Central neural control of thermoregulation and brown adipose tissue

Autonomic Neuroscience: Basic and Clinical

Volumn 196, Issue , 2016, Pages 14-24

  Morrison, Shaun F ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Brown adipose tissue; Cutaneous vasoconstriction; Dorsomedial hypothalamus; Fever; Preoptic hypothalamus; Rostral raphe pallidus; Shiver; Sympathetic nerve activity; Thermogenesis

Indexed keywords

NEUROTRANSMITTER;

BRAIN TEMPERATURE; BROWN ADIPOSE TISSUE; CENTRAL NERVOUS SYSTEM; COOLING; HEAT LOSS; HUMAN; HYPOTHALAMUS; LATERAL HYPOTHALAMUS; NERVE CELL; NERVE TRACT; NONHUMAN; NUCLEUS RAPHE PALLIDUS; PARABRACHIAL NUCLEUS; PREOPTIC AREA; PRIORITY JOURNAL; REVIEW; ROSTRAL VENTROMEDIAL MEDULLA; SENSATION; SENSORIMOTOR INTEGRATION; SENSORY NERVE; SHIVERING; SWEATING; SYMPATHETIC NERVE; THERMOGENESIS; THERMOREGULATION; VASOCONSTRICTION; ADRENERGIC SYSTEM; ANIMAL; BODY TEMPERATURE; METABOLISM; PHYSIOLOGY;

ADIPOSE TISSUE, BROWN; ANIMALS; BODY TEMPERATURE; BODY TEMPERATURE REGULATION; HUMANS; NEURAL PATHWAYS; SYMPATHETIC NERVOUS SYSTEM; THERMOGENESIS;

EID: 84959092992     PISSN: 15660702     EISSN: 18727484     Source Type: Journal    
DOI: 10.1016/j.autneu.2016.02.010     Document Type: Review

References (145)

1. Almeida M.C., Steiner A.A., Branco L.G., Romanovsky A.A. Neural substrate of cold-seeking behavior in endotoxin shock. PLoS One 2006, 1.
2. Andresen M.C., Hofmann M.E., Fawley J.A. The unsilent majority-TRPV1 drives "spontaneous" transmission of unmyelinated primary afferents within cardiorespiratory NTS. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2012, 303:R1207-R1216.
3. Baker M.A., Doris P.A. Control of evaporative heat loss during changes in plasma osmolality in the cat. J. Physiol. 1982, 328:535-545.
4. Bamshad M., Song C.K., Bartness T.J. CNS origins of the sympathetic nervous system outflow to brown adipose tissue. Am. J. Physiol. 1999, 276:R1569-R1578.
5. Bautista D.M., Siemens J., Glazer J.M., Tsuruda P.R., Basbaum A.I., Stucky C.L., Jordt S.E., Julius D. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 2007, 448:204-208.
6. Blessing W.W., Nalivaiko E. Raphe magnus/pallidus neurons regulate tail but not mesenteric arterial blood flow in rats. Neuroscience 2001, 105:923-929.
7. Blouet C., Schwartz G.J. Duodenal lipid sensing activates vagal afferents to regulate non-shivering brown fat thermogenesis in rats. PLoS One 2012, 7.
8. Boulant J.A. Counterpoint: Heat-induced membrane depolarization of hypothalamic neurons: an unlikely mechanism of central thermosensitivity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290:R1481-R1484. (discussion R1484).
9. Boulant J.A., Dean J.B. Temperature receptors in the central nervous system. Annu. Rev. Physiol. 1986, 48:639-654.
10. Boulant J.A., Hardy J.D. The effect of spinal and skin temperatures on the firing rate and thermosensitivity of preoptic neurones. J. Physiol. 1974, 240:639-660.
11. Brown J.W., Sirlin E.A., Benoit A.M., Hoffman J.M., Darnall R.A. Activation of 5-HT1A Receptors in Medullary Raphe Disrupts Sleep and Decreases Shivering during Cooling in the Conscious Piglet. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007.
12. Cannon B., Nedergaard J. Brown adipose tissue: Function and physiological significance. Physiol. Rev. 2004, 84:277-359.
