Functional subsets of serotonergic neurones: Implications for control of the hypothalamic-pituitary-adrenal axis

Journal of Neuroendocrinology

Volumn 14, Issue 11, 2002, Pages 911-923

  Lowry, C A ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Anxiety; Fear; Serotonin; Stress; Subiculum

Indexed keywords

GLUCOCORTICOID; SEROTONIN;

ADRENAL CORTEX; ANXIETY; AROUSAL; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; BEHAVIOR; BRAIN CORTEX; BRAIN STEM; CELL FUNCTION; CIRCADIAN RHYTHM; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; ENDOCRINE FUNCTION; FEAR; HORMONE RELEASE; HUMAN; HUMAN CELL; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LIMBIC SYSTEM; MEDIAN RAPHE NUCLEUS; MOTOR SYSTEM; NERVE PROJECTION; NEUROENDOCRINE SYSTEM; NEUROMODULATION; PRIORITY JOURNAL; RAPHE NUCLEUS; REGULATORY MECHANISM; SENSITIZATION; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; STRESS; SUBICULUM; TOPOGRAPHY; ULTRADIAN RHYTHM;

ANIMALS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; NEURONS; PITUITARY-ADRENAL SYSTEM; SEROTONIN;

EID: 0036854562     PISSN: 09538194     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2826.2002.00861.x     Document Type: Article

References (156)

1. Welch JE, Farrar GE, Dunn AJ, Saphier D. Central 5-HT1A receptors inhibit adrenocortical secretion. Neuroendocrinology 1993; 57: 272-281.
2. Saphier D, Welch JE. Central stimulation of adrenocortical secretion by 5-hydroxytryptamine1A agonists is mediated by sympathomedullary activation. J Pharmacol Exp Ther 1994; 270: 905-917.
3. Saphier D, Farrar GE, Welch JE. Differential inhibition of stress-induced adrenocortical responses by 5-HT1A agonists and by 5-HT2 and 5-HT3 antagonists. Psychoneuroendocrinology 1995; 20: 239-257.
4. Chaouloff F. Physiopharmacological interactions between stress hormones and central serotonergic systems. Brain Res Rev 1993; 18: 1-32.
5. Chaouloff F. Serotonin, stress and corticoids. J Psychopharmacol 2000; 14: 139-151.
6. Chaouloff F. Physiopharmacological interactions between stress hormones and central serotonergic systems. Brain Res Rev 1993; 18: 1-32.
7. Herman JP, Prewitt CMF, Cullman WE. Neuronal circuit regulation of the hypothalamo-pituitary-adrenocorticaI stress axis. Crit Rev Neurobiol 1996; 10: 371-394.
8. Herman JP, Cullman WE. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 1997; 20: 78-84.
9. Steinbusch HWM. Serotonin-immunoreactive neurons and their projections in the CNS. In: Björklund A, Hökfelt T, eds. Classical Transmitters and Transmitter Receptors in the CNS. Amsterdam: Elsevier Science Publishers BV, 1984: 68-125.
10. Rasmussen K, Heym J, Jacobs BL. Activity of serotonin-containing neurons in nucleus centralis superior of freely moving cats. Exp Neurol 1984; 83: 302-317.
11. Peyron C, Petit J-M, Rampon C, Jouvet M, Luppi P-H. Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 1998; 82: 443-468.
12. Kirby LG, Rice KC, Valentino RJ. Effects of corticotropin-releasing factor on neuronal activity in the serotonergic dorsal raphe nucleus. Neuropsychopharmacology 2000; 22: 148-162.
13. Price ML, Curtis AL, Kirby LG, Valentino RJ, Lucki I. Effects of corticotropin-releasing factor on brain serotonergic activity. Neuropsychopharmacology 1998; 18: 492-502.
14. Lowry CA, Rodda JE, Lightman SL, Ingram CD. Corticotropin-releasing factor increases in vitro firing rates of serotonergic neurons in the rat dorsal raphe nucleus: evidence for activation of a topographically organized mesolimbocortical serotonergic system. J Neurosci 2000; 20: 7728-7736.
