Integration, coincidence detection and resonance in networks of spiking neurons expressing Gamma oscillations and asynchronous states

PLoS Comput Biol. 2021 Sep 16;17(9):e1009416. doi: 10.1371/journal.pcbi.1009416. eCollection 2021 Sep.

Abstract

Gamma oscillations are widely seen in the awake and sleeping cerebral cortex, but the exact role of these oscillations is still debated. Here, we used biophysical models to examine how Gamma oscillations may participate to the processing of afferent stimuli. We constructed conductance-based network models of Gamma oscillations, based on different cell types found in cerebral cortex. The models were adjusted to extracellular unit recordings in humans, where Gamma oscillations always coexist with the asynchronous firing mode. We considered three different mechanisms to generate Gamma, first a mechanism based on the interaction between pyramidal neurons and interneurons (PING), second a mechanism in which Gamma is generated by interneuron networks (ING) and third, a mechanism which relies on Gamma oscillations generated by pacemaker chattering neurons (CHING). We find that all three mechanisms generate features consistent with human recordings, but that the ING mechanism is most consistent with the firing rate change inside Gamma bursts seen in the human data. We next evaluated the responsiveness and resonant properties of these networks, contrasting Gamma oscillations with the asynchronous mode. We find that for both slowly-varying stimuli and precisely-timed stimuli, the responsiveness is generally lower during Gamma compared to asynchronous states, while resonant properties are similar around the Gamma band. We could not find conditions where Gamma oscillations were more responsive. We therefore predict that asynchronous states provide the highest responsiveness to external stimuli, while Gamma oscillations tend to overall diminish responsiveness.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Cerebral Cortex / cytology
  • Cerebral Cortex / physiology
  • Computational Biology
  • Computer Simulation
  • Gamma Rhythm / physiology*
  • Humans
  • Interneurons / physiology
  • Models, Neurological*
  • Nerve Net / cytology
  • Nerve Net / physiology
  • Neural Networks, Computer
  • Neurons / physiology*
  • Pyramidal Cells / physiology

Grants and funding

A.D was supported by the Centre National de la Recherche Scientifique (CNRS) and the European Community (Human Brain Project, H2020-785907). E.S. acknowledges a PhD fellowship from the École des Neurosciences de Paris (ENP) and from the Fondation pour la Recherche Médicale (FRM) - grant FDT202012010566 - and the financial support from La Fondation des Treilles. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. CNRS: www.cnrs.fr Human Brain Project: www.humanbrainproject.eu ENP: www.paris-neuroscience.fr FRM: www.frm.org La Fondation des Treilles: https://www.les-treilles.com/la-recherche/le-prix-jeune-chercheur/.