13. Cano G., Passerin A.M., Schiltz J.C., Card J.P., Morrison S.F., Sved A.F. Anatomical substrates for the central control of sympathetic outflow to interscapular adipose tissue during cold exposure. J. Comp. Neurol. 2003, 460:303-326.
14. Cao W.H., Morrison S.F. Disinhibition of rostral raphe pallidus neurons increases cardiac sympathetic nerve activity and heart rate. Brain Res. 2003, 980:1-10.
15. Cao W.H., Morrison S.F. Glutamate receptors in the raphe pallidus mediate brown adipose tissue thermogenesis evoked by activation of dorsomedial hypothalamic neurons. Neuropharmacology 2006, 51:426-437.
16. Cao W.H., Fan W., Morrison S.F. Medullary pathways mediating specific sympathetic responses to activation of dorsomedial hypothalamus. Neuroscience 2004, 126:229-240.
17. Cao W.H., Madden C.J., Morrison S.F. Inhibition of brown adipose tissue thermogenesis by neurons in the ventrolateral medulla and in the nucleus tractus solitarius. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299:R277-R290.
18. Cerri M., Morrison S.F. Activation of lateral hypothalamic neurons stimulates brown adipose tissue thermogenesis. Neuroscience 2005, 135:627-638.
19. Chen X.M., Hosono T., Yoda T., Fukuda Y., Kanosue K. Efferent projection from the preoptic area for the control of non-shivering thermogenesis in rats. J. Physiol. 1998, 512(Pt 3):883-892.
20. Craig A.D. How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 2002, 3:655-666.
21. Craig A.D., Bushnell M.C., Zhang E.T., Blomqvist A. A thalamic nucleus specific for pain and temperature sensation. Nature 1994, 372:770-773.
22. Cypess A.M., Lehman S., Williams G., Tal I., Rodman D., Goldfine A.B., Kuo F.C., Palmer E.L., Tseng Y.H., Doria A., Kolodny G.M., Kahn C.R. Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 2009, 360:1509-1517.
23. Darian-Smith I., Johnson K.O., Dykes R. "Cold" fiber population innervating palmar and digital skin of the monkey: Responses to cooling pulses. J. Neurophysiol. 1973, 36:325-346.
24. Dimitrov E.L., Kim Y.Y., Usdin T.B. Regulation of hypothalamic signaling by tuberoinfundibular peptide of 39 residues is critical for the response to cold: A novel peptidergic mechanism of thermoregulation. J. Neurosci. 2011, 31:18166-18179.
25. Elmquist J.K., Scammell T.E., Jacobson C.D., Saper C.B. Distribution of fos-like immunoreactivity in the rat brain following intravenous lipopolysaccharide administration. J. Comp. Neurol. 1996, 371:85-103.
26. Escourrou P., Freund P.R., Rowell L.B., Johnson D.G. Splanchnic vasoconstriction in heat-stressed men: Role of renin-angiotensin system. J. Appl. Physiol. 1982, 52:1438-1443.
27. Farrell M.J., Trevaks D., Taylor N.A., McAllen R.M. Regional brain responses associated with thermogenic and psychogenic sweating events in humans. J. Neurophysiol. 2015, 114:2578-2587.
28. Feketa V.V., Balasubramanian A., Flores C.M., Player M.R., Marrelli S.P. Shivering and tachycardic responses to external cooling in mice are substantially suppressed by TRPV1 activation but not by TRPM8 inhibition. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 305:R1040-R1050.
29. Golozoubova V., Cannon B., Nedergaard J. UCP1 is essential for adaptive adrenergic nonshivering thermogenesis. Am. J. Physiol. Endocrinol. Metab. 2006, 291:E350-E357.
30. Guieu J.D., Hardy J.D. Effects of heating and cooling of the spinal cord on preoptic unit activity. J. Appl. Physiol. 1970, 29:675-683.
31. Gupta B.N., Nier K., Hensel H. Cold-sensitive afferents from the abdomen. Pflugers Arch. 1979, 380:203-204.
32. Hammel H.T., Hardy J.D., Fusco M.M. Thermoregulatory responses to hypothalamic cooling in unanesthetized dogs. Am. J. Physiol. 1960, 198:481-486.
