Gap junction coupling confers isopotentiality on astrocyte syncytium

Glia. 2016 Feb;64(2):214-26. doi: 10.1002/glia.22924. Epub 2015 Oct 5.

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.

Keywords: K+ clearance; coupling coefficient; electrical coupling; membrane potential.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Astrocytes / physiology*
  • Cations, Monovalent / metabolism
  • Cells, Cultured
  • Extracellular Space / metabolism
  • Female
  • Gap Junctions / physiology*
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Hippocampus / physiology
  • Humans
  • Male
  • Membrane Potentials / physiology*
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neural Pathways / physiology
  • Potassium / metabolism
  • Tissue Culture Techniques

Substances

  • Cations, Monovalent
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • Potassium