15. Hammack SE, Richey KJ, Schmid MJ, LoPresti ML, Watkins LR, Maier SF. The role of corticotropin-releasing hormone in the dorsal raphe nucleus in mediating the behavioral consequences of uncontrollable stress. J Neurosci 2002; 22: 1020-1026.
16. De Olmos J, Heimer L. Double and triple labeling of neurons with fluorescent substances; The study of collateral pathways in the ascending raphe system. Neurosci Lett 1980; 19: 7-12.
17. Imai H, Steindler D' Kitai ST. The organization of divergent axonal projections from the midbrain raphe nuclei in the rat. J Comp Neurol 1986; 243: 363-380.
18. Villar MJ, Vitale ML, Hokfelt T, Verhofstad AA. Dorsal raphe serotoninergic branching neurons projecting both to the lateral geniculate body and superior colliculus: a combined retrograde tracing-immunobistochemical study in the rat. J Comp Neurol 1988; 277: 126-140.
19. Li YQ. Takada M, Mizuno N. Collateral projections of single neurons in the periaqueductal gray and dorsal raphe nucleus to both the trigeminal sensory complex and spinal cord in the rat. Neurosci Lett 1993; 153: 153-156.
20. Li YQ, Takada M, Matsuzaki S, Shinonaga Y, Mizuno N. Identification of periaqueductal gray and dorsal raphe nucleus neurons projecting to both the trigeminal sensory complex and forebrain structures: a fluorescent retrograde double-labeling study in the rat. Brain Res 1993; 623: 267-277.
21. Losier BJ, Semba K. Dual projections of single cholinergic and aminergic brainstem neurons to the thalamus and basal forebrain in the rat. Brain Res 1993; 604: 41-52.
22. Petrov T, Krukoff TL, Jhamandas JH. The hypothalamic paraventricular and lateral parabrachial nuclei receive collaterals from raphe nucleus neurons: a combined double retrograde and immunocytochemical study. J Comp Neurol 1992; 318: 18-26.
23. Petrov T, Krukoff TL, Jhamandas JH. Chemically defined collateral projections from the pons to the central nucleus of the amygdala and hypothalamic paraventricular nucleus in the rat. Cell Tissue Res 1994; 277: 289-295.
24. Acsady L, Arabadzisz D, Katona I, Freund TF. Topographic distribution of dorsal and median raphe neurons with hippocampal, septal and dual projection. Acta Biol Hung 1996; 47: 9-19.
25. 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.
26. Azmitia EC Jr, Segal M. An autoradiographic analysis of the differential ascending projection of the dorsal and median raphe nuclei in the rat. J Comp Neurol 1978; 179: 651-668.
27. Steinbusch HWM, Nieuwenhuys R, Verhofstad AAJ, van der Kooy D. The nucleus raphe dorsalis of the rat and its projection upon the caudatoputamen. A combined cytoarchitectonic, immunohistochemical and retrograde transport study. J Physiol 1980; 77: 157-174.
28. Rueter LE, Fornal CA, Jacobs BL. A critical review of 5-HT brain microdialysis and behavior. Rev Neurosci 1997; 8: 117-137.
29. Rueter LE, Jacobs BL. A microdialysis examination of serotonin release in the rat forebrain induced by behavioral/environmental manipulations. Brain Res 1996; 739: 57-69.
30. Rueter LE, Jacobs BL. Changes in forebrain serotonin at the light-dark transition: correlation with behaviour. Neuroreport 1996; 7: 1107-1111.
31. Wilkinson LO, Auerbach SB, Jacobs BL. Extracellular serotonin levels change with behavioral state but not with pyrogen-induced hyperthermia. J Neurosci 1991; 11: 2732-2741.
32. Mendlin A, Martin FJ, Jacobs BL. Dopaminergic input is required for increases in serotonin output produced by behavioral activation: an in vivo microdialysis study in rat forebrain. Neuroscience 1999; 93: 897-905.
33. Kirby LG, Lucki I. Interaction between the forced swimming test and fluoxetine treatment on extracellular 5-hydroxytryptamine and 5-hydroxyindoleacetic acid in the rat. J Pharmacol Exp Ther 1997; 282: 967-976.
34. Kirby LG, Lucki I. The effect of repeated exposure to forced swimming on extracellular levels of 5-hydroxytryptamine in the rat. Stress 1998; 2: 251-263.
