Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses

Neuron. 2009 Nov 12;64(3):391-403. doi: 10.1016/j.neuron.2009.10.021.

Abstract

Afferent activity can induce fast, feed-forward changes in synaptic efficacy that are synapse specific. Using combined electrophysiology, caged molecule photolysis, and Ca(2+) imaging, we describe a plasticity in which the recruitment of astrocytes in response to afferent activity causes a fast and feed-forward, yet distributed increase in the amplitude of quantal synaptic currents at multiple glutamate synapses on magnocellular neurosecretory cells in the hypothalamic paraventricular nucleus. The plasticity is largely multiplicative, consistent with a proportional increase or "scaling" in the strength of all synapses on the neuron. This effect requires a metabotropic glutamate receptor-mediated rise in Ca(2+) in the astrocyte processes surrounding the neuron and the release of the gliotransmitter ATP, which acts on postsynaptic purinergic receptors. These data provide evidence for a form of distributed synaptic plasticity that is feed-forward, expressed quickly, and mediated by the synaptic activation of neighboring astrocytes.

Publication types

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

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Astrocytes / physiology*
  • Calcium / metabolism
  • Cell Communication / physiology
  • Excitatory Postsynaptic Potentials / physiology
  • Glutamic Acid / metabolism*
  • In Vitro Techniques
  • Inositol 1,4,5-Trisphosphate Receptors / metabolism
  • Male
  • Neuronal Plasticity / physiology*
  • Neurons / physiology*
  • Neurosecretory Systems / physiology
  • Paraventricular Hypothalamic Nucleus / physiology*
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Metabotropic Glutamate / metabolism
  • Receptors, Purinergic / metabolism
  • Synapses / physiology*
  • Synaptic Potentials / physiology
  • Synaptic Transmission / physiology

Substances

  • Inositol 1,4,5-Trisphosphate Receptors
  • Receptors, Metabotropic Glutamate
  • Receptors, Purinergic
  • Glutamic Acid
  • Adenosine Triphosphate
  • Calcium