Two forms of astrocyte calcium excitability have distinct effects on NMDA receptor-mediated slow inward currents in pyramidal neurons

J Neurosci. 2008 Jun 25;28(26):6659-63. doi: 10.1523/JNEUROSCI.1717-08.2008.

Abstract

Astrocytes display excitability in the form of intracellular calcium concentration ([Ca(2+)](i)) increases, but the signaling impact of these for neurons remains debated and controversial. A key unresolved issue is whether astrocyte [Ca(2+)](i) elevations impact neurons or not. Here we report that in the CA1 region of the hippocampus, agonists of native P2Y(1) and PAR-1 receptors, which are preferentially expressed in astrocytes, equally elevated [Ca(2+)](i) levels without affecting the passive membrane properties of pyramidal neurons. However, under conditions chosen to isolate NMDA receptor responses, we found that activation of PAR-1 receptors led to the appearance of NMDA receptor-mediated slow inward currents (SICs) in pyramidal neurons. In stark contrast, activation of P2Y(1) receptors was ineffective in this regard. The PAR-1 receptor-mediated increased SICs were abolished by several strategies that selectively impaired astrocyte [Ca(2+)](i) excitability and function. Our studies therefore indicate that evoked astrocyte [Ca(2+)](i) transients are not a binary signal for interactions with neurons, and that astrocytes result in neuronal NMDA receptor-mediated SICs only when appropriately excited. The data thus provide a basis to rationalize recent contradictory data on astrocyte-neuron interactions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / cytology
  • Astrocytes / drug effects
  • Astrocytes / metabolism*
  • Calcium / metabolism
  • Calcium Signaling / physiology*
  • Cell Communication / drug effects
  • Cell Communication / physiology
  • Glutamic Acid / metabolism*
  • Hippocampus / cytology
  • Hippocampus / metabolism*
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Organ Culture Techniques
  • Purinergic P2 Receptor Agonists
  • Pyramidal Cells / cytology
  • Pyramidal Cells / drug effects
  • Pyramidal Cells / metabolism*
  • Receptor, PAR-1 / agonists
  • Receptor, PAR-1 / metabolism
  • Receptors, N-Methyl-D-Aspartate / drug effects
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Receptors, Purinergic P2 / metabolism
  • Receptors, Purinergic P2Y1
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / physiology
  • Time Factors

Substances

  • P2ry1 protein, mouse
  • Purinergic P2 Receptor Agonists
  • Receptor, PAR-1
  • Receptors, N-Methyl-D-Aspartate
  • Receptors, Purinergic P2
  • Receptors, Purinergic P2Y1
  • Glutamic Acid
  • Calcium