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

James H Peters; Stuart J McDougall; Jessica A Fawley; Stephen M Smith; Michael C Andresen

doi:10.1016/j.neuron.2010.02.017

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

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

James H Peters, Stuart J McDougall, Jessica A Fawley, Stephen M Smith and Michael C Andresen

Neuron (Cambridge, Mass.), Vol.65(5), pp.657-669

2010

DOI: https://doi.org/10.1016/j.neuron.2010.02.017

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https://hdl.handle.net/2376/104793

PMCID: PMC2837850

PMID: 20223201

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Abstract

MOLNEURO

SIGNALING

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. ► Activity in TRPV1+, but not TRPV1−, afferents triggered asynchronous glutamate release ► Synchronous glutamate release properties were indistinguishable across all afferents ► TRPV1 antagonists and low temperature selectively blocked asynchronous release ► TPRV1 mediates tonic signaling and an activity-extending synaptic facilitation

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Title: Primary Afferent Activation of Thermosensitive TRPV1 Triggers Asynchronous Glutamate Release at Central Neurons
Creators: James H Peters - Department of Physiology and Pharmacology, Oregon Health & Science University, Portland, OR 97239, USA
Stuart J McDougall - Department of Physiology and Pharmacology, Oregon Health & Science University, Portland, OR 97239, USA
Jessica A Fawley - Department of Physiology and Pharmacology, Oregon Health & Science University, Portland, OR 97239, USA
Stephen M Smith - Division of Pulmonary and Critical Care Medicine, Oregon Health & Science University, Portland, OR 97239, USA
Michael C Andresen - Department of Physiology and Pharmacology, Oregon Health & Science University, Portland, OR 97239, USA
Publication Details: Neuron (Cambridge, Mass.), Vol.65(5), pp.657-669
Academic Unit: Integrative Physiology and Neuroscience, Department of
Publisher: Elsevier Inc
Identifiers: 99900546879101842
Language: English
Resource Type: Journal article