Primary Afferent Activation of Thermosensitive TRPV1 Triggers Asynchronous Glutamate Release at Central Neurons

James H. Peters, Stuart J. McDougall, Jessica A. Fawley, Stephen Smith, Michael Andresen

Research output: Contribution to journalArticle

116 Citations (Scopus)

Abstract

TRPV1 receptors feature prominently in nociception of spinal primary afferents but are also expressed in unmyelinated cranial visceral primary afferents linked to homeostatic regulation. Cranial visceral afferents enter the brain at the solitary tract nucleus (NTS) to control the heart, lungs, and other vital organs. Here we identify a role for central TRPV1 in the activity-dependent facilitation of glutamatergic transmission from solitary tract (ST) afferents. Fast, synchronous ST-NTS transmission from capsaicin-sensitive (TRPV1+) and -insensitive (TRPV1-) afferents was similar. However, afferent activation triggered long-lasting asynchronous glutamate release only from TRPV1+ synapses. Asynchronous release was proportional to synchronous EPSC amplitude, activity, and calcium entry. TRPV1 antagonists and low temperature blocked asynchronous release, but not evoked EPSCs. At physiological afferent frequencies, asynchronous release strongly potentiated the duration of postsynaptic spiking. This activity-dependent TPRV1-mediated facilitation is a form of synaptic plasticity that brings a unique central integrative feature to the CNS and autonomic regulation.

Original languageEnglish (US)
Pages (from-to)657-669
Number of pages13
JournalNeuron
Volume65
Issue number5
DOIs
StatePublished - Mar 11 2010

Fingerprint

Visceral Afferents
Glutamic Acid
Neurons
Neuronal Plasticity
Solitary Nucleus
Nociception
Capsaicin
Synapses
Calcium
Lung
Temperature
Brain

Keywords

  • MOLNEURO
  • SIGNALING

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Primary Afferent Activation of Thermosensitive TRPV1 Triggers Asynchronous Glutamate Release at Central Neurons. / Peters, James H.; McDougall, Stuart J.; Fawley, Jessica A.; Smith, Stephen; Andresen, Michael.

In: Neuron, Vol. 65, No. 5, 11.03.2010, p. 657-669.

Research output: Contribution to journalArticle

Peters, James H. ; McDougall, Stuart J. ; Fawley, Jessica A. ; Smith, Stephen ; Andresen, Michael. / Primary Afferent Activation of Thermosensitive TRPV1 Triggers Asynchronous Glutamate Release at Central Neurons. In: Neuron. 2010 ; Vol. 65, No. 5. pp. 657-669.
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