Evidence for in vivo thermosensitivity of serotonergic neurons in the rat dorsal raphe nucleus and raphe pallidus nucleus implicated in thermoregulatory cooling

Experimental Neurology

Volumn 227, Issue 2, 2011, Pages 264-278

  Hale, Matthew W ^a   Dady, Kathleen F ^a   Evans, Andrew K ^a,c   Lowry, Christopher A ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brainstem; Midbrain raphe; Serotonin; Thermoregulation; Thermosensation; Thermosensitive; Thermosensitivity; Warm temperature; Warming

Indexed keywords

PROTEIN C FOS; TRYPTOPHAN HYDROXYLASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; CELL ACTIVATION; COGNITION; CONTROLLED STUDY; COOLING; DORSAL RAPHE NUCLEUS; ENVIRONMENTAL TEMPERATURE; FOREBRAIN; GENE EXPRESSION REGULATION; HEAT SENSITIVITY; IMMEDIATE EARLY GENE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INCUBATION TEMPERATURE; MALE; MESENCEPHALON; NONHUMAN; NUCLEUS RAPHE PALLIDUS; ONCOGENE C FOS; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; ROOM TEMPERATURE; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; THERMAL EXPOSURE; THERMOREGULATION; WARMING;

ANIMALS; BODY TEMPERATURE; BODY TEMPERATURE REGULATION; EVIDENCE-BASED MEDICINE; MALE; NEURAL PATHWAYS; NEURONS; RAPHE NUCLEI; RATS; RATS, WISTAR; SEROTONIN; TRYPTOPHAN HYDROXYLASE;

EID: 78651421229     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.11.012     Document Type: Article

References (136)

1. Abrams J.K., Johnson P.L., Hollis J.H., Lowry C.A. Anatomical and functional topography of the dorsal raphe nucleus. Ann. NY Acad. Sci. 2004, 1018:46-57.
2. Abrams J.K., Johnson P.L., Hay-Schmidt A., Mikkelsen J.D., Shekhar A., Lowry C.A. Serotonergic systems associated with arousal and vigilance behaviors following administration of anxiogenic drugs. Neuroscience 2005, 133:983-997.
3. Amat J., Tamblyn J.P., Paul E.D., Bland S.T., Amat P., Foster A.C., Watkins L.R., Maier S.F. Microinjection of urocortin 2 into the dorsal raphe nucleus activates serotonergic neurons and increases extracellular serotonin in the basolateral amygdala. Neuroscience 2004, 129:509-519.
4. Azmitia E.C., Gannon P.J. Anatomy of the serotonergic system in the primate and sub-primate brain. Adv. Neurol. 1986, 43:407-468.
5. Bago M., Dean C. Sympathoinhibition from ventrolateral periaqueductal gray mediated by 5-HT(1A) receptors in the RVLM. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 280:R976-R984.
6. Bago M., Marson L., Dean C. Serotonergic projections to the rostroventrolateral medulla from midbrain and raphe nuclei. Brain Res. 2002, 945:249-258.
7. Beckett S., Marsden C.A. The effect of central and systemic injection of the 5-HT1A receptor agonist 8-OHDPAT and the 5-HT1A receptor antagonist WAY100635 on periaqueductal grey-induced defence behaviour. J. Psychopharmacol. 1997, 11:35-40.
8. Beckett S.R., Lawrence A.J., Marsden C.A., Marshall P.W. Attenuation of chemically induced defence response by 5-HT1 receptor agonists administered into the periaqueductal gray. Psychopharmacology (Berl.) 1992, 108:110-114.
9. Beitz A.J. The organization of afferent projections to the midbrain periaqueductal gray of the rat. Neuroscience 1982, 7:133-159.
10. Blessing W.W. 5-hydroxytryptamine 1A receptor activation reduces cutaneous vasoconstriction and fever associated with the acute inflammatory response in rabbits. Neuroscience 2004, 123:1-4.
11. Blessing W.W., Nalivaiko E. Raphe magnus/pallidus neurons regulate tail but not mesenteric arterial blood flow in rats. Neuroscience 2001, 105:923-929.