33. Hermann D.M., Luppi P.H., Peyron C., Hinckel P., Jouvet M. Afferent projections to the rat nuclei raphe magnus, raphe pallidus and reticularis gigantocellularis pars alpha demonstrated by iontophoretic application of choleratoxin (subunit b). J. Chem. Neuroanat. 1997, 13:1-21.
34. Horn T., Wilkinson M.F., Landgraf R., Pittman Q.J. Reduced febrile responses to pyrogens after lesions of the hypothalamic paraventricular nucleus. Am. J. Physiol. 1994, 267:R323-R328.
35. Hylden J.L., Anton F., Nahin R.L. Spinal lamina I projection neurons in the rat: Collateral innervation of parabrachial area and thalamus. Neuroscience 1989, 28:27-37.
36. Imai-Matsumura K., Matsumura K., Nakayama T. Involvement of ventromedial hypothalamus in brown adipose tissue thermogenesis induced by preoptic cooling in rats. Jpn. J. Phycol. 1984, 34:939-943.
37. Johnson C.D., Gilbey M.P. Effects of aortic nerve stimulation on discharges of sympathetic neurons innervating rat tail artery and vein. Am. J. Physiol. 1998, 275:R942-R949.
38. Kataoka N., Hioki H., Kaneko T., Nakamura K. Psychological stress activates a dorsomedial hypothalamus-medullary raphe circuit driving brown adipose tissue thermogenesis and hyperthermia. Cell Metab. 2014, 20:346-358.
39. Kerman I.A., Enquist L.W., Watson S.J., Yates B.J. Brainstem substrates of sympatho-motor circuitry identified using trans-synaptic tracing with pseudorabies virus recombinants. J. Neurosci. 2003, 23:4657-4666.
40. Kobayashi A., Osaka T. Involvement of the parabrachial nucleus in thermogenesis induced by environmental cooling in the rat. Pflugers Arch. 2003, 446:760-765.
41. Kregel K.C., Stauss H., Unger T. Modulation of autonomic nervous system adjustments to heat stress by Central ANG II receptor antagonism. Am. J. Physiol. 1994, 266:R1985-R1991.
42. Kregel K.C., Wall P.T., Gisolfi C.V. Peripheral vascular responses to hyperthermia in the rat. J. Appl. Physiol. 1988, 64:2582-2588.
43. Leite L.H., Zheng H., Coimbra C.C., Patel K.P. Contribution of the paraventricular nucleus in autonomic adjustments to heat stress. Exp. Biol. Med. (Maywood) 2012, 237:570-577.
44. Li J., Xiong K., Pang Y., Dong Y., Kaneko T., Mizuno N. Medullary dorsal horn neurons providing axons to both the parabrachial nucleus and thalamus. J. Comp. Neurol. 2006, 498:539-551.
45. Lkhagvasuren B., Nakamura Y., Oka T., Sudo N., Nakamura K. Social defeat stress induces hyperthermia through activation of thermoregulatory sympathetic premotor neurons in the medullary raphe region. Eur. J. Neurosci. 2011, 34:1442-1452.
46. Lu J., Zhang Y.H., Chou T.C., Gaus S.E., Elmquist J.K., Shiromani P., Saper C.B. Contrasting effects of ibotenate lesions of the paraventricular nucleus and subparaventricular zone on sleep-wake cycle and temperature regulation. J. Neurosci. 2001, 21:4864-4874.
47. Lundius E.G., Sanchez-Alavez M., Ghochani Y., Klaus J., Tabarean I.V. Histamine influences body temperature by acting at H1 and H3 receptors on distinct populations of preoptic neurons. J. Neurosci. 2010, 30:4369-4381.
48. Macefield V.G., Wallin B.G. Respiratory and cardiac modulation of single sympathetic vasoconstrictor and sudomotor neurones to human skin. J. Physiol. 1999, 516(Pt 1):303-314.
49. Madden C.J., Morrison S.F. Excitatory amino acid receptor activation in the raphe pallidus area mediates prostaglandin-evoked thermogenesis. Neuroscience 2003, 122:5-15.
