Function and innervation of the locus ceruleus in a macaque model of Functional Hypothalamic Amenorrhea

Neurobiology of Disease

Volumn 50, Issue 1, 2013, Pages 96-106

  Bethea, Cynthia L ^a,b   Kim, Aaron ^a   Cameron, Judy L ^c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Amenorrhea; CRF; Dendrites; Excitotoxicity; Locus ceruleus; Macaques; Ovulation; Serotonin; Stress; Tyrosine hydroxylase

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; ESTROGEN; NORADRENALIN; SEROTONIN; TYROSINE 3 MONOOXYGENASE;

ANIMAL EUTHANASIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOVULATION; ARTICLE; BRAIN FUNCTION; CEREBELLAR PEDUNCLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DENDRITE; DISEASE MODEL; ESTROGEN SYNTHESIS; EXCITOTOXICITY; FEMALE INFERTILITY; FUNCTIONAL HYPOTHALAMIC AMENORRHEA; HYPOTHALAMIC AMENORRHEA; IMAGE ANALYSIS; INNERVATION; LOCUS CERULEUS; MACACA; MENSTRUAL CYCLE; MENTAL STRESS; METABOLIC STRESS; NEUROANATOMY; NONHUMAN; NORADRENALIN RELEASE; OVULATION; PRIORITY JOURNAL; REST;

AMENORRHEA; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOHISTOCHEMISTRY; LOCUS COERULEUS; MACACA; NOREPINEPHRINE; SEROTONIN; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL; TYROSINE 3-MONOOXYGENASE;

EID: 84868468411     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.10.009     Document Type: Article

References (82)

