TRPV1 marks synaptic segregation of multiple convergent afferents at the rat medial solitary tract nucleus

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

doi:10.1371/journal.pone.0025015

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TRPV1 marks synaptic segregation of multiple convergent afferents at the rat medial solitary tract nucleus

Journal article

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TRPV1 marks synaptic segregation of multiple convergent afferents at the rat medial solitary tract nucleus

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

PloS one, Vol.6(9), pp.e25015-e25015

2011

DOI: https://doi.org/10.1371/journal.pone.0025015

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https://hdl.handle.net/2376/104834

PMCID: PMC3176783

PMID: 21949835

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Abstract

Receptors, Glutamate - metabolism

Electric Stimulation

Capsaicin - pharmacology

Brain Stem - metabolism

Rats

Male

Neurons - cytology

Brain Stem - cytology

Rats, Sprague-Dawley

Brain Stem - drug effects

Sensory System Agents - pharmacology

Excitatory Postsynaptic Potentials - physiology

TRPV Cation Channels - metabolism

Patch-Clamp Techniques

Animals

Synaptic Transmission - drug effects

Afferent Pathways - drug effects

Glutamic Acid - metabolism

Neurons - metabolism

Visceral Afferents - drug effects

Neurons - drug effects

Solitary Nucleus - metabolism

Solitary Nucleus - cytology

TRPV1 receptors are expressed on most but not all central terminals of cranial visceral afferents in the caudal solitary tract nucleus (NTS). TRPV1 is associated with unmyelinated C-fiber afferents. Both TRPV1+ and TRPV1- afferents enter NTS but their precise organization remains poorly understood. In horizontal brainstem slices, we activated solitary tract (ST) afferents and recorded ST-evoked glutamatergic excitatory synaptic currents (ST-EPSCs) under whole cell voltage clamp conditions from neurons of the medial subnucleus. Electrical shocks to the ST produced fixed latency EPSCs (jitter<200 µs) that identified direct ST afferent innervation. Graded increases in shock intensity often recruited more than one ST afferent and ST-EPSCs had consistent threshold intensity, latency to onset, and unique EPSC waveforms that characterized each unitary ST afferent contact. The TRPV1 agonist capsaicin (100 nM) blocked the evoked TRPV1+ ST-EPSCs and defined them as either TRPV1+ or TRPV1- inputs. No partial responses to capsaicin were observed so that in NTS neurons that received one or multiple (2-5) direct ST afferent inputs--all were either blocked by capsaicin or were unaltered. Since TRPV1 mediates asynchronous release following TRPV1+ ST-evoked EPSCs, we likewise found that recruiting more than one ST afferent further augmented the asynchronous response and was eliminated by capsaicin. Thus, TRPV1+ and TRPV1- afferents are completely segregated to separate NTS neurons. As a result, the TRPV1 receptor augments glutamate release only within unmyelinated afferent pathways in caudal medial NTS and our work indicates a complete separation of C-type from A-type afferent information at these first central neurons.

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Title: TRPV1 marks synaptic segregation of multiple convergent afferents at the rat medial solitary tract nucleus
Creators: James H Peters - Department of Physiology and Pharmacology, Oregon Health & Science University, Portland, Oregon, United States of America
Stuart J McDougall
Jessica A Fawley
Michael C Andresen
Publication Details: PloS one, Vol.6(9), pp.e25015-e25015
Academic Unit: Integrative Physiology and Neuroscience, Department of
Publisher: United States
Grant note: R01 HL105703 / NHLBI NIH HHS HL-88894 / NHLBI NIH HHS R01 HL041119 / NHLBI NIH HHS HL-41119 / NHLBI NIH HHS F32 HL088894 / NHLBI NIH HHS HL-105703 / NHLBI NIH HHS
Identifiers: 99900546846901842
Language: English
Resource Type: Journal article