35. Takahashi H, Takanda Y, Nagai N, Urano T, Takada A. Extracellular serotonin in the striatum increased after immobilization stress only in the nighttime. Behav Brain Res 2002; 91: 185-191.
36. Kirby LG, Chou-Green JM, Davis K, Lucki I. The effects of different stressors on extracellular 5-hydroxytryptamine and 5-hydroxyindoleacetic acid. Brain Res 1997; 760: 218-230.
37. Anisman H. Neurochemical changes elicited by stress. In: Anisman H, Bignami G, eds. Psychopharmacology of Aversively Motivated Behavior. New York: Plenum Press, 1978: 119-172.
38. Keay KA, Bandler R. Parallel circuits mediating distinct emotional coping reactions to different types of stress. Neurosci Biobehav Rev 2001; 25: 669-678.
39. Holstege G. Descending motor pathways and the spinal motor system: limbic and nonlimbic components. Prog Brain Res 1991; 87: 307-421.
40. Holstege G. The basic, somatic, and emotional components of the motor system in mammals. In: Paxinos G, ed. The Rat Nervous System. San Diego: Academic Press, 1995: 137-154.
41. Dampney RAL. Functional organization of central pathways regulating the cardiovascular system. Physiol Rev 1994; 74: 323-364.
42. Jansen ASP, Van Nguyen X, Karpitskiy V, Mettenleiter TC, Loewy AD. Central command neurons of the sympathetic nervous system: basis of the fight-or-flight response. Science 1995; 270: 644-646.
43. Buijs RM, Wortel J, van Heerikhuize JJ, Feenstra MG, ter Horst GJ, Romijn HJ, Kalsbeek A. Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway. Eur J Neurosci 1999; 11: 1535-1544.
44. Jasper MS, Engeland WC. Splanchnic neural activity modulates ultradian and circadian rhythms in adrenocorticall secretion in awake rats. Neuroendocrinology 1994; 59: 97-109.
45. Swanson LW, Petrovich GD. What is the amygdala? Trends Neurosci 1998: 21: 323-331.
46. Hadziefendic S, Haxhiu MA. CNS innervation of vagal preganglionic neurons controlling peripheral airways: a transneuronal labeling study using pseudorabies virus. J Auton Nerv Syst 1999; 76: 135-145.
47. ter Horst GJ, Postema F. Forebrain parasympathetic control of heart activity: retrograde transneuronal viral labeling in rats. Am J Physiol 1997; 273: H2926-H2930.
48. Di Micco JA, Samuels BC, Zaretskaia MV, Zaretsky DV. The dorsomedial hypothalamus and the response to stress. Part renaissance, part revolution. Pharmacol Biochem Behav 2002; 71: 469-480.
49. Fontes MAP, Tagawa T, Polson JW, Cavanagh S-J, Dampney RAL. Descending pathways mediating cardiovascular response from dorsomedial hypothalamic nucleus. Am J Physiol Heart Circ Physiol 2001; 280: H2891-H2901.
50. Dunn JD. Plasma corticosterone responses to electrical stimulation of the bed nucleus of the stria terminalis. Brain Res 1987; 407: 327-331.
51. Feldman S, Conforti N, Weidenfeld J. Limbic pathways and hypothalamic neurotransmitters mediating adrenocortical responses to neural stimuli. Neurosci Biobehav Rev 1995; 19: 235-240.
52. Feldman S, Weidenfeld J. The excitatory effects of the amygdala on hypothalamo-pituitary-adrenocortical responses are mediated by hypothalamic norepinephrine, serotonin, and CRF-41. Brain Res Bull 1998; 45: 389-393.
53. Gray TS. Amygdala role in autonomic and neuroendocrine responses to stress. In: Stress, Neuropptides and Systemic Disease. New York: Academic Press, 1991: 37-53.
54. Feldman S, Conforti N, Itzik A, Weidenfeld J. Differential effect of amygdaloid lesions on CRF-41, ACTH and corticosterone responses following neural stimuli. Brain Res 1994; 658: 21-26.
55. Feldman S, Conforti N. Amygdalectomy inhibits adrenocortical responses to somatosensory and olfactory stimulation. Neuroendocrinology 1981; 32: 331-344.