50. Madden C.J., Morrison S.F. Excitatory amino acid receptors in the dorsomedial hypothalamus mediate prostaglandin-evoked thermogenesis in brown adipose tissue. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 286:R320-R325.
51. Madden C.J., Morrison S.F. Hypoxic Activation of Arterial Chemoreceptors Inhibits Sympathetic Outflow to Brown Adipose Tissue (BAT) in Rats. J. Physiol. 2005.
52. Madden C.J., Morrison S.F. Serotonin potentiates sympathetic responses evoked by spinal NMDA. J. Physiol. 2006, 577:525-537.
53. Madden C.J., Morrison S.F. Neurons in the paraventricular nucleus of the hypothalamus inhibit sympathetic outflow to brown adipose tissue. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296:R831-R843.
54. Madden C.J., Morrison S.F. Endogenous activation of spinal 5-hydroxytryptamine (5-HT) receptors contributes to the thermoregulatory activation of brown adipose tissue. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R776-R783.
55. van Marken Lichtenbelt W.D., Vanhommerig J.W., Smulders N.M., Drossaerts J.M., Kemerink G.J., Bouvy N.D., Schrauwen P., Teule G.J. Cold-activated brown adipose tissue in healthy men. N. Engl. J. Med. 2009, 360:1500-1508.
56. Martin-Cora F.J., Fornal C.A., Metzler C.W., Jacobs B.L. Single-unit responses of serotonergic medullary and pontine raphe neurons to environmental cooling in freely moving cats. Neuroscience 2000, 98:301-309.
57. McKinley M.J., Yao S.T., Uschakov A., McAllen R.M., Rundgren M., Martelli D. The median preoptic nucleus: Front and centre for the regulation of body fluid, sodium, temperature, sleep and cardiovascular homeostasis. Acta Physiol (Oxf.) 2015, 214:8-32.
58. Minson C.T., Wladkowski S.L., Pawelczyk J.A., Kenney W.L. Age, splanchnic vasoconstriction, and heat stress during tilting. Am. J. Physiol. 1999, 276:R203-R212.
59. Morrison S.F. Raphe pallidus neurons mediate prostaglandin E2-evoked increases in brown adipose tissue thermogenesis. Neuroscience 2003, 121:17-24.
60. Morrison S.F. 2010 Carl Ludwig Distinguished lectureship of the APS neural control and autonomic regulation section: Central neural pathways for thermoregulatory cold defense. J. Appl. Physiol. 2011, 110:1137-1149.
61. Morrison S.F., Madden C.J. Central nervous system regulation of brown adipose tissue. Compr. Physiol. 2014, 4:1677-1713.
62. Morrison S.F., Nakamura K. Central neural pathways for thermoregulation. Front. Biosci. (Landmark Ed.) 2011, 16:74-104.
63. Morrison S.F., Cao W.-H., Madden C.J. Dorsomedial hypothalamic and brainstem pathways controlling thermogenesis in brown adipose tissue. J. Therm. Biol. 2004, 29:333-337.
64. Morrison S.F., Madden C.J., Tupone D. Central neural regulation of brown adipose tissue thermogenesis and energy expenditure. Cell Metab. 2014, 19:741-756.
65. Morrison S.F., Sved A.F., Passerin A.M. GABA-mediated inhibition of raphe pallidus neurons regulates sympathetic outflow to brown adipose tissue. Am. J. Physiol. 1999, 276:R290-R297.
66. Muzzi M., Blasi F., Masi A., Coppi E., Traini C., Felici R., Pittelli M., Cavone L., Pugliese A.M., Moroni F., Chiarugi A. Neurological basis of AMP-dependent thermoregulation and its relevance to central and peripheral hyperthermia. J. Cereb. Blood Flow Metab. 2013, 33:183-190.
67. Nagashima K., Nakai S., Tanaka M., Kanosue K. Neuronal circuitries involved in thermoregulation. Auton. Neurosci. 2000, 85:18-25.
68. Nakamura K. Central circuitries for body temperature regulation and fever. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 301:R1207-R1228.
69. Nakamura K., Morrison S.F. Central efferent pathways mediating skin cooling-evoked sympathetic thermogenesis in brown adipose tissue. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R127-R136.