1. Aston-Jones G., Cohen J.D. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu. Rev. Neurosci. 2005, 28:403-450.
2. Aston-Jones G., et al. Serotonin selectively attenuates glutamate-evoked activation of noradrenergic locus coeruleus neurons. J. Neurosci. 1991, 11:760-769.
3. Aston-Jones G., et al. Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog. Brain Res. 1991, 88:501-520.
4. Aston-Jones G., et al. Afferent regulation of locus coeruleus neurons: anatomy, physiology and pharmacology. Prog. Brain Res. 1991, 88:47-75.
5. Bangasser D.A., et al. Sex differences in corticotropin-releasing factor receptor signaling and trafficking: potential role in female vulnerability to stress-related psychopathology. Mol. Psychiatry 2010, 15(877):896-904.
6. Bangasser D.A., et al. Increased vulnerability of the brain norepinephrine system of females to corticotropin-releasing factor overexpression. Mol. Psychiatry 2012, (Electronic publication ahead of print). 10.1038/mp.2012.24.
7. Berga S.L., Girton L.G. The psychoneuroendocrinology of functional hypothalamic amenorrhea. Psychiatr. Clin. North Am. 1989, 12:105-116.
8. Berga S.L., Loucks T.L. The diagnosis and treatment of stress-induced anovulation. Minerva Ginecol. 2005, 57:45-54.
9. Berga S.L., et al. Women with functional hypothalamic amenorrhea but not other forms of anovulation display amplified cortisol concentrations. Fertil. Steril. 1997, 67:1024-1030.
10. Berga S.L., et al. Recovery of ovarian activity in women with functional hypothalamic amenorrhea who were treated with cognitive behavior therapy. Fertil. Steril. 2003, 80:976-981.
11. Berod A., et al. Importance of fixation in immunohistochemisty: use of formaldehyde solutions at variable pH for the localization of tyrosine hydroxylase. J. Histochem. Cytochem. 1981, 29:844-850.
12. Bethea C.L. Regulation of progestin receptors in raphe neurons of steroid-treated monkeys. Neuroendocrinology 1994, 60:50-61.
13. Bethea C.L., et al. Anxious behavior and fenfluramine-induced prolactin secretion in young rhesus macaques with different alleles of the serotonin reuptake transporter polymorphism (5HTTLPR). Behav. Genet. 2004, 34:295-307.
14. Bethea C.L., et al. Sensitivity to stress-induced reproductive dysfunction linked to activity of the serotonin system. Fertil. Steril. 2005, 83:148-155.
15. Bethea C.L., et al. Neurobiology of stress-induced reproductive dysfunction in female macaques. Mol. Neurobiol. 2008, 38:199-230.
16. Biederman J., et al. Psychiatric correlates of behavioral inhibition in young children of parents with and without psychiatric disorders. Arch. Gen. Psychiatry 1990, 47:21-26.
17. Biller B.M.K., et al. Abnormal cortisol secretion and responses to corticotropin-releasing hormone in women with hypothalamic amenorrhea. J. Clin. Endocrinol. Metab. 1990, 70:311-317.
18. Bonne O., et al. Adaptive and maladaptive psychobiological responses to severe psychological stress: implications for the discovery of novel pharmacotherapy. Neurosci. Biobehav. Rev. 2004, 28:65-94.
19. Cameron J.L. Reproductive Dysfunction in Primates, Behaviorally Induced. Encyclopedia of Stress 2000, 366-372. Academic Press, New York. G. Fink (Ed.).
20. Cameron J.L., et al. Basal heart rate predicts development of reproductive dysfunction in response to psychological stress. 80th Annual Meeting of the Endocrine Society 1998, P1-P76.
21. Centeno M.L., et al. Corticotropin-releasing hormone and pro-opiomelanocortin gene expression in female monkeys with differences in sensitivity to stress. Neuroendocrinology 2007, 86:277-288.
22. Chang M.S., et al. Increased transcription of the tyrosine hydroxylase gene in individual locus coeruleus neurons following footshock stress. Neuroscience 2000, 101:131-139.
23. Charlety P.J., et al. Serotonin differentially modulates responses mediated by specific excitatory amino acid receptors in the rat locus coeruleus. Eur. J. Neurosci. 1993, 5:1024-1028.
24. Charney D.S. Psychobiological mechanisms of resilience and vulnerability: implications for successful adaptation to extreme stress. Am. J. Psychiatry 2004, 161:195-216.
25. Charney D.S., Deutch A. A functional neuroanatomy of anxiety and fear: implications for the pathophysiology and treatment of anxiety disorders. Crit. Rev. Neurobiol. 1996, 10:419-446.
26. Chen D., et al. Angiotensin type 1A receptors in C1 neurons of the rostral ventrolateral medulla modulate the pressor response to aversive stress. J. Neurosci. 2012, 32:2051-2061.
27. Coleman K., et al. Growth hormone response to growth hormone-releasing hormone and clonidine in young monkeys: correlation with behavioral characteristics. J. Child Adolesc. Psychopharmacol. 2003, 13:227-241.