56. Van de Kar L, Piechowski RA, Rittenhouse PA, Gray TS. Amygdaloid lesions: differential effect on conditioned stress and immobilization-induced increase in corticosterone and renin secretion. Neuroendocrinology 1991; 54: 89-95.
57. Beaulieu S, Di Paolo T, Cote J, Barden N. Participation of the central amygdaloid nucleus in the response of adrenocorticotropin secretion to immobilization stress: opposing roles of the noradrenergic and dopaminergic systems. Neuroendocrinology 1987; 45: 37-46.
58. Mor G, Saphier D, Feldman S. Neural pathways that mediate the effects of afferent stimuli on paraventricular nucleus multiunit activity in freely moving rats. J Neurosci Res 1987; 17: 452-458.
59. Feldman S, Conforti N, Saphier D. The preoptic area and bed nucleus of the stria terminalis are involved in the effects of the amygdala on adrenocortical secretion. Neuroscience 1990; 37: 775-779.
60. Grahn RE, Will MJ, Hammack SE, Maswood S, McQueen MB, Watkins LR, Maier SF. Activation of serotonin-immunoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor. Brain Res 1999; 826: 35-43.
61. Maier SF, Grahn RE, Watkins LR. 8-OH-DPAT microinjected in the region of the dorsal raphe nucleus blocks and reverses the enhancement of fear conditioning and interference with escape produced by exposure to inescapable shock. Behav Neurosci 1995; 109: 404-412.
62. Maier SF, Watkins LF. Stressor controllability, anxiety, and serotonin. Cognitive Ther Res 1998; 22: 595-613.
63. Singewald N, Sharp T. Neuroanatomical targets of anxiogenic drugs in the hindbrain as revealed by Fos immunocytochemistry. Neuroscience 2000; 98: 759-770.
64. Maswood S, Barter JE, Watkins LR, Maier SF. Exposure to inescapable but not escapable shock increases extracellular levels of 5-HT in the dorsal raphe nucleus of the rat. Brain Res 1998; 783: 115-120.
65. Amat J, Matus-Amat P, Watkins LR, Maier SF. Escapable and inescapable stress differentially alter extracellular levels of 5-HT in the basolateral amygdala of the rat. Brain Res 1998; 812: 113-120.
66. Blanchard DC, Cholvanich P, Blanchard RJ, Clow DW, Hammer RP Jr, Rowlett JK, Bardo MT. Serotonin, but not dopamme, metabolites are increased in selected brain regions of subordinate male rats in a colony environment. Brain Res 1991; 568: 61-66.
67. Ge J, Barnes NM, Costall B, Naylor RJ. Effect of aversive stimulation on 5-hydroxytryptamine and dopamine metabolism in the rat brain. Pharmacol Biochem Behav 1997; 58: 775-783.
68. Sawchenko P, Swanson LW, Stembusch HWM, Verhofstad AAJ. The distribution and cells of origin of serotonergic inputs to the paraventricular and supraoptic nuclei of the rat. Brain Res 1983; 277: 355-360.
69. Levin MC, Sawchenko PE, Howe PRC, Bloom SR, Polak JM. Organization of galanin-immunoreactive inputs to the paraventricular nucleus with special reference to their relationship to catecholaminergic afferents. J Comp Neurol 1987; 261: 562-582.
70. Ottersen OP. Afferent connections of the amygdaloid complex of the rat with some observations in the cat: III. Afferents from the lower brain stem. J Comp Neurol 1981; 202: 335-356.
71. Norita M, Kawamura K. Subcortical afferents to the monkey amygdala: an HRP study. Brain Res 1980; 190: 225-230.
72. Kazakov VN, Kravtsov P, Ya Krakhotkina ED, Maisky VA. Sources of cortical, hypothalamic and spinal serotonergic projections: topical organization within the nucleus raphe dorsalis. Neuroscience 1993; 56: 157-164.
73. Underwood MD, Arango V, Bakalian MJ, Ruggiero DA, Mann JJ. Dorsal raphe nucleus serotonergic neurons innervate the rostral ventrolateral medulla in rat. Brain Res 1999; 824: 45-55.
