Anterograde transneuronal viral tract tracing reveals central sensory circuits from brown fat and sensory denervation alters its thermogenic responses

Brown adipose tissue (BAT) thermogenic activity and growth are controlled by its sympathetic nervous system (SNS) innervation, but nerve fibers containing sensory-associated neuropeptides [substance P, calcitonin gene-related peptide (CGRP)] also suggest sensory innervation. The central nervous syst...

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Veröffentlicht in:American journal of physiology. Regulatory, integrative and comparative physiology integrative and comparative physiology, 2012-05, Vol.302 (9), p.R1049-R1058
Hauptverfasser: Vaughan, Cheryl H, Bartness, Timothy J
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container_title American journal of physiology. Regulatory, integrative and comparative physiology
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creator Vaughan, Cheryl H
Bartness, Timothy J
description Brown adipose tissue (BAT) thermogenic activity and growth are controlled by its sympathetic nervous system (SNS) innervation, but nerve fibers containing sensory-associated neuropeptides [substance P, calcitonin gene-related peptide (CGRP)] also suggest sensory innervation. The central nervous system (CNS) projections of BAT afferents are unknown. Therefore, we used the H129 strain of the herpes simplex virus-1 (HSV-1), an anterograde transneuronal viral tract tracer used to delineate sensory nerve circuits, to define these projections. HSV-1 was injected into interscapular BAT (IBAT) of Siberian hamsters and HSV-1 immunoreactivity (ir) was assessed 24, 48, 72, 96, and 114 h postinjection. The 96- and 114-h groups had the most HSV-1-ir neurons with marked infections in the hypothalamic paraventricular nucleus, periaqueductal gray, olivary areas, parabrachial nuclei, raphe nuclei, and reticular areas. These sites also are involved in sympathetic outflow to BAT suggesting possible BAT sensory-SNS thermogenesis feedback circuits. We tested the functional contribution of IBAT sensory innervation on thermogenic responses to an acute (24 h) cold exposure test by injecting the specific sensory nerve toxin capsaicin directly into IBAT pads and then measuring core (T(c)) and IBAT (T(IBAT)) temperature responses. CGRP content was significantly decreased in capsaicin-treated IBAT demonstrating successful sensory nerve destruction. T(IBAT) and T(c) were significantly decreased in capsaicin-treated hamsters compared with the saline controls at 2 h of cold exposure. Thus the central sensory circuits from IBAT have been delineated for the first time, and impairment of sensory feedback from BAT appears necessary for the appropriate, initial thermogenic response to acute cold exposure.
doi_str_mv 10.1152/ajpregu.00640.2011
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Regulatory, integrative and comparative physiology</jtitle><addtitle>Am J Physiol Regul Integr Comp Physiol</addtitle><date>2012-05-01</date><risdate>2012</risdate><volume>302</volume><issue>9</issue><spage>R1049</spage><epage>R1058</epage><pages>R1049-R1058</pages><issn>0363-6119</issn><eissn>1522-1490</eissn><coden>AJPRDO</coden><abstract>Brown adipose tissue (BAT) thermogenic activity and growth are controlled by its sympathetic nervous system (SNS) innervation, but nerve fibers containing sensory-associated neuropeptides [substance P, calcitonin gene-related peptide (CGRP)] also suggest sensory innervation. The central nervous system (CNS) projections of BAT afferents are unknown. Therefore, we used the H129 strain of the herpes simplex virus-1 (HSV-1), an anterograde transneuronal viral tract tracer used to delineate sensory nerve circuits, to define these projections. HSV-1 was injected into interscapular BAT (IBAT) of Siberian hamsters and HSV-1 immunoreactivity (ir) was assessed 24, 48, 72, 96, and 114 h postinjection. The 96- and 114-h groups had the most HSV-1-ir neurons with marked infections in the hypothalamic paraventricular nucleus, periaqueductal gray, olivary areas, parabrachial nuclei, raphe nuclei, and reticular areas. These sites also are involved in sympathetic outflow to BAT suggesting possible BAT sensory-SNS thermogenesis feedback circuits. We tested the functional contribution of IBAT sensory innervation on thermogenic responses to an acute (24 h) cold exposure test by injecting the specific sensory nerve toxin capsaicin directly into IBAT pads and then measuring core (T(c)) and IBAT (T(IBAT)) temperature responses. CGRP content was significantly decreased in capsaicin-treated IBAT demonstrating successful sensory nerve destruction. T(IBAT) and T(c) were significantly decreased in capsaicin-treated hamsters compared with the saline controls at 2 h of cold exposure. Thus the central sensory circuits from IBAT have been delineated for the first time, and impairment of sensory feedback from BAT appears necessary for the appropriate, initial thermogenic response to acute cold exposure.</abstract><cop>United States</cop><pub>American Physiological Society</pub><pmid>22378771</pmid><doi>10.1152/ajpregu.00640.2011</doi><oa>free_for_read</oa></addata></record>
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subjects Adipose Tissue, Brown - innervation
Adipose Tissue, Brown - physiology
Adrenergic Fibers - physiology
Afferent Pathways - anatomy & histology
Afferent Pathways - physiology
Animals
Cricetinae
Denervation
Heat
Herpes viruses
Herpesvirus 1, Human
Nervous system
Obesity, Diabetes and Energy Homeostasis
Peptides
Physiology
Rodents
Sympathectomy
Sympathetic Nervous System - anatomy & histology
Sympathetic Nervous System - physiology
Sympathetic Nervous System - virology
Thermogenesis - physiology
Thermosensing - physiology
Tissues
title Anterograde transneuronal viral tract tracing reveals central sensory circuits from brown fat and sensory denervation alters its thermogenic responses
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