 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
The Journal of Neuroscience, June 9, 2004, 24(23):5370-5380; doi:10.1523/JNEUROSCI.1219-04.2004
Previous Article | Next Article
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.
This article has been cited by other articles:
C. J. Madden and S. F. Morrison
Endogenous activation of spinal 5-hydroxytryptamine (5-HT) receptors contributes to the thermoregulatory activation of brown adipose tissue
Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2010; 298(3): R776 - R783.
[Abstract] [Full Text] [PDF]
F. Seebacher
Responses to temperature variation: integration of thermoregulation and metabolism in vertebrates
J. Exp. Biol., September 15, 2009; 212(18): 2885 - 2891.
[Abstract] [Full Text] [PDF]
E. Kuramoto, T. Furuta, K. C. Nakamura, T. Unzai, H. Hioki, and T. Kaneko
Two Types of Thalamocortical Projections from the Motor Thalamic Nuclei of the Rat: A Single Neuron-Tracing Study Using Viral Vectors
Cereb Cortex, September 1, 2009; 19(9): 2065 - 2077.
[Abstract] [Full Text] [PDF]
A. A. Romanovsky, M. C. Almeida, A. Garami, A. A. Steiner, M. H. Norman, S. F. Morrison, K. Nakamura, J. J. Burmeister, and T. B. Nucci
The Transient Receptor Potential Vanilloid-1 Channel in Thermoregulation: A Thermosensor It Is Not
Pharmacol. Rev., September 1, 2009; 61(3): 228 - 261.
[Abstract] [Full Text] [PDF]
W. Matsuda, T. Furuta, K. C. Nakamura, H. Hioki, F. Fujiyama, R. Arai, and T. Kaneko
Single Nigrostriatal Dopaminergic Neurons Form Widely Spread and Highly Dense Axonal Arborizations in the Neostriatum
J. Neurosci., January 14, 2009; 29(2): 444 - 453.
[Abstract] [Full Text] [PDF]
E. Audero, E. Coppi, B. Mlinar, T. Rossetti, A. Caprioli, M. A. Banchaabouchi, R. Corradetti, and C. Gross
Sporadic Autonomic Dysregulation and Death Associated with Excessive Serotonin Autoinhibition
Science, July 4, 2008; 321(5885): 130 - 133.
[Abstract] [Full Text] [PDF]
J. A. Rathner, C. J. Madden, and S. F. Morrison
Central pathway for spontaneous and prostaglandin E2-evoked cutaneous vasoconstriction
Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2008; 295(1): R343 - R354.
[Abstract] [Full Text] [PDF]
S. F. Morrison, K. Nakamura, and C. J. Madden
Central control of thermogenesis in mammals
Exp Physiol, July 1, 2008; 93(7): 773 - 797.
[Abstract] [Full Text] [PDF]
H. Tsuchiya, T. Oka, K. Nakamura, A. Ichikawa, C. B. Saper, and Y. Sugimoto
Prostaglandin E2 Attenuates Preoptic Expression of GABAA Receptors via EP3 Receptors
J. Biol. Chem., April 18, 2008; 283(16): 11064 - 11071.
[Abstract] [Full Text] [PDF]
S. Thammacharoen, T. A. Lutz, N. Geary, and L. Asarian
Hindbrain Administration of Estradiol Inhibits Feeding and Activates Estrogen Receptor-{alpha}-Expressing Cells in the Nucleus Tractus Solitarius of Ovariectomized Rats
Endocrinology, April 1, 2008; 149(4): 1609 - 1617.
[Abstract] [Full Text] [PDF]
Y. Ootsuka, W. W. Blessing, A. A. Steiner, and A. A. Romanovsky
Fever response to intravenous prostaglandin E2 is mediated by the brain but does not require afferent vagal signaling
Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2008; 294(4): R1294 - R1303.
[Abstract] [Full Text] [PDF]
J. W. Brown, E. A. Sirlin, A. M. Benoit, J. M. Hoffman, and R. A. Darnall
Activation of 5-HT1A receptors in medullary raphe disrupts sleep and decreases shivering during cooling in the conscious piglet
Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2008; 294(3): R884 - R894.
[Abstract] [Full Text] [PDF]
T. J. Sajdyk, P. L. Johnson, R. J. Leitermann, S. D. Fitz, A. Dietrich, M. Morin, D. R. Gehlert, J. H. Urban, and A. Shekhar
Neuropeptide Y in the Amygdala Induces Long-Term Resilience to Stress-Induced Reductions in Social Responses But Not Hypothalamic-Adrenal-Pituitary Axis Activity or Hyperthermia
J. Neurosci., January 23, 2008; 28(4): 893 - 903.
[Abstract] [Full Text] [PDF]
D. K. Mulkey, D. L. Rosin, G. West, A. C. Takakura, T. S. Moreira, D. A. Bayliss, and P. G. Guyenet
Serotonergic Neurons Activate Chemosensitive Retrotrapezoid Nucleus Neurons by a pH-Independent Mechanism
J. Neurosci., December 19, 2007; 27(51): 14128 - 14138.
[Abstract] [Full Text] [PDF]
K. M. Hellman, T. S. Brink, and P. Mason
Activity of Murine Raphe Magnus Cells Predicts Tachypnea and On-Going Nociceptive Responsiveness
J Neurophysiol, December 1, 2007; 98(6): 3121 - 3133.