74. Weller KL, Smith DA. Afferent connections to the bed nucleus of the stria terminalis. Brain Res 1982; 232: 255-270.
75. Pasquier DA, Reinoso-Suarez F. Different efferent connections of the brain stem to the hippocampus in the cat. Brain Res 1977; 120: 540-548.
76. Azmitia EC. The serotonin-producing neurons of the midbrain median and dorsal raphe nuclei. In: Iversen LL, Iversen SS, Snyder SH, eds. Chemical Pathways in the Brain. New York: Plenum, 1981: 233-314.
77. Buchan AM, Azmitia EC. The fimbrial and cingulum bundle serotonin afferents to the hippocampus. Exp Brain Res 1977; 27: R11.
78. van Groen T, Wyss JM. Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J Comp Neurol 1990; 302: 515-528.
79. Risold PY, Swanson LW. Structural evidence for functional domains in the rat hippocampus. Science 1996; 272: 1484-1486.
80. Canteras NS, Swanson LW. Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J Comp Neurol 1992; 324: 180-194.
81. Canteras NS. The medial hypothalamic defensive system: hodological organization and functional implications. Pharmacol Biochem Behav 2002; 71: 481-491.
82. Vertes RP, Fortin WJ, Crane AM. Projections of the median raphe nucleus in the rat. J Comp Neurol 1999; 407: 555-582.
83. Köhler C, Chan-Palay V, Steinbusch H. The distribution and origin of serotonin-containing fibers in the septal area: a combined immunohistochemical and fluorescent retrograde tracing study in the rat. J Comp Neurol 1982; 209: 91-111.
84. Graeff FG, Guimaraes FS, De Andrade TG, Deakin JF. Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 1996; 54: 129-141.
85. Deakin JF. 5-HT, antidepressant drugs and the psychosocial origins of depression. J Psychopharmacol 1996; 10: 31-38.
86. Gray JA. The Neuropsychology of Anxiety: an Enquiry Into the Functions of the Septo-Hippocampal System. Oxford: Clarendon Press, 1982.
87. Jacobson L, Sapolsky R. The role of the hippocampus in feedback regulation of the hypothatamic-pituitary-adrenocortical axis. Endocr Rev, 1991; 12: 118-134.
88. Herman JP, Cullman WE, Morano MI, Akil H, Watson SJ. Contribution of the ventral subiculum to inhibitory regulation of the hypothalamo-pituitary-adrenocortical axis. J Neuroendocrinol 1995; 7: 475-482.
89. Herman JP, Dolgas CM, Carlson SL. Ventral subiculum regulates hypothalamo-pituitary-adrenocortical and behavioural responses to cognitive stressors. Neuroscience 1998; 86: 449-459.
90. Cullinan WE, Herman JP, Watson SJ. Ventral subicular interaction with the hypothalamic, paraventricular nucleus: Evidence for a relay in the bed nucleus of the stria terminalis. J Comp Neurol 1993; 332: 1-20.
91. Bowers G, Cullman WE, Herman JP. Region-specific regulation of glutamic acid decarboxylase (GAD) mRNA expression in central stress circuits. J Neurosci 1998; 18: 5938-5947.
92. Herman JP, Tasker JG, Ziegler DR, Cullman WE. Local circuit regulation of paraventricular nucleus stress integration. Glutamate-GABA connections. Pharmacol Biochem Behav 2002; 71: 457-468.
93. Boudaba C, Szabo K, Tasker JG. Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J Neurosci 1996; 16: 7151-7160.
94. Munaro NI, Morello H, Taleisnik S. Glutamic acid decarboxylase activity of the preoptic area and hypothalamus is influenced by the serotonergic system. J Neurochem 1991; 57: 1302-1306.
95. Diorio D, Viau V, Meancy MJ. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci 1993; 13: 3839-3847.
96. Brake WG, Flores G, Francis D, Meaney MJ, Srivastava LK, Gratton A. Enhanced nucleus accumbens dopamine and plasma corticosterone stress responses in adult rats with neonatal excitotoxic lesions to the medial prefrontal cortex. Neuroscience 2000; 96: 687-695.
97. Sullivan RM, Gratton A. Lateralized effects of medial prefrontal cortex lesions on neuroendocrine and autonomic stress responses in rats. J Neurosci 1999; 19: 2834-2840.
