Glucocorticoids disrupt neuroendocrine and behavioral responses during lactation

Endocrinology

Volumn 152, Issue 12, 2011, Pages 4838-4845

  Vilela, Fabiana C ^a   Giusti Paiva, Alexandre ^a  

^a FEDERAL UNIVERSITY OF ALFENAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; DEXAMETHASONE; DRUG VEHICLE; OXYTOCIN; PROLACTIN; SODIUM CHLORIDE;

AGGRESSION; ANIMAL EXPERIMENT; ARTICLE; BITE; BLOOD SAMPLING; CAGE; CORTICOSTERONE RELEASE; FEMALE; GROOMING; HORMONAL REGULATION; LACTATION; LATENT PERIOD; MALE; MATERNAL BEHAVIOR; NEUROENDOCRINE SYSTEM; NONHUMAN; OXYTOCIN RELEASE; PRIORITY JOURNAL; PROLACTIN RELEASE; PUP (RODENT); RAT; REARING; SUCKLING; THREAT; WEIGHT GAIN;

AGGRESSION; ANIMALS; BEHAVIOR, ANIMAL; DEXAMETHASONE; FEMALE; GLUCOCORTICOIDS; LACTATION; MALE; MATERNAL BEHAVIOR; NEUROSECRETORY SYSTEMS; OXYTOCIN; PROLACTIN; RATS;

EID: 82355163414     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1096     Document Type: Article

References (83)