70. Nakamura K., Morrison S.F. Preoptic mechanism for cold-defensive responses to skin cooling. J. Physiol. 2008, 586:2611-2620.
71. Nakamura K., Morrison S.F. A thermosensory pathway that controls body temperature. Nat. Neurosci. 2008, 11:62-71.
72. Nakamura K., Morrison S.F. A thermosensory pathway mediating heat-defense responses. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:8848-8853.
73. Nakamura K., Morrison S.F. Central efferent pathways for cold-defensive and febrile shivering. J. Physiol. 2011, 589:3641-3658.
74. Nakamura K., Matsumura K., Hubschle T., Nakamura Y., Hioki H., Fujiyama F., Boldogkoi Z., Konig M., Thiel H.J., Gerstberger R., Kobayashi S., Kaneko T. Identification of sympathetic premotor neurons in medullary raphe regions mediating fever and other thermoregulatory functions. J. Neurosci. 2004, 24:5370-5380.
75. Nakamura K., Matsumura K., Kaneko T., Kobayashi S., Katoh H., Negishi M. The rostral raphe pallidus nucleus mediates pyrogenic transmission from the preoptic area. J. Neurosci. 2002, 22:4600-4610.
76. Nakamura Y., Nakamura K., Matsumura K., Kobayashi S., Kaneko T., Morrison S.F. Direct pyrogenic input from prostaglandin EP3 receptor-expressing preoptic neurons to the dorsomedial hypothalamus. Eur. J. Neurosci. 2005, 22:3137-3146.
77. Nakamura Y., Nakamura K., Morrison S.F. Different populations of prostaglandin EP3 receptor-expressing preoptic neurons project to two fever-mediating sympathoexcitatory brain regions. Neuroscience 2009, 161:614-620.
78. Nakayama T., Eisenman J.S., Hardy J.D. Single unit activity of anterior hypothalamus during local heating. Science 1961, 134:560-561.
79. Nakayama T., Hammel H., Hardy J., Eisenman J. Thermal stimulation of electrical activity of single units of the preoptic region. Am. J. Physiol. 1963, 204:1122-1126.
80. Nason M.W., Mason P. Modulation of sympathetic and somatomotor function by the ventromedial medulla. J. Neurophysiol. 2004, 92:510-522.
81. Nason M.W., Mason P. Medullary raphe neurons facilitate brown adipose tissue activation. J. Neurosci. 2006, 26:1190-1198.
82. Nedergaard J., Bengtsson T., Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E444-E452.
83. Oldfield B.J., Giles M.E., Watson A., Anderson C., Colvill L.M., McKinley M.J. The neurochemical characterisation of hypothalamic pathways projecting polysynaptically to brown adipose tissue in the rat. Neuroscience 2002, 110:515-526.
84. Ono K., Tsukamoto-Yasui M., Hara-Kimura Y., Inoue N., Nogusa Y., Okabe Y., Nagashima K., Kato F. Intragastric administration of capsiate, a transient receptor potential channel agonist, triggers thermogenic sympathetic responses. J. Appl. Physiol. 2011, 110:789-798. (1985).
85. Ootsuka Y., Blessing W.W. Inhibition of medullary raphe/parapyramidal neurons prevents cutaneous vasoconstriction elicited by alerting stimuli and by cold exposure in conscious rabbits. Brain Res. 2005, 1051:189-193.
86. Ootsuka Y., McAllen R.M. Interactive drives from two brain stem premotor nuclei are essential to support rat tail sympathetic activity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 289:R1107-R1115.
87. Ootsuka Y., Blessing W.W., Steiner A.A., Romanovsky A.A. Fever response to intravenous prostaglandin E2 is mediated by the brain but does not require afferent vagal signaling. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294:R1294-R1303.
88. Osaka T. Cold-induced thermogenesis mediated by GABA in the preoptic area of anesthetized rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 287:R306-R313.
89. Owens N.C., Ootsuka Y., Kanosue K., McAllen R.M. Thermoregulatory control of sympathetic fibres supplying the rat's tail. J. Physiol. 2002, 543:849-858.