98. Marcilhac A, Faudon M, Anglade G, Hery F, Siaud P. An investigation of serotonergic involvement in the regulation of ACTH and corticosterone in the olfactory bulbectomized rat. Pharmacol Biochem Behav 1999; 63: 599-605.
99. Marcilhac A, Anglade G, Hery F, Siaud P. Effects of bilateral olfactory bulbectomy on the anterior pituitary corticotropic, cell activity in male rats. Horm Metab Res 1999; 31: 399-401.
100. Seggie J, Uhlir I, Brown GM. Adrenal stress responses following septal lesions in the rat. Neuroendocrinology 1974; 16: 225-236.
101. Uhlir I, Seggie J, Brown GM. The effect of septal lesions on the threshold of adrenal stress response. Neuroendocrinology 1974; 14: 351-355.
102. Dobrakovova M, Kvetnansky R, Torda T, Murgas K. Changes of plasma and adrenal catecholamines and corticosterone in stressed rats with septal lesions. Physiol Behav 1982; 29: 41-45.
103. Thomas E. Forebrain mechanisms in the relief of fear: the role of the lateral septum. Psychobiology 1988; 16: 36-44.
104. Usher DR, Lieblich I, Siegel RA. Pituitary adrenal function after small and large lesions in the lateral septal area in food-deprived rats. Neuroendocrinology 1974; 16: 156-164.
105. Seggie J. Differential responsivity of corticosterone and prolactin to stress following lesions of the septum or amygdala: implications for psychoneuroendocrinology. Prog Neuropsychopharmacol Biol Psychiatry 1987; 11: 315-324.
106. Campeau S, Falls WA, Cullman WE, Helmreich DL, Davis M, Watson SJ. Elicitation and reduction of fear: behavioural and neuroendocrine indices and brain induction of the immediate-early gene C-FOS. Neuroscience 1997; 78: 1087-1104.
107. Herman JP, Cullman WE, Watson SJ. Involvement of the bed nucleus of the stria terminalis in tonic regulation of paraventricular hypothalamic CRH and AVP mRNA expression. J Neuroendocrinol 1994; 6:433-442.
108. Murphy CA, DiCamillo AM, Haun F, Murray M. Lesion of the habenular efferent pathway produces anxiety and locomotor hyperactivity in rats: a comparison ofthe effects of neonatal and adult lesions. Behav Brain Res 1996; 81: 43-52.
109. Suarez M, Perassi NI. Plasma corticosterone responses to lesions and stimulation of the limbic thalami nuclei, medial mammillary nucleus and cingulate cortex. Arch Int Physiol Biochim 1988; 96: 69 74.
110. Viau V, Meaney MJ. The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area. J Neurosci 1996; 16: 1866-1876.
111. Cullman WE, Helmreich DL, Watson SJ. Fos expression in forebrain afferents to the hypothalamic paraventricular nucleus following swim stress. J Comp Neural 1996; 368: 88 -99.
112. Grizzle WE, Johnson RN, Schramm LP, Gann DS. Hypothalamic cells in an area mediating ACTH release respond to right atrial stretch. Am J Physiol 1975; 228: 1039-1045.
113. Bradbury MJ, Strack AM, Dallman MF. Lesions of the hippocampal efferent pathway (fimbria-fornix) do not alter sensitivity of adrenocorticotropin to feedback inhibition by corticosterone in rats. Neuroendocrinology 1993; 58: 396-407.
114. Herman JP, Cullinan WE, Young EA, Akil H, Watson SJ. Selective forebrain fiber tract lesions implicate ventral hippocampal structures in tonic regulation of paraventricular nucleus corticotropin-releasing hormone (CRH) and arginine vasopressin (AVP) mRNA expression. Brain Res 1992; 592: 228-238.
115. Dilts RP, Boadle-Biber MC. Differential activation of the 5-hydroxytryptamine-containing neurons of the midbrain raphe of the rat in response to randomly presented inescapable sound. Neurosci Lett 1995; 199: 78-80.
116. Clement HW, Kirsch M, Hasse C, Opper C, Gemsa D, Wesemann W. Effect of repeated immobilization on serotonin metabolism in different rat brain areas and on serum corticosterone. J Neural Transmission 1998; 105: 1155-1170.
