Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity

Neuron. 2007 May 24;54(4):611-26. doi: 10.1016/j.neuron.2007.04.032.

Abstract

Astrocytes are considered the third component of the synapse, responding to neurotransmitter release from synaptic terminals and releasing gliotransmitters--including glutamate--in a Ca(2+)-dependent manner to affect neuronal synaptic activity. Many studies reporting astrocyte-driven neuronal activity have evoked astrocyte Ca(2+) increases by application of endogenous ligands that directly activate neuronal receptors, making astrocyte contribution to neuronal effect(s) difficult to determine. We have made transgenic mice that express a Gq-coupled receptor only in astrocytes to evoke astrocyte Ca(2+) increases using an agonist that does not bind endogenous receptors in brain. By recording from CA1 pyramidal cells in acute hippocampal slices from these mice, we demonstrate that widespread Ca(2+) elevations in 80%-90% of stratum radiatum astrocytes do not increase neuronal Ca(2+), produce neuronal slow inward currents, or affect excitatory synaptic activity. Our findings call into question the developing consensus that Ca(2+)-dependent glutamate release by astrocytes directly affects neuronal synaptic activity in situ.

MeSH terms

  • Animals
  • Animals, Newborn
  • Astrocytes / metabolism*
  • Calcium / metabolism*
  • Cell Communication / physiology
  • Drug Interactions
  • Excitatory Postsynaptic Potentials / physiology
  • GTP-Binding Protein alpha Subunits, Gq-G11 / genetics
  • Green Fluorescent Proteins / genetics
  • Hippocampus / cytology
  • In Vitro Techniques
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neurotransmitter Agents / pharmacology
  • Oligopeptides / pharmacology
  • Patch-Clamp Techniques / methods
  • Phosphopyruvate Hydratase / metabolism
  • Presynaptic Terminals / drug effects
  • Presynaptic Terminals / physiology
  • Pyramidal Cells / cytology
  • Pyramidal Cells / physiology*
  • Receptors, G-Protein-Coupled / genetics
  • Synapses / physiology*
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / physiology*

Substances

  • MrgA1 protein, mouse
  • Neurotransmitter Agents
  • Oligopeptides
  • Receptors, G-Protein-Coupled
  • Green Fluorescent Proteins
  • phenylalanyl-leucyl-arginyl phenylalaninamide
  • GTP-Binding Protein alpha Subunits, Gq-G11
  • Phosphopyruvate Hydratase
  • Calcium