90. Palmes E.D., Park C.R. The regulation of body temperature during fever. Arch. Environ. Health 1965, 11:749-759.
91. Peyron C., Tighe D.K., van den Pol A.N., de Lecea L., Heller H.C., Sutcliffe J.G., Kilduff T.S. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci. 1998, 18:9996-10015.
92. Rathner J.A., Morrison S.F. Rostral ventromedial periaqueductal gray: A source of inhibition of the sympathetic outflow to brown adipose tissue. Brain Res. 2006, 1077:99-107.
93. Rathner J.A., Madden C.J., Morrison S.F. Central pathway for spontaneous and prostaglandin E2-evoked cutaneous vasoconstriction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295:R343-R354.
94. Riedel W. Warm receptors in the dorsal abdominal wall of the rabbit. Pflugers Arch. 1976, 361:205-206.
95. Romanovsky A.A. Do fever and anapyrexia exist? Analysis of set point-based definitions. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 287:R992-R995.
96. Romanovsky A.A. Thermoregulation: Some concepts have changed. Functional architecture of the thermoregulatory system. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R37-R46.
97. Romanovsky A. Skin temperature: Its role in thermoregulation. Acta Physiol (Oxf.) 2014, 210:498-507.
98. Rothwell N.J., Stock M.J., Thexton A.J. Decerebration activates thermogenesis in the rat. J. Physiol. Lond. 1983, 342:15-22.
99. Samuels B.C., Zaretsky D.V., DiMicco J.A. Tachycardia evoked by disinhibition of the dorsomedial hypothalamus in rats is mediated through medullary raphe. J. Physiol. 2002, 538:941-946.
100. Saper C.B., Breder C.D. The neurologic basis of fever. N. Engl. J. Med. 1994, 330:1880-1886.
101. Sarkar S., Zaretskaia M.V., Zaretsky D.V., Moreno M., DiMicco J.A. Stress- and lipopolysaccharide-induced c-fos expression and nNOS in hypothalamic neurons projecting to medullary raphe in rats: A triple immunofluorescent labeling study. Eur. J. Neurosci. 2007, 26:2228-2238.
102. Satinoff E., Rutstein J. Behavioral thermoregulation in rats with anterior hypothalamic lesions. J. Comp. Physiol. Psychol. 1970, 71:77-82.
103. Schafer S.S., Schafer S. The behavior of the proprioceptors of the muscle and the innervation of the fusimotor system during cold shivering. Exp. Brain Res. 1973, 17:364-380.
104. Schafer S.S., Schafer S. The role of the primary afference in the generation of a cold shivering tremor. Exp. Brain Res. 1973, 17:381-393.
105. Shafton A.D., McAllen R.M. Location of cat brain stem neurons that drive sweating. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 304:R804-R809.
106. Shafton A.D., Oldfield B.J., McAllen R.M. CRF-like immunoreactivity selectively labels preganglionic sudomotor neurons in cat. Brain Res. 1992, 599:253-260.
107. Shibasaki M., Crandall C.G. Mechanisms and controllers of eccrine sweating in humans. Front. Biosci. (Schol. Ed.) 2010, 2:685-696.
108. Shibasaki M., Aoki K., Morimoto K., Johnson J.M., Takamata A. Plasma hyperosmolality elevates the internal temperature threshold for active thermoregulatory vasodilation during heat stress in humans. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 297:R1706-R1712.
109. Smith C.J., Johnson J.M. Responses to hyperthermia. Optimizing heat dissipation by convection and evaporation: Neural control of skin blood flow and sweating in humans. Auton. Neurosci. 2016, 10.1016/j.autneu.2016.1001.1002.
110. Smith J.E., Jansen A.S., Gilbey M.P., Loewy A.D. CNS cell groups projecting to sympathetic outflow of tail artery: Neural circuits involved in heat loss in the rat. Brain Res. 1998, 786:153-164.
111. Steiner A.A., Turek V.F., Almeida M.C., Burmeister J.J., Oliveira D.L., Roberts J.L., Bannon A.W., Norman M.H., Louis J.C., Treanor J.J., Gavva N.R., Romanovsky A.A. Nonthermal activation of transient receptor potential vanilloid-1 channels in abdominal viscera tonically inhibits autonomic cold-defense effectors. J. Neurosci. 2007, 27:7459-7468.