117. Daugherty WP, Corley KC, Phan T-H, Boadle-Biber MC. Further studies on the activation of rat median raphe serotonergic neurons by inescapable sound stress. Brain Res 2001; 923: 103-111.
118. Moore RY, Eichler VB. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 1972; 42: 201-206.
119. Szafarczyk A, Ixart G, Malaval F, Nouguier-Soule J, Assenmacher I. Effects of lesions of the suprachiasmatic nuclei and of p-chloropheny-lalanine on the circadian rhythms of adrenocorticotrophic hormone and corticosterone in the plasma, and on locomotor activity of rats. J Endocrinol 1979; 83: 1-16.
120. Cascio CS, Shinsako J, Dallman ME. The suprachiasmatic nuclei stimulate evening ACTH secretion in the rat. Brain Res 1987; 423: 173-178.
121. Kant GJ, Mougey EH, Meyerhoff JL. Diurnal variation in neuroendocrine response to stress in rats: plasma ACTH, β-endorphin, β-LPH, corticosterone, prolactin and pituitary cyclic AMP responses. Neuroendocrinology 1986; 43: 383-390.
122. Dunn J, Scheving L, Millet P. Circadian variation in stress evoked increases in plasma corticosterone. Am J Physiol 1972; 223: 402-406.
123. Kalsbeek A, Buijs RM, van Heerikhuize JJ, Arts M, van der Woude TP. Vasopressin-containing neurons of the suprachiasmatic nuclei inhibit corticosterone release. Brain Res 1992; 580: 62-67.
124. Buijs RM, Markman M, Nunes-Cardoso B, Hou YX, Shinn S. Projections of the suprachiasmatic nucleus to stress-related areas in the rat hypothalamus: a light and electron microscopic study. J Comp Neurol 1993; 335: 42-54.
125. Vrang N, Mikkelsen JD, Larsen PJ. Direct link from the suprachiasmatic nucleus to hypothalamic neurons projecting to the spinal cord: a combined tracing study using cholera toxin subunit B and Phaseolds vulgaris-leucoagglutinin. Brain Res Bull 1997; 44: 671-680.
126. Yamazaki S, Kerbeshian MC, Hocker CG, Block GD, Menaker M. Rhythmic properties of the hamster suprachiasmatic nucleus in vivo. J Neurosci 1998; 18: 10709-10723.
127. Lightman SL, Windle RJ, Julian MD, Harbuz MS, Shanks N, Wood SA, Kershaw YM, Ingram CD. Significance of pulsatility in the HPA axis. Novartis Found Symp 2000; 227: 244-257.
128. Windle RJ, Wood SA, Lightman SL, Ingram CD. The pulsatile characteristics of hypothalamo-pituitary-adrenal activity in female Lewis and Fischer 344 rats and its relationship to differential stress responses. Endocrinology 1998; 139: 4044-4052.
129. Windle RJ, Wood SA, Shanks N, Lightman SL, Ingram CD. Ultradian rhythm of basal corticosterone release in the female rat: dynamic interaction with the response to acute stress. Endocrinology 1998; 139: 443-450.
130. Meyer-Bernstein EL, Morin LP. Differential serotonergic innervation of the suprachiasmatic nucleus and the intergeniculate leaflet and its role in circadian rhythm modulation. J Neurosci 1996; 16: 2097-2111.
131. Harrington ME. The ventral lateral geniculate nucleus and the intergeniculate leaflet: interrelated structures in the visual and circadian systems. Neurosci Biobehav Rev 1997; 21: 705-727.
132. 3H-5HT and HRP after retrograde transport. J Comp Neurol 1981; 203: 737-743.
133. Moga MM, Moore RY. Organization of neural inputs to the suprachiasmatic nucleus in the rat. J Comp Neurol 1997; 389: 508-534.
134. Dudley TE, Dinardo LA, Glass J D. In vivo assessment of the midbrain raphe nuclear regulation of serotonin release in the hamster suprachiasmatic nucleus. J Neurophysiol 1999; 81: 1469-1477.
135. Meyer-Bernstein EL, Morin LP. Electrical stimulation of the median or dorsal raphe nuclei reduces light-induced FOS protein in the suprachiasmatic nucleus and causes circadian activity rhythm phase shifts. Neuroscience 1999; 92: 267-279.
