Dynamic electrical synapses rewire brain networks for persistent oscillations and epileptogenesis

Ya Chin Yang*, Guan Hsun Wang, Ping Chou, Shu Wei Hsueh, Yi Chen Lai, Chung Chin Kuo*

*Corresponding author for this work

Research output: Contribution to journalJournal Article peer-review

Abstract

One of the very fundamental attributes for telencephalic neural computation in mammals involves network activities oscillating beyond the initial trigger. The continuing and automated processing of transient inputs shall constitute the basis of cognition and intelligence but may lead to neuropsychiatric disorders such as epileptic seizures if carried so far as to engross part of or the whole telencephalic system. From a conventional view of the basic design of the telencephalic local circuitry, the GABAergic interneurons (INs) and glutamatergic pyramidal neurons (PNs) make negative feedback loops which would regulate the neural activities back to the original state. The drive for the most intriguing self-perpetuating telencephalic activities, then, has not been posed and characterized. We found activity-dependent deployment and delineated functional consequences of the electrical synapses directly linking INs and PNs in the amygdala, a prototypical telencephalic circuitry. These electrical synapses endow INs dual (a faster excitatory and a slower inhibitory) actions on PNs, providing a network-intrinsic excitatory drive that fuels the IN-PN interconnected circuitries and enables persistent oscillations with preservation of GABAergic negative feedback. Moreover, the entities of electrical synapses between INs and PNs are engaged in and disengaged from functioning in a highly dynamic way according to neural activities, which then determine the spatiotemporal scale of recruited oscillating networks. This study uncovers a special wide-range and context-dependent plasticity for wiring/rewiring of brain networks. Epileptogenesis or a wide spectrum of clinical disorders may ensue, however, from different scales of pathological extension of this unique form of telencephalic plasticity.

Original languageEnglish
Article numbere2313042121
Pages (from-to)e2313042121
JournalProceedings of the National Academy of Sciences of the United States of America
Volume121
Issue number8
DOIs
StatePublished - 20 02 2024

Bibliographical note

Publisher Copyright:
Copyright © 2024 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

Keywords

  • cognition
  • context-dependent plasticity
  • epileptogenesis
  • gap junction
  • persistent oscillations
  • Brain
  • Interneurons/physiology
  • Humans
  • Synapses/physiology
  • Seizures/pathology
  • Electrical Synapses
  • Mammals
  • Animals
  • Epilepsy/pathology

Fingerprint

Dive into the research topics of 'Dynamic electrical synapses rewire brain networks for persistent oscillations and epileptogenesis'. Together they form a unique fingerprint.

Cite this