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PMID: 20223201 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Primary afferent activation of thermosensitive TRPV1 triggers asynchronous glutamate release at central neurons.

Neuron ·Vol. 65 ·No. 5 ·2010-03-11 ·Pages 657-69

Peters JH, McDougall SJ, Fawley JA, Smith SM, Andresen MC

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.

MeSH Terms
Afferent Pathways/physiology Anilides/pharmacology Animals Capsaicin/pharmacology Cinnamates/pharmacology Electric Stimulation/methods Excitatory Postsynaptic Potentials/drug effects,physiology Glutamic Acid/metabolism In Vitro Techniques Male Neurons/classification,drug effects,metabolism Patch-Clamp Techniques/methods Rats Rats, Sprague-Dawley Sensory System Agents/pharmacology Solitary Nucleus/cytology TRPV Cation Channels/antagonists & inhibitors,metabolism Thermosensing/drug effects,physiology
Chemicals
Anilides Cinnamates N-(3-methoxyphenyl)-4-chlorocinnamanilide Sensory System Agents TRPV Cation Channels Trpv1 protein, rat Glutamic Acid Capsaicin
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Peters James H
Department of Physiology and Pharmacology, Oregon Health & Science University, Portland, OR 97239, USA.
McDougall Stuart J
Fawley Jessica A
Smith Stephen M
Andresen Michael C
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Article Info
Journal
Neuron
Abbr.
Neuron
ISSN
1097-4199
DOI
10.1016/j.neuron.2010.02.017
Published
2010-03-11
Pages
657-69
Language
English
Region
United States
NLM ID
8809320
PMCID
PMC2837850
Subset
IM
Grants
NHLBI NIH HHS · R01 HL041119-19 · United States
NHLBI NIH HHS · R01 HL083115-02 · United States
NHLBI NIH HHS · R01 HL041119 · United States
NHLBI NIH HHS · R01 HL083115-01 · United States
NHLBI NIH HHS · R01 HL041119-18 · United States
NHLBI NIH HHS · F32 HL088894 · United States
NHLBI NIH HHS · R01 HL083115-03 · United States
NHLBI NIH HHS · R01 HL083115-04 · United States
NHLBI NIH HHS · R01 HL041119-16 · United States
NHLBI NIH HHS · R01 HL041119-17 · United States
NHLBI NIH HHS · R01 HL083115 · United States
NHLBI NIH HHS · R01 HL105703 · United States
NHLBI NIH HHS · R01 HL041119-15 · United States
External Links
PubMed source DOI: 10.1016/j.neuron.2010.02.017 PMC Full Text View journal details
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