136. Ehlen JC, Grossman GH, Glass JD. In vivo resetting of the hamster circadian clock by 5-HT7 receptors in the suprachiasmatic nucleus. J Neurosci 2001; 21: 5351-5357.
137. Lowry CA, Renner KJ, Moore FL. Catecholamines and indoleamines in the central nervous system of a urodele amphibian a microdissection study with emphasis on the distribution of epinephrine. Brain Behav Evol 1996; 48: 70-93.
138. Brownstein MJ, Palkovits M, Tappaz ML, Saavedra JM, Kizer JS. Effect of surgical isolation of the hypothalamus on its neurotransmitter content. Brain Res 1976; 117: 287-295.
139. Van de Kar LD, Lorens SA. Differential serotonergic innervation of individual hypothalamic nuclei and other forebrain regions by the dorsal and median midbrain raphe nuclei. Brain Res 1979; 162: 45-54.
140. Steinbusch HW. Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 1981; 6: 557-618.
141. Sladek JR Jr, Sladek CD. Localization of serotonin within tanycytes of the rat median eminence. Cell Tissue Res 1978; 186: 465-474.
142. Mezey E, Leranth C, Brownstein MJ, Friedman E, Krieger DT, Palkovits M. On the origin of the serotonergic input to the intermediate lobe of the rat pituitary. Brain Res 1984; 294: 231-237.
143. Kang M, Park C, Ahn H, Hub Y. Ectopic expression of serotonin-positive neurons in the hypothalamus associated with a significant serotonin decrease in the midbrain of food restricted rats. Neurosci Lett 2001; 314: 25-28.
144. Johnson PL, Lowry CA, Lightman SL. Serotonin-accumulating systems in the hypothalamus. Soc Neurosci Abstract 2001; 27: 415.14.
145. Saper CB. Central autonomic system. In: Paxinos G, ed. The Rat Nervous System. San Diego: Academic Press, 1995: 107-135.
146. Alheid GF, de Olmos JS, Beltramino CA. Amygdala and extended amygdala. In: Paxinos G, ed. The Rat Nervous System. San Diego: Academic Press, 1995: 495-578.
147. Wiersma A, Bohus B, Koolhaas JM. Corticotropin-releasing hormone microinfusion in the central amygdala diminishes a cardiac parasympathetic outflow under stress-free conditions. Brain Res 1993; 625: 219-227.
148. Porter ID, Whitehouse BJ, Taylor AH, Nussey SS. Effect of arginine vasopressin and oxytocin on acetylcholine-stimulation of corticosteroid and catecholamine secretion from the rat adrenal gland perfused in situ. Neuropeptides 1988; 12: 265-271.
149. Gonzalez-Fernandez I, Gonzalo-Sanz LM. Vagal influence on the adrenocortical function of the rat. Rev Esp Fisiol 1987; 43: 203-207.
150. Janossy A, Orso E, Szalay KS, Juranyi Z, Beck M, Vizi ES, Vinson GP. Cholinergic regulation of the rat adrenal zona glomerulosa. J Endocrinol 1998; 157: 305-315.
151. Davis M. A neural systems approach to the study of the amygdala, fear and anxiety. In: Elliott JM, Heal DJ, Marsden CA, eds. Experimental Approaches to Anxiety and Depression. Chichester: John Wiley and Sons, 1992: 45-71.
152. Hosoya Y, Ito R, Kohno K. The topographical organization of neurons in the dorsal hypothalamic area that project to the spinal cord or to the nucleus raphe pallidus in the rat. Exp Brain Res 1987; 66: 500-506.
153. McDonald AJ. Projections of the intermediate subdivision of the central amygdaloid nucleus to the bed nucleus of the stria terminalis and medial diencephalon. Neurosci Lett 1988; 85-290.
154. Watts AG, Swanson LW, Sanchez-Watts G. Efferent projections of the suprachiasmatic nucleus. I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. J Comp Neurol 1987; 258: 204-229.
155. Watts AG, Swanson LW. Efferent projections of the suprachiasmatic nucleus. II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat. J Comp Neurol 1987; 258: 230-252.
156. Leak RK, Moore RY. Topographic organization of suprachiasmatic nucleus projection neurons. J Comp Neurol 2001; 433: 312-334.