112. Stornetta R.L., Rosin D.L., Simmons J.R., McQuiston T.J., Vujovic N., Weston M.C., Guyenet P.G. Coexpression of vesicular glutamate transporter-3 and gamma-aminobutyric acidergic markers in rat rostral medullary raphe and intermediolateral cell column. J. Comp. Neurol. 2005, 492:477-494.
113. Szekely M. The vagus nerve in thermoregulation and energy metabolism. Auton. Neurosci. 2000, 85:26-38.
114. Szymusiak R., Satinoff E. Acute thermoregulatory effects of unilateral electrolytic lesions of the medial and lateral preoptic area in rats. Physiol. Behav. 1982, 28:161-170.
115. Tabarean I.V., Behrens M.M., Bartfai T., Korn H. Prostaglandin E2-increased thermosensitivity of anterior hypothalamic neurons is associated with depressed inhibition. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2590-2595.
116. Takahashi Y., Zhang W., Sameshima K., Kuroki C., Matsumoto A., Sunanaga J., Kono Y., Sakurai T., Kanmura Y., Kuwaki T. Orexin Neurons Are Indispensable for Prostaglandin E2-Induced Fever and Defence against Environmental Cooling in Mice. J. Physiol. 2013.
117. Takamata A., Mack G.W., Gillen C.M., Jozsi A.C., Nadel E.R. Osmoregulatory modulation of thermal sweating in humans: Reflex effects of drinking. Am. J. Physiol. 1995, 268:R414-R422.
118. Tanaka M., McAllen R.M. A subsidiary fever center in the medullary raphe?. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 289:R1592-R1598.
119. Tanaka M., McKinley M.J., McAllen R.M. Roles of two preoptic cell groups in tonic and febrile control of rat tail sympathetic fibers. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296:R1248-R1257.
120. Tanaka M., McKinley M.J., McAllen R.M. Preoptic-raphe connections for thermoregulatory vasomotor control. J. Neurosci. 2011, 31:5078-5088.
121. Tanaka M., McKinley M.J., McAllen R.M. Role of an excitatory preoptic-raphe pathway in febrile vasoconstriction of the rat's tail. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 305:R1479-R1489.
122. Tanaka M., Nagashima K., McAllen R.M., Kanosue K. Role of the medullary raphe in thermoregulatory vasomotor control in rats. J. Physiol. 2002, 540:657-664.
123. Tanaka M., Owens N.C., Nagashima K., Kanosue K., McAllen R.M. Reflex activation of rat fusimotor neurons by body surface cooling, and its dependence on the medullary raphe. J. Physiol. 2006, 572:569-583.
124. Tanaka M., Tonouchi M., Hosono T., Nagashima K., Yanase-Fujiwara M., Kanosue K. Hypothalamic region facilitating shivering in rats. Jpn. J. Physiol. 2001, 51:625-629.
125. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Raumann B.E., Basbaum A.I., Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 1998, 21:531-543.
126. Toth I.E., Toth D.E., Boldogkoi Z., Hornyak A., Palkovits M., Blessing W.W. Serotonin-synthesizing neurons in the rostral medullary raphe/parapyramidal region transneuronally labelled after injection of pseudorabies virus into the rat tail. Neurochem. Res. 2006, 31:277-286.
127. Tsukita S., Yamada T., Uno K., Takahashi K., Kaneko K., Ishigaki Y., Imai J., Hasegawa Y., Sawada S., Ishihara H., Oka Y., Katagiri H. Hepatic glucokinase modulates obesity predisposition by regulating BAT thermogenesis via neural signals. Cell Metab. 2012, 16:825-832.
128. Tupone D., Madden C.J., Cano G., Morrison S.F. An orexinergic projection from perifornical hypothalamus to raphe pallidus increases rat brown adipose tissue thermogenesis. J. Neurosci. 2011, 31:15944-15955.
129. Tupone D., Madden C.J., Morrison S.F. Central activation of the A1 adenosine receptor (A1AR) induces a hypothermic, torpor-like state in the rat. J. Neurosci. 2013, 33:14512-14525.