28. Curtis A.L., et al. Predator stress engages corticotropin-releasing factor and opioid systems to alter the operating mode of locus coeruleus norepinephrine neurons. Neuropharmacology 2012, 62:1737-1745.
29. Emery D.G., Lucas J.H. Ultrastructural damage and neuritic beading in cold-stressed spinal neurons with comparisons to NMDA and A23187 toxicity. Brain Res. 1995, 692:161-173.
30. Feder A., et al. Psychobiology and molecular genetics of resilience. Nat. Rev. Neurosci. 2009, 10:446-457.
31. Fox N.A. Temperament and early experience form social behavior. Ann. N. Y. Acad. Sci. 2004, 1038:171-178.
32. Giles D.E., Berga S.L. Cognitive and psychiatric correlates of functional hypothalamic amenorrhea: a controlled comparison. Fertil. Steril. 1993, 60:486-492.
33. Gordon C.M. Clinical practice. Functional hypothalamic amenorrhea. N. Engl. J. Med. 2010, 363:365-371.
34. Haller J., et al. Catecholaminergic involvement in the control of aggression: hormones, the peripheral sympathetic, and central noradrenergic systems. Neurosci. Biobehav. Rev. 1998, 22:85-97.
35. Hasbani M.J., et al. Distinct roles for sodium, chloride, and calcium in excitotoxic dendritic injury and recovery. Exp. Neurol. 1998, 154:241-258.
36. Herbison A.E. Noradrenergic regulation of cyclic GnRH secretion. Rev. Reprod. 1997, 2:1-6.
37. Herod S.M., Bytheway J., Dolney R., Cameron J.L. Female monkeys who are sensitive to stress-induced reproductive dysfunction show increases in certain forms of anxious behavior. Annual Meeting of the Society for Neuroscience, Oct 14-18, Atlanta, GA (Abstract #257.22) 2006.
38. Herod S.M., et al. Sensitivity to stress-induced reproductive dysfunction is associated with a selective but not a generalized increase in activity of the adrenal axis. Am. J. Physiol. Endocrinol. Metab. 2011, 300:E28-E36.
39. Herod S.M., et al. Treatment with a CRH-R1 antagonist prevents stress-induced suppression of the central neural drive to the reproductive axis in female macaques. Am. J. Physiol. Endocrinol. Metab. 2011, 300:E19-E27.
40. Hsu M., Buzsaki G. Vulnerability of mossy fiber targets in the rat hippocampus to forebrain ischemia. J. Neurosci. 1993, 13:3964-3979.
41. Itoi K., Sugimoto N. The brainstem noradrenergic systems in stress, anxiety and depression. J. Neuroendocrinol. 2010, 22:355-361.
42. Jedema H.P., Grace A.A. Corticotropin-releasing hormone directly activates noradrenergic neurons of the locus ceruleus recorded in vitro. J. Neurosci. 2004, 24:9703-9713.
43. Kaehler S.T., et al. Dependence of serotonin release in the locus coeruleus on dorsal raphe neuronal activity. Naunyn Schmiedebergs Arch. Pharmacol. 1999, 359:386-393.
44. Kalin N.H., Shelton S.E. Nonhuman primate models to study anxiety, emotion regulation, and psychopathology. Ann. N. Y. Acad. Sci. 2003, 1008:189-200.
45. Kelly J.P., et al. The olfactory bulbectomized rat as a model of depression: an update. Pharmacol. Ther. 1997, 74:299-316.
46. Kim M.A., et al. Reciprocal connections between subdivisions of the dorsal raphe and the nuclear core of the locus coeruleus in the rat. Brain Res. 2004, 1026:56-67.
47. Kohama S.G., et al. Immunocytochemical colocalization of hypothalamic progestin receptors and tyrosine hydroxylase in steroid-treated monkeys. Endocrinology 1992, 131:509-517.
48. Kondoh Y., et al. A longitudinal study of disturbances of the hypothalamic-pituitary-adrenal axis in women with progestin-negative functional hypothalamic amenorrhea. Fertil. Steril. 2001, 76:748-752.
49. Laughlin G.A., et al. Nutritional and endocrine-metabolic aberrations in women with functional hypothalamic amenorrhea. J. Clin. Endocrinol. Metab. 1998, 83:25-32.
50. Lima F.B., Bethea C.L. Ovarian steroids decrease DNA fragmentation in the serotonin neurons of non-injured rhesus macaques. Mol. Psychiatry 2010, 15:657-668.
51. Lima F.B., et al. Stress sensitive female macaques have decreased fifth Ewing variant (Fev) and serotonin-related gene expression that is not reversed by citalopram. Neuroscience 2009, 164:676-691.
52. Lindenmayer J.P. The pathophysiology of agitation. J. Clin. Psychiatry 2000, 61(Suppl. 14):5-10.
53. Lukkes J.L., et al. Corticotropin-releasing factor 1 and 2 receptors in the dorsal raphe differentially affect serotonin release in the nucleus accumbens. Eur. J. Pharmacol. 2008, 578:185-193.
54. Marino M.D., et al. Genetic reduction of noradrenergic function alters social memory and reduces aggression in mice. Behav. Brain Res. 2005, 161:197-203.
55. McEwen B.S. The End of Stress As We Know It 2002, Joseph Henry Press, Washington, DC.