12. Blessing W.W., Seaman B., Pedersen N.P., Ootsuka Y. Clozapine reverses hyperthermia and sympathetically mediated cutaneous vasoconstriction induced by 3, 4-methylenedioxymethamphetamine (ecstasy) in rabbits and rats. J. Neurosci. 2003, 23:6385-6391.
13. Bramwell G.J. Factors affecting the activity of 5-HT-containing neurones. Brain Res. 1974, 79:515-519.
14. Bratincsak A., Palkovits M. Activation of brain areas in rat following warm and cold ambient exposure. Neuroscience 2004, 127:385-397.
15. 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.
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. Cerri M., Zamboni G., Tupone D., Dentico D., Luppi M., Martelli D., Perez E., Amici R. Cutaneous vasodilation elicited by disinhibition of the caudal portion of the rostral ventromedial medulla of the free-behaving rat. Neuroscience 2010, 165:984-995.
18. Commons K.G. Evidence for topographically organized endogenous 5-HT-1A receptor-dependent feedback inhibition of the ascending serotonin system. Eur. J. Neurosci. 2008, 27:2611-2618.
19. Craig A.D. How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 2002, 3:655-666.
20. 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.
21. Crawford L.K., Craige C.P., Beck S.G. Increased intrinsic excitability of lateral wing serotonin neurons of the dorsal raphe: a mechanism for selective activation in stress circuits. J. Neurophysiol. 2010, 103:2652-2663.
22. Cronin M.J., Baker M.A. Heat-sensitive midbrain raphe neurons in the anesthetized cat. Brain Res. 1976, 110:175-181.
23. Cronin M.J., Baker M.A. Midbrain heating in freely behaving cats (Felis domesticus): further evidence on the role of serotonin in thermoregulation. Gen. Pharmacol. 1977, 8:359-363.
24. Cronin M.J., Baker M.A. Physiological responses to midbrain thermal stimulation in the cat. Brain Res. 1977, 128:542-546.
25. Cronin M.J., Baker M.A. Thermosensitive midbrain neurons in the cat. Brain Res. 1977, 128:461-472.
26. Dampney R.A.L. Functional organization of central pathways regulating the cardiovascular system. Physiol. Rev. 1994, 74:323-364.
27. Davies S.J., Lowry C.A., Nutt D.J. Panic and hypertension: brothers in arms through 5-HT?. J. Psychopharmacol. 2007, 21:563-566.
28. Dickenson A.H. Specific responses of rat raphe neurones to skin temperature. J. Physiol. 1977, 273:277-293.
29. Fornal C.A., Litto W.J., Morilak D.A., Jacobs B.L. Single-unit responses of serotonergic dorsal raphe nucleus neurons to environmental heating and pyrogen administration in freely moving cats. Exp. Neurol. 1987, 98:388-403.
30. Gardner K.L., Thrivikraman K.V., Lightman S.L., Plotsky P.M., Lowry C.A. Early life experience alters behavior during social defeat: focus on serotonergic systems. Neuroscience 2005, 136:181-191.
31. Gardner K.L., Hale M.W., Lightman S.L., Plotsky P.M., Lowry C.A. Adverse early life experience and social stress during adulthood interact to increase serotonin transporter mRNA expression. Brain Res. 2009, 1305:47-63.
32. Gardner K.L., Hale M.W., Oldfield S., Lightman S.L., Plotsky P.M., Lowry C.A. Adverse experience during early life and adulthood interact to elevate tph2 mRNA expression in serotonergic neurons within the dorsal raphe nucleus. Neuroscience 2009, 163:991-1001.
33. Gautier H. Body temperature regulation in the rat. J. Therm. Biol. 2000, 25:273-279.
34. Gordon C.J. Thermal biology of the laboratory rat. Physiol. Behav. 1990, 47:963-991.
35. Gordon C.J., Heath J.E. Effect of monoamines on firing rate and thermal sensitivity of neurons in the preoptic area of awake rabbits. Exp. Neurol. 1981, 72:352-365.