1. Bosch OJ 2011 Maternal nurturing is dependent on her innate anxiety: the behavioral roles of brain oxytocin and vasopressin. Horm Behav 59:202-212
2. Numan M, Stolzenberg DS 2009 Medial preoptic area interaction with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats. Front Neuroendocrinol 30: 46-64
3. Bridges RS, DiBiase R, Loundes DD, Doherty PC 1985 Prolactin stimulation of maternal behavior in female rats. Science 227: 782-784 (Pubitemid 15168273)
4. Higuchi T, Honda K, Fukuoka T, Negoro H, Wakabayashi K 1985 Release of oxytocin during suckling and parturition in the rat. J Endocrinol 105:339-346 (Pubitemid 15045849)
5. Higuchi T, Tadokoro Y, Honda K, Negoro H 1986 Detailed analysis of blood oxytocin levels during suckling and parturition in the rat. J Endocrinol 110:251-256 (Pubitemid 16035796)
6. Mann PE 2006 Finasteride delays the onset of maternal behavior in primigravid rats. Physiol Behav 88:333-338 (Pubitemid 44093604)
7. Moos F, Poulain DA, Rodriguez F, Guerne Y, Vincent JD, Richard P 1989 Release of oxytocin within the supraoptic nucleus during the milk ejection reflex in rats. Exp. Brain Res 76:593-602 (Pubitemid 19203612)
8. Neumann I, Russell JA, Landgraf R 1993 Oxytocin and vasopressin release within the supraoptic and paraventricular nuclei of pregnant, parturient and lactating rats: a microdialysis study. Neuroscience 53:65-75 (Pubitemid 23083308)
9. Taya K, Sasamoto S 1990 Involvement of the adrenal gland in the suckling-induced decrease in LH and FSH secretion and the concomitant increase in prolactin secretion in the rat. J Endocrinol 125: 279-285 (Pubitemid 20146344)
10. Giovenardi M, Padoin MJ, Cadore LP, Lucion AB 1998 Hypothalamic paraventricular nucleus modulates maternal aggression in rats: effects of ibotenic acid lesion and oxytocin antisense. Physiol Behav 63:351-359 (Pubitemid 28055562)
11. Lee HJ, Macbeth AH, Pagani JH, Young 3rd WS 2009 Oxytocin: the great facilitator of life. Prog Neurobiol 88:127-151
12. Durlo FV, Castro M, Elias LL, Antunes-Rodrigues J 2004 Interaction of prolactin, ANPergic, oxytocinergic and adrenal systems in response to extracellular volume expansion in rats. Exp Physiol 89: 541-548 (Pubitemid 39255725)
13. Lauand F, Ruginsk SG, Rodrigues HL, Reis WL, de Castro M, Elias LL, Antunes-Rodrigues J 2007 Glucocorticoid modulation of atrial natriuretic peptide, oxytocin, vasopressin and Fos expression in response to osmotic, angiotensinergic and cholinergic stimulation. Neuroscience 147:247-257 (Pubitemid 46876701)
14. Ruginsk SG, Oliveira FR, Margatho LO, Vivas L, Elias LL, Antunes- Rodrigues J 2007 Glucocorticoid modulation of neuronal activity and hormone secretion induced by blood volume expansion. Exp Neurol 206:192-200
15. Torner L, Toschi N, Nava G, Clapp C, Neumann ID 2002 Increased hypothalamic expression of prolactin in lactation: involvement in behavioural and neuroendocrine stress responses. Eur J Neurosci 15:1381-1389 (Pubitemid 35477999)
16. Brunton PJ, Russell JA, Douglas AJ 2008 Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation. J Neuroendocrinol 20:764-776 (Pubitemid 351858728)
17. ThomanEB, Levine S 1970 Hormonal and behavioral changes in the rat mother as a function of early experience treatments of the offspring. Physiol Behav 12:1417-1421
18. Hennessy MB, Harney KS, Smotherman WP, Coyle S, Levine S 1977 Adrenalectomy-induced deficits in maternal retrieval in the rat. Horm Behav 9:222-227
19. Rees SL, Panesar S, Steiner M, Fleming AS 2004 The effects of adrenalectomy and corticosterone replacement on maternal behavior in the postpartum rat. Horm Behav 46:411-419 (Pubitemid 39311909)
20. Grosvenor CE, Mena F 1983 Effect of underfeeding upon the rate of milk ejection in the lactating rat. J Endocrinol 96:215-222 (Pubitemid 13138074)
21. Haanwinckel MA, Elias LK, Favaretto AL, Gutkowska J, McCann SM, Antunes-Rodrigues J 1995 Oxytocin mediates atrial natriuretic peptide release and natriuresis after volume expansion in the rat. Proc Natl Acad Sci USA 92:7902-7906
22. Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ 1998 Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci USA 95:5335-5340 (Pubitemid 28208598)
23. Myers MM, Brunelli SA, Squire JM, Shindeldecker RD, Hofer MA 1989 Maternal behavior of SHR rats and its relationship to offspring blood pressures. Dev Psychobiol 22:29-53
24. Slamberová R, Szilágyi B, Vathy I 2001 Repeated morphine administration during pregnancy attenuates maternal behavior. Psychoneuroendocrinology 26:565-576 (Pubitemid 32524187)
25. De Almeida RM, Lucion AB 1997 8-OH-DPAT in the median raphe, dorsal periaqueductal gray and corticomedial amygdala nucleus decreases, but the medial septal area it can increase maternal aggressive behavior in rats. Psychopharmacology 134:392-400 (Pubitemid 28023414)
26. Consiglio AR, Borsoi A, Pereira GA, Lucion AB 2005 Effects of oxytocin microinjected into the central amiygdaloid nucleus and bad nucleus of stria terminalis on maternal aggressive behavior in rats. Physiol Behav 85:354-362 (Pubitemid 40840753)