[Abstract] [Full Text] [PDF]
M. B. Dias, T. B. Nucci, L. O. Margatho, J. Antunes-Rodrigues, L. H. Gargaglioni, and L. G. S. Branco
Raphe magnus nucleus is involved in ventilatory but not hypothermic response to CO2
J Appl Physiol, November 1, 2007; 103(5): 1780 - 1788.
[Abstract] [Full Text] [PDF]
J. M. Hoffman, J. W. Brown, E. A. Sirlin, A. M. Benoit, W. H. Gill, M. B. Harris, and R. A. Darnall
Activation of 5-HT1A receptors in the paragigantocellularis lateralis decreases shivering during cooling in the conscious piglet
Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2007; 293(1): R518 - R527.
[Abstract] [Full Text] [PDF]
M. Tanaka, Y. Ootsuka, M. J. McKinley, and R. M. McAllen
Independent vasomotor control of rat tail and proximal hairy skin
J. Physiol., July 1, 2007; 582(1): 421 - 433.
[Abstract] [Full Text] [PDF]
J. L. Cham and E. Badoer
Cardiovascular Control: Exposure to a hot environment can activate spinally projecting and nitrergic neurones in the lower brainstem in the rat
Exp Physiol, May 1, 2007; 92(3): 529 - 540.
[Abstract] [Full Text] [PDF]
J. A. DiMicco and D. V. Zaretsky
The dorsomedial hypothalamus: a new player in thermoregulation
Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2007; 292(1): R47 - R63.
[Abstract] [Full Text] [PDF]
K. Nakamura and S. F. Morrison
Central efferent pathways mediating skin cooling-evoked sympathetic thermogenesis in brown adipose tissue
Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2007; 292(1): R127 - R136.
[Abstract] [Full Text] [PDF]
C. J. Madden and S. F. Morrison
Serotonin potentiates sympathetic responses evoked by spinal NMDA
J. Physiol., December 1, 2006; 577(2): 525 - 537.
[Abstract] [Full Text] [PDF]
A. Bartolomucci, G. La Corte, R. Possenti, V. Locatelli, A. E. Rigamonti, A. Torsello, E. Bresciani, I. Bulgarelli, R. Rizzi, F. Pavone, et al.
TLQP-21, a VGF-derived peptide, increases energy expenditure and prevents the early phase of diet-induced obesity
PNAS, September 26, 2006; 103(39): 14584 - 14589.
[Abstract] [Full Text] [PDF]
Y. Ootsuka and R. M. McAllen
Comparison between two rat sympathetic pathways activated in cold defense
Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2006; 291(3): R589 - R595.
[Abstract] [Full Text] [PDF]
M. Shibasaki, T. E. Wilson, and C. G. Crandall
Neural control and mechanisms of eccrine sweating during heat stress and exercise
J Appl Physiol, May 1, 2006; 100(5): 1692 - 1701.
[Abstract] [Full Text] [PDF]
N. Marina, M. Taheri, and M. P. Gilbey
Generation of a physiological sympathetic motor rhythm in the rat following spinal application of 5-HT
J. Physiol., March 1, 2006; 571(2): 441 - 450.
[Abstract] [Full Text] [PDF]
M. W. Nason Jr and P. Mason
Medullary Raphe Neurons Facilitate Brown Adipose Tissue Activation
J. Neurosci., January 25, 2006; 26(4): 1190 - 1198.
[Abstract] [Full Text] [PDF]
R. M. McAllen, M. Farrell, J. M. Johnson, D. Trevaks, L. Cole, M. J. McKinley, G. Jackson, D. A. Denton, and G. F. Egan
Human medullary responses to cooling and rewarming the skin: A functional MRI study
PNAS, January 17, 2006; 103(3): 809 - 813.
[Abstract] [Full Text] [PDF]
J. A. DiMicco and D. V. Zaretsky
The mysterious role of prostaglandin E2 in the medullary raphe: a hot topic or not?
Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2005; 289(6): R1589 - R1591.
[Full Text] [PDF]
Y. Ootsuka and R. M. McAllen
Interactive drives from two brain stem premotor nuclei are essential to support rat tail sympathetic activity
Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2005; 289(4): R1107 - R1115.
[Abstract] [Full Text] [PDF]
R. A. Darnall, M. B. Harris, W. H. Gill, J. M. Hoffman, J. W. Brown, and M. M. Niblock
Inhibition of Serotonergic Neurons in the Nucleus Paragigantocellularis Lateralis Fragments Sleep and Decreases Rapid Eye Movement Sleep in the Piglet: Implications for Sudden Infant Death Syndrome
J. Neurosci., September 7, 2005; 25(36): 8322 - 8332.
[Abstract] [Full Text] [PDF]
P. Mason
DECONSTRUCTING ENDOGENOUS PAIN MODULATIONS
J Neurophysiol, September 1, 2005; 94(3): 1659 - 1663.
[Abstract] [Full Text] [PDF]
Y. Ootsuka and W. W. Blessing
Activation of slowly conducting medullary raphe-spinal neurons, including serotonergic neurons, increases cutaneous sympathetic vasomotor discharge in rabbit
Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2005; 288(4): R909 - R918.
[Abstract] [Full Text] [PDF]
W. W. Blessing
BAT control shows the way: medullary raphe/parapyramidal neurons and sympathetic regulation of brown adipose tissue
Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2005; 288(3): R557 - R560.
[Full Text] [PDF]
|
|
|
|
 |
|