36. Gottschlich K.W., Werner J. Effects of medial midbrain lesions on thermoresponsive neurons in the thalamus of the rat. Exp. Brain Res. 1985, 57:355-361.
37. Gottschlich K.W., Werner J., Schingnitz G. Thermoafferent signal processing in rats: an electrophysiological analysis of midbrain influences on thermoresponsive neurons in the ventrobasal thalamus. Pflugers Arch. 1984, 401:91-96.
38. Graeff F.G., Guimaraes F.S., De Andrade T.G., Deakin J.F. Role of 5-HT in stress, anxiety, and depression. Pharmacol. Biochem. Behav. 1996, 54:129-141.
39. Gray T.S., Magnuson D.J. Galanin-like immunoreactivity within amygdaloid and hypothalamic neurons that project to the midbrain central grey in rat. Neurosci. Lett. 1987, 83:264-268.
40. Gray T.S., Magnuson D.J. Peptide immunoreactive neurons in the amygdala and the bed nucleus of the stria terminalis project to the midbrain central gray in the rat. Peptides 1992, 13:451-460.
41. Grubbs F.E. Procedures for detecting outlying observations in samples. Technometrics 1969, 11:1-21.
42. Guscott M.R., Egan E., Cook G.P., Stanton J.A., Beer M.S., Rosahl T.W., Hartmann S., Kulagowski J., McAllister G., Fone K.C., Hutson P.H. The hypothermic effect of 5-CT in mice is mediated through the 5-HT7 receptor. Neuropharmacology 2003, 44:1031-1037.
43. Hagan J.J., Price G.W., Jeffrey P., Deeks N.J., Stean T., Piper D., Smith M.I., Upton N., Medhurst A.D., Middlemiss D.N., Riley G.J., Lovell P.J., Bromidge S.M., Thomas D.R. Characterization of SB-269970-A, a selective 5-HT(7) receptor antagonist. Br. J. Pharmacol. 2000, 130:539-548.
44. Hale M.W., Stamper C.E., Staub D.R., Lowry C.A. Urocortin 2 increases c-Fos expression in serotonergic neurons projecting to the ventricular/periventricular system. Exp. Neurol. 2010, 224:271-281.
45. Hedlund P.B., Sutcliffe J.G. Functional, molecular and pharmacological advances in 5-HT7 receptor research. Trends Pharmacol. Sci. 2004, 25:481-486.
46. Hedlund P.B., Danielson P.E., Thomas E.A., Slanina K., Carson M.J., Sutcliffe J.G. No hypothermic response to serotonin in 5-HT7 receptor knockout mice. Proc. Natl Acad. Sci. USA 2003, 100:1375-1380.
47. Hedlund P.B., Kelly L., Mazur C., Lovenberg T., Sutcliffe J.G., Bonaventure P. 8-OH-DPAT acts on both 5-HT1A and 5-HT7 receptors to induce hypothermia in rodents. Eur. J. Pharmacol. 2004, 487:125-132.
48. Herbert H. Evidence for projections from medullary nuclei onto serotonergic and dopaminergic neurons in the midbrain dorsal raphe nucleus of the rat. Cell Tissue Res. 1992, 270:149-156.
49. 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.
50. Hollis J.H., Evans A.K., Bruce K.P., Lightman S.L., Lowry C.A. Lipopolysaccharide has indomethacin-sensitive actions on Fos expression in topographically organized subpopulations of serotonergic neurons. Brain Behav. Immun. 2006, 20:569-577.
51. Holstege G. The basic, somatic, and emotional components of the motor system in mammals. The Rat Nervous System 1995, 137-154. Academic Press, San Diego. G. Paxinos (Ed.).
52. Holstege G., Meiners L., Tan K. Projections of the bed nucleus of the stria terminalis to the mesencephalon, pons, and medulla oblongata in the cat. Exp. Brain Res. 1985, 58:379-391.
53. Hori T., Harada Y. Responses of midbrain raphe neurons to local temperature. Pflugers Arch. 1976, 364:205-207.
54. Hurley K.M., Herbert H., Moga M.M., Saper C.B. Efferent projections of the infralimbic cortex of the rat. J. Comp. Neurol. 1991, 308:249-276.