27. Consiglio AR, Bridges RS 2009 Circulating prolactin, MPOA prolactin receptor expression and maternal aggression in lactating rats. Behav Brain Res 197:97-102
28. Veiga CP, Miczek KA, Lucion AB, Almeida RM 2007 Effect of 5-HT 1B receptor agonists injected into the prefrontal cortex on maternal aggression in rats. Braz J Med Biol Res 40:825-830 (Pubitemid 47009460)
29. Champagne FA, Francis DD, Mar A, Meaney MJ 2003 Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79:359-371 (Pubitemid 37098279)
30. Grosvenor CE, Shyr SW, Goodman GT, Mena F 1986 Comparison of plasma profiles of oxytocin and prolactin following suckling in the rat. Neuroendocrinology 43:679-685 (Pubitemid 16015365)
31. Taya K, Greenwald GS 1982 Mechanisms of suppression of ovarian follicular development during lactation in the rat. Biol Reprod 27: 1090-1101
32. Taya K, Sasamoto S 1989 Inhibitory effects of corticotrophin releasing factor and β-endorphin on LH and FSH secretion in the lactating rat. J Endocrinol 120:509-515 (Pubitemid 19075111)
33. Gimpl G, Fahrenholz F 2001 The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81:629-683 (Pubitemid 32267075)
34. Voogt JL, Sar M, Meites J 1969 Influence of cycling, pregnancy, labor, and suckling on corticosterone-ACTH levels. Am J Physiol 216:655-658
35. Freeman ME, Kanyicska B, Lerant A, Nagy G 2000 Prolactin: structure, function, and regulation of secretion. Physiol Rev 80:1523-1631
36. Ben-Jonathan N, Hnasko R 2001 Dopamine as a prolactin (PRL) inhibitor. Endocr Rev 22:724-763 (Pubitemid 34214293)
37. Pi XJ, Grattan DR 1999 Increased expression of both short and long form of prolactin receptor mRNA in hypothalamic nuclei of lactating rats. J Mol Endocrinol 23:13-22 (Pubitemid 29369555)
38. Walsh RJ, Slaby FJ, Posner BI 1987 A receptor-mediated mechanism for the transport of prolactin from blood to cerebrospinal fluid. Endocrinology 120:1846-1850 (Pubitemid 17069213)
39. Bridges RS, Numan M, Ronsheim PM, Mann PE, Lupini CE 1990 Central prolactin infusion stimulates maternal behavior in steroidtreated nulliparous female rats. Proc Natl Acad Sci USA 87:8003-8007
40. Melo AI, Pérez-Ledezma M, Clapp C, Arnold E, Rivera JC, Fleming AS 2009 Effects of prolactin deficiency during the early postnatal period on the development of maternal behavior in female rats: mother's milk makes the difference. Horm Behav 56:281-291
41. Lucas BK, Ormandy CJ, Binart N, Bridges RS, Kelly PA 1998 Null mutation of the prolactin receptor gene produces a defect in maternal behavior. Endocrinology 139:4102-4107 (Pubitemid 28513694)
42. Leng G, Meddle SL, Douglas AJ 2008 Oxytocin and the maternal brain. Curr Opin Pharmacol 8:731-734
43. Kendrick KM 2000 Oxytocin, motherhood and bonding. Exp Physiol 85:111S-124S (Pubitemid 30182272)
44. Neumann I, Ludwig M, Engelmann M, Pittman QJ, Landgraf R 1993 Simultaneous microdialysis in blood and brain: oxytocin and vasopressin release in response to central and peripheral osmotic stimulation and suckling in the rat. Neuroendocrinology 58:637-645 (Pubitemid 24008622)
45. Bealer SL, Crowley WR 1998 Noradrenergic control of central oxytocin release during lactation in rats. Am J Physiol 274(3 Part 1): E453-E458
46. Landgraf R, Neumann ID 2004 Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front Neuroendocrinol 25:150-176 (Pubitemid 39642188)
47. Neumann ID 2007 Stimuli and consequences of dendritic release of oxytocin within the brain. Biochem Soc Trans 35:1252-1257 (Pubitemid 350206473)
48. Fahrbach SE, Morrell JI, Pfaff DW 1985 Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 40:526-532 (Pubitemid 15042694)
49. van Leengoed E, Kerker E, Swanson HH 1987 Inhibition of postpartum maternal behaviour in the rat by injecting an oxytocin antagonist into the cerebral ventricles. J Endocrinol 112:275-282 (Pubitemid 17232626)
50. Johns JM, Noonan LR, Zimmerman LI, McMillen BA, Means LW, Walker CH, Lubin DA, Meter KE, Nelson CJ, Pedersen CA, Mason GA, Lauder JM 1998 Chronic cocaine treatment alters social/aggressive behavior in Sprague-Dawley rat dams and in their prenatally exposed offspring. Ann NY Acad Sci 846:399-404 (Pubitemid 28365421)
51. Elliott JC, Lubin DA, Walker CH, Johns JM 2001 Acute cocaine alters oxytocin levels in the medial preoptic area and amygdala in lactating rat dams: implications for cocaine-induced changes in maternal behavior and maternal aggression. Neuropeptides 35: 127-134 (Pubitemid 32575055)
52. Lubin DA, Elliott JC, Black MC, Johns JM 2003 An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior. Behav Neurosci 117:195-201 (Pubitemid 36384238)
53. Insel TR 1992 Oxytocin-a neuropeptide for affiliation: evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendocrinology 17:3-35
54. Chozick BS 1986 The behavioral effects of lesions of the amygdala: a review. Int J Neurosci 29:205-221
55. Kemble ED, Blanchard DC, Blanchard RJ 1990 Effects of regional amygdaloid lesions on flight and defensive behaviors of wild black rats (Rattus rattus). Physiol Behav 48:1-5 (Pubitemid 20248705)
