Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses.
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.
Gordon
Grant R J
GR
Hotchkiss Brain Institute, Department of Physiology and Pharmacology, University of Calgary, Calgary, AB, Canada.
Iremonger
Karl J
KJ
Kantevari
Srinivas
S
Ellis-Davies
Graham C R
GC
MacVicar
Brian A
BA
Bains
Jaideep S
JS
D000255:Adenosine Triphosphate / Q000378:metabolism; D000818:Animals; D001253:Astrocytes / Q000502:physiology*; D002118:Calcium / Q000378:metabolism; D002450:Cell Communication / Q000502:physiology; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology; D018698:Glutamic Acid / Q000378:metabolism*; D066298:In Vitro Techniques; D053496:Inositol 1,4,5-Trisphosphate Receptors / Q000378:metabolism; D008297:Male; D009473:Neuronal Plasticity / Q000502:physiology*; D009474:Neurons / Q000502:physiology*; D009490:Neurosecretory Systems / Q000502:physiology; D010286:Paraventricular Hypothalamic Nucleus / Q000502:physiology*; D051381:Rats; D017207:Rats, Sprague-Dawley; D018094:Receptors, Metabotropic Glutamate / Q000378:metabolism; D011983:Receptors, Purinergic / Q000378:metabolism; D013569:Synapses / Q000502:physiology*; D055366:Synaptic Potentials / Q000502:physiology; D009435:Synaptic Transmission / Q000502:physiology
D053496:Inositol 1,4,5-Trisphosphate Receptors; D018094:Receptors, Metabotropic Glutamate; D011983:Receptors, Purinergic; D018698:Glutamic Acid; D000255:Adenosine Triphosphate; D002118:Calcium