55. Institute of Laboratory Animal Resources Commission on Life Sciences National Research Council Guide for the Care and Use of Laboratory Animals 1996, National Academy Press, Washington, DC.
56. Jahns R. Different projections of cutaneous thermal inputs to single units of the midbrain raphe nuclei. Brain Res. 1976, 101:355-361.
57. Johnson C.D., Gilbey M.P. Sympathetic activity recorded from the rat caudal ventral artery in vivo. J. Physiol. 1994, 476:437-442.
58. Johnson C.D., Gilbey M.P. On the dominant rhythm in the discharges of single postganglionic sympathetic neurones innervating the rat tail artery. J. Physiol. 1996, 497(Pt 1):241-259.
59. Johnson P.L., Lightman S.L., Lowry C.A. A functional subset of serotonergic neurons in the rat ventrolateral periaqueductal gray implicated in the inhibition of sympathoexcitation and panic. Ann. NY Acad. Sci. 2004, 1018:58-64.
60. Johnson P.L., Hollis J.H., Moratalla R., Lightman S.L., Lowry C.A. Acute hypercarbic gas exposure reveals functionally distinct subpopulations of serotonergic neurons in rats. J. Psychopharmacol. 2005, 19:327-341.
61. Johnson P.L., Lowry C.A., Truitt W., Shekhar A. Disruption of GABAergic tone in the dorsomedial hypothalamus attenuates responses in a subset of serotonergic neurons in the dorsal raphe nucleus following lactate-induced panic. J. Psychopharmacol. 2008, 22:642-645.
62. Keenan C.L., Chu N.S. Thermosensitivity of dorsal raphe neurons in vitro. Brain Res. 1987, 410:189-194.
63. Kerman I.A., Shabrang C., Taylor L., Akil H., Watson S.J. Relationship of presympathetic-premotor neurons to the serotonergic transmitter system in the rat brainstem. J. Comp. Neurol. 2006, 499:882-896.
64. Key B.J., Wigfield C.C. Changes in the tail surface temperature of the rat following injection of 5-hydroxytryptamine into the ventrolateral medulla. Neuropharmacology 1992, 31:717-723.
65. Köhler C., Steinbusch H. Identification of serotonin and non-serotonin-containing neurons of the mid-brain raphe projecting to the entorhinal area and the hippocampal formation. A combined immunohistochemical and fluorescent retrograde tracing study in the rat brain. Neuroscience 1982, 7:951-975.
66. Konishi M., Kanosue K., Kano M., Kobayashi A., Nagashima K. The median preoptic nucleus is involved in the facilitation of heat-escape/cold-seeking behavior during systemic salt loading in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R150-R159.
67. Lancel M., Cronlein J., Muller-Preuss P., Holsboer F. Lipopolysaccharide increases EEG delta activity within non-REM sleep and disrupts sleep continuity in rats. Am. J. Physiol. 1995, 268:R1310-R1318.
68. Lee H.S., Kim M.A., Valentino R.J., Waterhouse B.D. Glutamatergic afferent projections to the dorsal raphe nucleus of the rat. Brain Res. 2003, 963:57-71.
69. Lin M.T., Wu J.J., Tsay B.L. Serotonergic mechanisms in the hypothalamus mediate thermoregulatory responses in rats. Naunyn-Schmiedebergs Arch. Pharmacol. 1983, 322:271-278.
70. Linthorst A.C., Flachskamm C., Muller-Preuss P., Holsboer F., Reul J.M. Effect of bacterial endotoxin and interleukin-1 beta on hippocampal serotonergic neurotransmission, behavioral activity, and free corticosterone levels: an in vivo microdialysis study. J. Neurosci. 1995, 15:2920-2934.
71. Linthorst A.C., Flachskamm C., Reul J.M. Water temperature determines neurochemical and behavioural responses to forced swim stress: An in vivo microdialysis and biotelemetry study in rats. Stress 2007, 11:88-100.
