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The Journal of Neuroscience, June 9, 2004, 24(23):5370-5380; doi:10.1523/JNEUROSCI.1219-04.2004
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Behavioral/Systems/Cognitive
Identification of Sympathetic Premotor Neurons in Medullary Raphe Regions Mediating Fever and Other Thermoregulatory Functions
Kazuhiro Nakamura,1 Kiyoshi Matsumura,2 Thomas Hübschle,4 Yoshiko Nakamura,2 Hiroyuki Hioki,1 Fumino Fujiyama,1 Zsolt Boldogköi,6 Matthias König,5 Heinz-Jürgen Thiel,5 Rüdiger Gerstberger,4 Shigeo Kobayashi,2 andTakeshi Kaneko1,3 1Department of Morphological Brain Science, Graduate School of Medicine, 2Department of Intelligence Science and Technology, Graduate School of Informatics, and 3Core Research for Evolution Science and Technology, Japan Science and Technology, Kyoto University, Kyoto 606-8501, Japan, Institutes of 4Veterinary-Physiology and 5Virology, Justus-Liebig-University, D-35392 Giessen, Germany, and 6Department of Medical Biology, Faculty of Medicine, University of Szeged, Szeged H-6720, Hungary
Sympathetic premotor neurons directly control sympathetic preganglionic neurons (SPNs) in the intermediolateral cell column (IML) of the thoracic spinal cord, and many of these premotor neurons are localized in the medulla oblongata. The rostral ventrolateral medulla contains premotor neurons controlling the cardiovascular conditions, whereas rostral medullary raphe regions are a candidate source of sympathetic premotor neurons for thermoregulatory functions. Here, we show that these medullary raphe regions contain putative glutamatergic neurons and that these neurons directly control thermoregulatory SPNs. Neurons expressing vesicular glutamate transporter 3 (VGLUT3) were distributed in the rat medullary raphe regions, including the raphe magnus and rostral raphe pallidus nuclei, and mostly lacked serotonin immunoreactivity. These VGLUT3-positive neurons expressed Fos in response to cold exposure or to central administration of prostaglandin E2, a pyrogenic mediator. Transneuronal retrograde labeling after inoculation of pseudorabies virus into the interscapular brown adipose tissue (BAT) or the tail indicated that those VGLUT3-expressing medullary raphe neurons innervated these thermoregulatory effector organs multisynaptically through SPNs of specific thoracic segments, and microinjection of glutamate into the IML of the BAT-controlling segments produced BAT thermogenesis. An anterograde tracing study further showed a direct projection of those VGLUT3-expressing medullary raphe neurons to the dendrites of SPNs. Furthermore, intra-IML application of glutamate receptor antagonists blocked BAT thermogenesis triggered by disinhibition of the medullary raphe regions. The present results suggest that VGLUT3-expressing neurons in the medullary raphe regions constitute excitatory neurons that could be categorized as a novel group of sympathetic premotor neurons for thermoregulatory functions, including fever.
Key words: fever; glutamate; premotor neuron; prostaglandin E2; raphe; sympathetic nervous system; thermoregulation; vesicular glutamate transporter
Received April 1, 2004; revised April 30, 2004; accepted May 3, 2004.
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