56. Meczekalski B., et al. Hypothalamic amenorrhea with normal body weight: ACTH, allopregnanolone and cortisol responses to corticotropin-releasing hormone test. Eur. J. Endocrinol. 2000, 142:280-285.
57. Miller R.L., et al. Serotonergic inputs to FoxP2 neurons of the pre-locus coeruleus and parabrachial nuclei that project to the ventral tegmental area. Neuroscience 2011, 193:229-240.
58. Milner T.A., et al. Ultrastructural localization of phenylethanolamine N-methyltransferase-like immunoreactivity in the rat locus coeruleus. Brain Res. 1989, 478:1-15.
59. Olney J.W. Glutamate-induced neuronal necrosis in the infant mouse hypothalamus. An electron microscopic study. J. Neuropathol. Exp. Neurol. 1971, 30:75-90.
60. Park J.S., et al. Rapid alterations in dendrite morphology during sublethal hypoxia or glutamate receptor activation. Neurobiol. Dis. 1996, 3:215-227.
61. Paxinos G., et al. The Rhesus Monkey Brain in Stereotaxic Coordinates 2000, Academic Press, New York.
62. Perkins R.B., et al. Aetiology, previous menstrual function and patterns of neuro-endocrine disturbance as prognostic indicators in hypothalamic amenorrhea. Hum. Reprod. 2001, 16:2198-2205.
63. Reul J.M., Holsboer F. Corticotropin-releasing factor receptors 1 and 2 in anxiety and depression. Curr. Opin. Pharmacol. 2002, 2:23-33.
64. Reyes B.A., et al. Hypothalamic projections to locus coeruleus neurons in rat brain. Eur. J. Neurosci. 2005, 22:93-106.
65. Sanchez R.L., et al. Ovarian steroid regulation of the midbrain corticotropin releasing factor and urocortin systems in macaques. Neuroscience 2010, 171:893-909.
66. Schulkin J. Angst and the amygdala. Dialogues Clin. Neurosci. 2006, 8:407-416.
67. Segal M. Serotonergic innervation of the locus coeruleus from the dorsal raphe and its action on responses to noxious stimuli. J. Physiol. 1979, 286:401-415.
68. Shimizu N., et al. Cellular organization of locus coeruleus in the rat as studied by Golgi method. Arch. Histol. Jpn. 1978, 41:103-112.
69. Shroff H., et al. Features associated with excessive exercise in women with eating disorders. Int. J. Eat. Disord. 2006, 39:454-461.
70. Simmons D.M., et al. A complete protocol for in situ hybridization of messenger RNAs in brain and other tissues with radio-labeled single-stranded RNA probes. J. Histotechnol. 1989, 12:169-181.
71. Strekalova T., et al. Stress-induced hyperlocomotion as a confounding factor in anxiety and depression models in mice. Behav. Pharmacol. 2005, 16:171-180.
72. Swanson L.W. The locus coeruleus: a cytoarchitectonic, Golgi and immunohistochemical study in the albino rat. Brain Res. 1976, 110:39-56.
73. Valentino R.J., et al. The locus coeruleus as a site for integrating corticotropin-releasing factor and noradrenergic mediation of stress responses. Ann. N. Y. Acad. Sci. 1993, 697:173-188.
74. Valentino R.J., et al. Corticotropin-releasing factor is preferentially colocalized with excitatory rather than inhibitory amino acids in axon terminals in the peri-locus coeruleus region. Neuroscience 2001, 106:375-384.
75. Warren M.P., Fried J.L. Hypothalamic amenorrhea. The effects of environmental stresses on the reproductive system: a central effect of the central nervous system. Endocrinol. Metab. Clin. North Am. 2001, 30:611-629.
76. Warren M.P., Stiehl A.L. Exercise and female adolescents: effects on the reproductive and skeletal systems. J. Am. Med. Womens Assoc. 1999, 54(115-20):138.
77. Weissheimer K.V., Herod S.M., Cameron J.L., Bethea C.L. Interactions of corticotropin-releasing factor, urocortin and citalopram in a primate model of stress-induced amenorrhea. Neuroendocrinology 2010, 92:224-234.
78. Williams N.I., et al. Mild metabolic stress potentiates the suppressive effect of psychological stress on reproductive function in female cynomolgus monkeys. Endocr. Soc. Abstr. 1997, (PI-367).
79. Williams N.I., et al. Evidence for a causal role of low energy availability in the induction of menstrual cycle disturbances during strenuous exercise training. J. Clin. Endocrinol. Metab. 2001, 86:5184-5193.
80. Williams N.I., et al. Synergism between psychosocial and metabolic stressors: impact on reproductive function in cynomolgus monkeys. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E270-E276.
81. Williamson D.E., et al. Heritability of fearful-anxious endophenotypes in infant rhesus macaques: a preliminary report. Biol. Psychiatry 2003, 53:284-291.
82. Xiao E., et al. Stress and the menstrual cycle: short- and long-term response to a five-day endotoxin challenge during the luteal phase in the rhesus monkey. J. Clin. Endocrinol. Metab. 1999, 84:623-626.