72. Lowry C.A., Hollis J.H., de V.A., Pan B., Brunet L.R., Hunt J.R., Paton J.F., van K.E., Knight D.M., Evans A.K., Rook G.A., Lightman S.L. Identification of an immune-responsive mesolimbocortical serotonergic system: Potential role in regulation of emotional behavior. Neuroscience 2007, 146:756-772.
73. Lowry C.A., Lightman S.L., Nutt D.J. That warm fuzzy feeling: brain serotonergic neurons and the regulation of emotion. J. Psychopharmacol. 2009, 23:392-400.
74. Luiten P.G., ter Horst G.J., Steffens A.B. The hypothalamus, intrinsic connections and outflow pathways to the endocrine system in relation to the control of feeding and metabolism. Prog. Neurobiol. 1987, 28:1-54.
75. 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.
76. Madden C.J., Ito S., Rinaman L., Wiley R.G., Sved A.F. Lesions of the C1 catecholaminergic neurons of the ventrolateral medulla in rats using anti-DbetaH-saporin. Am. J. Physiol. 1999, 277:R1063-R1075.
77. Maruyama M., Nishi M., Konishi M., Takashige Y., Nagashima K., Kiyohara T., Kanosue K. Brain regions expressing Fos during thermoregulatory behavior in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 285:R1116-R1123.
78. Mathias S., Schiffelholz T., Linthorst A.C., Pollmacher T., Lancel M. Diurnal variations in lipopolysaccharide-induced sleep, sickness behavior and changes in corticosterone levels in the rat. Neuroendocrinology 2000, 71:375-385.
79. Morrison S.F. Raphe pallidus neurons mediate prostaglandin E2-evoked increases in brown adipose tissue thermogenesis. Neuroscience 2003, 121:17-24.
80. Morrison S.F. Central pathways controlling brown adipose tissue thermogenesis. News Physiol. Sci. 2004, 19:67-74.
81. Morrison S.F., Nakamura K., Madden C.J. Central control of thermogenesis in mammals. Exp. Physiol. 2008, 93:773-797.
82. Myers R.D. Impairment of thermoregulation, food and water intakes in the rat after hypothalamic injections of 5, 6-dihydroxytryptamine. Brain Res. 1975, 94:491-506.
83. Myers R.D. Hypothalamic control of thermoregulation. Handbook of the Hypothalamus 1980, Dekker, New York. P.J. Morgane, J. Panksepp (Eds.).
84. Nagashima K. Central mechanisms for thermoregulation in a hot environment. Ind. Health 2006, 44:359-367.
85. Nakamura K., Morrison S.F. A thermosensory pathway that controls body temperature. Nat. Neurosci. 2008, 11:62-71.
86. 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.
87. O'Leary D.S., Johnson J.M., Taylor W.F. Mode of neural control mediating rat tail vasodilation during heating. J. Appl. Physiol. 1985, 59:1533-1538.
88. Ootsuka Y., Blessing W.W. 5-Hydroxytryptamine 1A receptors inhibit cold-induced sympathetically mediated cutaneous vasoconstriction in rabbits. J. Physiol. 2003, 552:303-314.
89. Ootsuka Y., Blessing W.W. Activation of slowly conducting medullary raphe-spinal neurons, including serotonergic neurons, increases cutaneous sympathetic vasomotor discharge in rabbit. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288:R909-R918.
90. Ootsuka Y., Blessing W.W., McAllen R.M. Inhibition of rostral medullary raphe neurons prevents cold-induced activity in sympathetic nerves to rat tail and rabbit ear arteries. Neurosci. Lett. 2004, 357:58-62.
91. Ootsuka Y., Nalivaiko E., Blessing W.W. Spinal 5-HT2A receptors regulate cutaneous sympathetic vasomotor outflow in rabbits and rats; relevance for cutaneous vasoconstriction elicited by MDMA (3, 4-methylenedioxymethamphetamine, "ecstasy") and its reversal by clozapine. Brain Res. 2004, 1014:34-44.
92. 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.