56. Gammie SC, Nelson RJ 2001 cFOS and pCREB activation and maternal aggression in mice. Brain Res 898:232-241 (Pubitemid 32299952)
57. Francis DD, Champagne FC, Meaney MJ 2000 Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12:1145-1148
58. Kendrick KM, Keverne EB, Hinton MR, Goode JA 1992 Oxytocin, amino acid and monoamine release in the region of the medial preoptic area and bed nucleus of the stria terminalis of the sheep during parturition and suckling. Brain Res 569:199-209
59. Tribollet E, Dubois-Dauphin M, Dreifuss JJ, Barberis C, Jard S 1992 Oxytocin receptors in the central nervous system. Ann NY Acad Sci 652:29-38
60. Ingram CD, Wakerley JB 1993 Post-partum increase in oxytocin- induced excitation of neurons in the bed nuclei of the stria terminalis in vitro. Brain Res 602:325-330 (Pubitemid 23053204)
61. Condés-Lara M, Veinante P, Rabai M, Freund-Mercier MJ 1994 Correlation between oxytocin neuronal sensitivity and oxytocinbinding sites in the amygdala of the rat: electrophysiological and histoautoradiographic study. Brain Res 637:277-286
62. Wakerley JB, Terenzi MG, HoushamSJ, Jiang QB, Ingram CD 1998 Electrophysiological effects of oxytocin within the bed nuclei of the stria terminalis: influence of reproductive stage and ovarian steroids. Prog Brain Res 119:321-334 (Pubitemid 29099980)
63. Agrell J, Wolff JO, Ylonen H 1998 Counter-strategies to infanticide in mammals: costs and consequences. Oikos 83:507-517 (Pubitemid 29072993)
64. Numan M, Insel TR 2003 The neurobiology of parental behavior. New York: Springer Verlag
65. Tribollet E, Barberis C, Dreifuss JJ, Jard S 1988 Autoradiographic localization of vasopressin and oxytocin binding sites in rat kidney. Kidney Int 33:959-965
66. Yoshimura R, Kiyama H, Kimura T, Araki T, Maeno H, Tanizawa O, Tohyama M 1993 Localization of oxytocin receptor messenger ribonucleic acid in the rat brain. Endocrinology 133:1239-1246 (Pubitemid 23267777)
67. Veinante P, Freund-Mercier MJ 1997 Distribution of oxytocin- and vasopressin-binding sites in the rat extended amygdala: a histoautoradiographic study. J Comp Neurol 383:305-325 (Pubitemid 27280078)
68. Yoshida M, Takayanagi Y, Inoue K, Kimura T, Young LJ, Onaka T, Nishimori K 2009 Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice. J Neurosci 29:2259-2271
69. Liberzon I, Chalmers DT, Mansour A, Lopez JF, Watson SJ, Young EA 1994 Glucocorticoid regulation of hippocampal oxytocin receptor binding. Brain Res 650:317-322 (Pubitemid 24207079)
70. Liberzon I, Young EA 1997 Effects of stress and glucocorticoids on CNS oxytocin receptor binding. Psychoneuroendocrinology 22: 411-422 (Pubitemid 27431504)
71. Patchev VK, Schlosser SF, Hassan AH, Almeida OF 1993 Oxytocin binding sites in rat limbic and hypothalamic structures: site-specific modulation by adrenal and gonadal steroids. Neuroscience 57:537-543 (Pubitemid 23350544)
72. Di S, Malcher-Lopes R, Halmos KC, Tasker JG 2003 Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J Neurosci 23:4850-4857 (Pubitemid 36793211)
73. Di S, Malcher-Lopes R, Marcheselli VL, Bazan NG, Tasker JG 2005 Rapid glucocorticoid-mediated endocannabinoid release and opposing regulation of glutamate and γ-aminobutyric acid inputs to hypothalamic magnocellular neurons. Endocrinology 146:4292-4301
74. Evanson NK, Tasker JG, Hill MN, Hillard CJ, Herman JP 2010 Fast feedback inhibition of the HPA axis by glucocorticoids is mediated by endocannabinoid signaling. Endocrinology 151:4811-4819
75. Ruginsk SG, Lopes da Silva A, Ventura RR, Elias LL, Antunes- Rodrigues J 2009 Central actions of glucocorticoids in the control of body fluid homeostasis: review. Braz J Med Biol Res 42:61-67
76. Ruginsk SG, Uchoa ET, Elias LL, Antunes-Rodrigues J 2010 CB(1) modulation of hormone secretion, neuronal activation and mRNA expression following extracellular volume expansion. Exp Neurol 224:114-122
77. Wingfield JC, Sapolsky RM 2003 Reproduction and resistance to stress: when and how. J Neuroendocrinol 15:711-724 (Pubitemid 36874367)
78. Bókony V, Lendvai AZ, Liker A, Angelier F, Wingfield JC, Chastel O 2009 Stress response and the value of reproduction: are birds prudent parents? Am Nat 173:589-598
79. Shanks N, Windle RJ, Perks P, Wood S, Ingram CD, Lightman SL 1999 The hypothalamic-pituitary-adrenal axis response to endotoxin is attenuated during lactation. J Neuroendocrinol 11:857-865
80. Thoman EB, Conner RL, Levine S 1970 Lactation suppresses adrenal corticosteroid activity and aggressiveness in rats. J Comp Physiol Psychol 70:364-369
81. Hard E, Hansen S 1985 Reduced fearfulness in the lactating rat. Physiol Behav 35:641-643 (Pubitemid 16237722)
82. Ferreira A, Hansen S, Nielsen M, Archer T, Minor BG 1989 Behavior of mother rats in conflict tests sensitive to antianxiety agents. Behav Neurosci 103:193-201 (Pubitemid 19058662)
83. Neumann ID 2003 Brain mechanisms underlying emotional alterations in the peripartum period in rats. Depress Anxiety 17:111-121 (Pubitemid 36644709)