Gap junction coupling confers isopotentiality on astrocyte syncytium

Baofeng Ma, Richard Buckalew, Yixing Du, Conrad M. Kiyoshi, Catherine C. Alford, Wei Wang, Dana M. Mctigue, John J. Enyeart, David Terman, Min Zhou

Research output: Contribution to journalArticlepeer-review

73 Scopus citations

Abstract

Astrocytes are extensively coupled through gap junctions into a syncytium. However, the basic role of this major brain network remains largely unknown. Using electrophysiological and computational modeling methods, we demonstrate that the membrane potential (VM) of an individual astrocyte in a hippocampal syncytium, but not in a single, freshly isolated cell preparation, can be well-maintained at quasi-physiological levels when recorded with reduced or K+ free pipette solutions that alter the K+ equilibrium potential to non-physiological voltages. We show that an astrocyte's associated syncytium provides powerful electrical coupling, together with ionic coupling at a lesser extent, that equalizes the astrocyte's VM to levels comparable to its neighbors. Functionally, this minimizes VM depolarization attributable to elevated levels of local extracellular K+ and thereby maintains a sustained driving force for highly efficient K+ uptake. Thus, gap junction coupling functions to achieve isopotentiality in astrocytic networks, whereby a constant extracellular environment can be powerfully maintained for crucial functions of neural circuits.

Original languageEnglish (US)
Pages (from-to)214-226
Number of pages13
JournalGlia
Volume64
Issue number2
DOIs
StatePublished - Feb 1 2016

Bibliographical note

Funding Information:
National Institute of Neurological Disorders and Stroke; Grant numbers: RO1NS062784 (to M.Z.), RO1NS043246 (to D.D.M.); Grant sponsor: The Ohio State University College of Medicine (to M.Z.).; Grant sponsor: National Science Foundation; Grant numbers: DMS 1410935 (to D.T.) and DMS 0931642 (to the Mathematical Biosciences Institute). The authors thank Drs. Harold K. Kimelberg and Maiken Nedergaard for critical comments on the manuscript. They thank Dr. Bruce R. Ransom for providing insightful comments and suggestions for manuscript improvement during revision.

Publisher Copyright:
© 2016 Wiley Periodicals, Inc.

Keywords

  • Coupling coefficient
  • Electrical coupling
  • K clearance
  • Membrane potential

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