130. Turlejska E., Baker M.A. Elevated CSF osmolality inhibits thermoregulatory heat loss responses. Am. J. Physiol. 1986, 251:R749-R754.
131. Virtanen K.A., Lidell M.E., Orava J., Heglind M., Westergren R., Niemi T., Taittonen M., Laine J., Savisto N.J., Enerback S., Nuutila P. Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 2009, 360:1518-1525.
132. Wallin B.G., Charkoudian N. Sympathetic neural control of integrated cardiovascular function: Insights from measurement of human sympathetic nerve activity. Muscle Nerve 2007, 36:595-614.
133. Whyte D.G., Johnson A.K. Lesions of the anteroventral third ventricle region (AV3V) disrupt cardiovascular responses to an elevation in core temperature. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288:R1783-R1790.
134. Yoshida K., Konishi M., Nagashima K., Saper C.B., Kanosue K. Fos activation in hypothalamic neurons during cold or warm exposure: Projections to periaqueductal gray matter. Neuroscience 2005, 133:1039-1046.
135. Yoshida K., Li X., Cano G., Lazarus M., Saper C.B. Parallel preoptic pathways for thermoregulation. J. Neurosci. 2009, 29:11954-11964.
136. Yoshida K., Maruyama M., Hosono T., Nagashima K., Fukuda Y., Gerstberger R., Kanosue K. Fos expression induced by warming the preoptic area in rats. Brain Res. 2002, 933:109-117.
137. Yoshida K., Nakamura K., Matsumura K., Kanosue K., Konig M., Thiel H.J., Boldogkoi Z., Toth I., Roth J., Gerstberger R., Hubschle T. Neurons of the rat preoptic area and the raphe pallidus nucleus innervating the brown adipose tissue express the prostaglandin E receptor subtype EP3. Eur. J. Neurosci. 2003, 18:1848-1860.
138. Zaretskaia M.V., Zaretsky D.V., DiMicco J.A. Role of the dorsomedial hypothalamus in thermogenesis and tachycardia caused by microinjection of prostaglandin E2 into the preoptic area in anesthetized rats. Neurosci. Lett. 2003, 340:1-4.
139. Zaretsky D.V., Hunt J.L., Zaretskaia M.V., DiMicco J.A. Microinjection of prostaglandin E2 and muscimol into the preoptic area in conscious rats: Comparison of effects on plasma adrenocorticotrophic hormone (ACTH), body temperature, locomotor activity, and cardiovascular function. Neurosci. Lett. 2006, 397:291-296.
140. Zaretsky D.V., Zaretskaia M.V., DiMicco J.A. Stimulation and blockade of GABAA receptors in the raphe pallidus: Effects on body temperature, heart rate, and blood pressure in conscious rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 285:R110-R116.
141. Zhang Y.H., Hosono T., Yanase-Fujiwara M., Chen X.M., Kanosue K. Effect of midbrain stimulations on thermoregulatory vasomotor responses in rats. J. Physiol. Lond. 1997, 503:177-186.
142. Zhang Y., Kerman I.A., Laque A., Nguyen P., Faouzi M., Louis G.W., Jones J.C., Rhodes C., Munzberg H. Leptin-receptor-expressing neurons in the dorsomedial hypothalamus and median preoptic area regulate sympathetic brown adipose tissue circuits. J. Neurosci. 2011, 31:1873-1884.
143. Zhang Y.H., Lu J., Elmquist J.K., Saper C.B. Lipopolysaccharide activates specific populations of hypothalamic and brainstem neurons that project to the spinal cord. J. Neurosci. 2000, 20:6578-6586.
144. Zhang W., Sunanaga J., Takahashi Y., Mori T., Sakurai T., Kanmura Y., Kuwaki T. Orexin neurons are indispensable for stress-induced thermogenesis in mice. J. Physiol. 2010, 588:4117-4129.
145. Zhang Y.H., Yanase-Fujiwara M., Hosono T., Kanosue K. Warm and cold signals from the preoptic area: Which contribute more to the control of shivering in rats?. J. Physiol. 1995, 485(Pt 1):195-202.