, enabling the analysis by nonlinear dynamics theory and linear noise approximation. The generic dynamical principle revealed here contributes to a more integrative understanding of neural systems and brain functions and incorporates multimodal and multilevel experimental observations. The E–I balanced neural network in combination with the effective mean-field theory can serve as a mechanistic modeling framework to study the multilevel neural dynamics underlying neural information and cognitive processes.

Original languageEnglish
Article numbere1009848
Number of pages27
JournalPLoS Computational Biology
Volume18
Issue number1
DOIs
Publication statusPublished - Jan 2022

Scopus Subject Areas

  • Genetics
  • Ecology, Evolution, Behavior and Systematics
  • Cellular and Molecular Neuroscience
  • Molecular Biology
  • Ecology
  • Computational Theory and Mathematics
  • Modelling and Simulation

User-Defined Keywords

  • Action Potentials/physiology
  • Cerebral Cortex/physiology
  • Humans
  • Nerve Net/physiology
  • Nonlinear Dynamics
  • Reaction Time
  • Reproducibility of Results

Fingerprint

Dive into the research topics of 'Criticality enhances the multilevel reliability of stimulus responses in cortical neural networks'. Together they form a unique fingerprint.

Cite this