93. Patel P.D., Pontrello C., Burke S. Robust and tissue-specific expression of TPH2 versus TPH1 in rat raphe and pineal gland. Biol. Psychiatry 2004, 55:428-433.
94. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, San Diego. Fourth Edition.
95. Petersen R.G. Design and Analysis of Experiments 1985, Marcel Dekker, Inc., New York.
96. Peyron C., Luppi P.H., Fort P., Rampon C., Jouvet M. Lower brainstem catecholamine afferents to the rat dorsal raphe nucleus. J. Comp. Neurol. 1996, 364:402-413.
97. Raman E.R., Roberts M.F., Vanhuyse V.J. Body temperature control of rat tail blood flow. Am. J. Physiol. 1983, 245:R426-R432.
98. Rand R.P., Burton A.C., Ing T. The tail of the rat, in temperature regulation and acclimatization. Can. J. Physiol. Pharmacol. 1963, 43:257-267.
99. Rasmussen K., Heym J., Jacobs B.L. Activity of serotonin-containing neurons in nucleus centralis superior of freely moving cats. Exp. Neurol. 1984, 83:302-317.
100. Rathner J.A., Owens N.C., McAllen R.M. Cold-activated raphe-spinal neurons in rats. J. Physiol. 2001, 535:841-854.
101. 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.
102. Rizvi T.A., Ennis M., Behbehani M.M., Shipley M.T. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J. Comp. Neurol. 1991, 303:121-131.
103. Rizvi T.A., Ennis M., Shipley M.T. Reciprocal connections between the medial preoptic area and the midbrain periaqueductal gray in rat: a WGA-HRP and PHA-L study. J. Comp. Neurol. 1992, 315:1-15.
104. Roche M., Commons K.G., Peoples A., Valentino R.J. Circuitry underlying regulation of the serotonergic system by swim stress. J. Neurosci. 2003, 23:970-977.
105. Rusyniak D.E., Zaretskaia M.V., Zaretsky D.V., DiMicco J.A. 3, 4-Methylenedioxymethamphetamine- and 8-hydroxy-2-di-n-propylamino-tetralin-induced hypothermia: role and location of 5-hydroxytryptamine 1A receptors. J. Pharmacol. Exp. Ther. 2007, 323:477-487.
106. Sakowski S.A., Geddes T.J., Thomas D.M., Levi E., Hatfield J.S., Kuhn D.M. Differential tissue distribution of tryptophan hydroxylase isoforms 1 and 2 as revealed with monospecific antibodies. Brain Res. 2006, 1085:11-18.
107. 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.
108. Saper C.B., Loewy A.D. Efferent connections of the parabrachial nucleus in the rat. Brain Res. 1980, 197:291-317.
109. Saper C.B., Swanson L.W., Cowan W.M. An autoradiographic study of the efferent connections of the lateral hypothalamic area in the rat. J. Comp. Neurol. 1979, 183:689-706.
110. Schingnitz G., Werner J. Thalamic burst firing-a neuronal code for temperature information$. Brain Res. 1980, 195:467-470.
111. Simerly R.B., Swanson L.W. Projections of the medial preoptic nucleus: a Phaseolus vulgaris leucoagglutinin anterograde tract-tracing study in the rat. J. Comp. Neurol. 1988, 270:209-242.
112. 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.
113. Squires R.F. Hyperthermia- and L-tryptophan-induced increases in serotonin turnover in rat brain. Adv. Biochem. Psychopharmacol. 1974, 10:207-211.
114. Staub D.R., Spiga F., Lowry C.A. Urocortin 2 increases c-Fos expression in topographically organized subpopulations of serotonergic neurons in the rat dorsal raphe nucleus. Brain Res. 2005, 1044:176-189.
115. Staub D.R., Evans A.K., Lowry C.A. Evidence supporting a role for corticotropin-releasing factor type 2 (CRF(2)) receptors in the regulation of subpopulations of serotonergic neurons. Brain Res. 2006, 1070:77-89.
