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

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

Pulmonary and Critical Care Medicine

Research output: Contribution to journal › Article › peer-review

149 Scopus citations

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 language	English (US)
Pages (from-to)	657-669
Number of pages	13
Journal	Neuron
Volume	65
Issue number	5
DOIs	https://doi.org/10.1016/j.neuron.2010.02.017
State	Published - Mar 11 2010

Keywords

MOLNEURO
SIGNALING

ASJC Scopus subject areas

General Neuroscience

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title = "Primary Afferent Activation of Thermosensitive TRPV1 Triggers Asynchronous Glutamate Release at Central Neurons",

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.",

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author = "Peters, {James H.} and McDougall, {Stuart J.} and Fawley, {Jessica A.} and Smith, {Stephen M.} and Andresen, {Michael C.}",

note = "Funding Information: We thank Craig Jahr for comments on an early version of the manuscript. J.H.P., J.A.F., S.M.S., and M.C.A. are funded by the National Institutes of Health, U.S.A. S.J.M. is funded by the National Health and Medical Research Council of Australia. The authors declare no competing financial interests. ",

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AU - Smith, Stephen M.

AU - Andresen, Michael C.

N1 - Funding Information: We thank Craig Jahr for comments on an early version of the manuscript. J.H.P., J.A.F., S.M.S., and M.C.A. are funded by the National Institutes of Health, U.S.A. S.J.M. is funded by the National Health and Medical Research Council of Australia. The authors declare no competing financial interests.

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N2 - 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.

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

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