116. Steinbusch H.W.M. Serotonin-immunoreactive neurons and their projections in the CNS. Classical Transmitters and Transmitter Receptors in the CNS 1984, 68-125. Elsevier Science Publishers B.V., Amsterdam. A. Björklund, T. Hökfelt (Eds.).
117. Swanson L.W., Mogenson G.J., Simerly R.B., Wu M. Anatomical and electrophysiological evidence for a projection from the medial preoptic area to the 'mesencephalic and subthalamic locomotor regions' in the rat. Brain Res. 1987, 405:108-122.
118. Taber Pierce E., Foote W.E., Hobson J.A. The efferent connection of the nucleus raphe dorsalis. Brain Res. 1976, 107:137-144.
119. 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.
120. Thomas D.R., Melotto S., Massagrande M., Gribble A.D., Jeffrey P., Stevens A.J., Deeks N.J., Eddershaw P.J., Fenwick S.H., Riley G., Stean T., Scott C.M., Hill M.J., Middlemiss D.N., Hagan J.J., Price G.W., Forbes I.T. SB-656104-A, a novel selective 5-HT7 receptor antagonist, modulates REM sleep in rats. Br. J. Pharmacol. 2003, 139:705-714.
121. Thompson G.E., Stevenson J.A. The temperature response of the male rat to treadmill exercise, and the effect of anterior hypothalamic lesions. Can. J. Physiol. Pharmacol. 1965, 43:279-287.
122. Tillet Y. Serotoninergic projections from the raphe nuclei to the preoptic area in sheep as revealed by immunohistochemistry and retrograde labeling. J. Comp. Neurol. 1992, 320:267-272.
123. 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.
124. Underwood M.D., Arango V., Bakalian M.J., Ruggiero D.A., Mann J.J. Dorsal raphe nucleus serotonergic neurons innervate the rostral ventrolateral medulla in rat. Brain Res. 1999, 824:45-55.
125. Van Bockstaele E.J., Biswas A., Pickel V.M. Topography of serotonin neurons in the dorsal raphe nucleus that send axon collaterals to the rat prefrontal cortex and nucleus accumbens. Brain Res. 1993, 624:188-198.
126. Vianna D.M., Allen C., Carrive P. Cardiovascular and behavioral responses to conditioned fear after medullary raphe neuronal blockade. Neuroscience 2008, 153:1344-1353.
127. Waller M.B., Myers R.D., Martin G.E. Thermoregulatory deficits in the monkey produced by 5,6-dihydroxytryptamine injected into the hypothalamus. Neuropharmacology 1976, 15:61-68.
128. Walther D.J., Peter J.U., Bashammakh S., Hortnagl H., Voits M., Fink H., Bader M. Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 2003, 299:76.
129. Weiss B.L., Aghajanian G.K. Activation of brain serotonin metabolism by heat: role of midbrain raphe neurons. Brain Res. 1971, 26:37-48.
130. Werner J., Bienek A. The significance of nucleus raphe dorsalis and centralis for thermoafferent signal transmission to the preoptic area of the rat. Exp. Brain Res. 1985, 59:543-547.
131. Werner J., Bienek A. Loss and restoration of preoptic thermoreactiveness after lesions of the rostral raphe nuclei. Exp. Brain Res. 1990, 80:429-435.
132. Wilson M.A., Molliver M.E. The organization of serotonergic projections to cerebral cortex in primates: retrograde transport studies. Neuroscience 1991, 44:555-570.
133. Winer B.J., Brown D.R., Michels K.M. Statistical Principles in Experimental Design 1991, McGraw-Hill, New York. 3rd ed.
134. Young A.A., Dawson N.J. Evidence for on-off control of heat dissipation from the tail of the rat. Can. J. Physiol. Pharmacol. 1982, 60:392-398.
135. Zaretsky D.V., Zaretskaia M.V., DiMicco J.A. Stimulation and blockade of GABA(A) 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.
136. Zaretsky D.V., Zaretskaia M.V., Samuels B.C., Cluxton L.K., DiMicco J.A. Microinjection of muscimol into raphe pallidus suppresses tachycardia associated with air stress in conscious rats. J. Physiol. 2003, 546:243-250.