Neuroendocrine regulation of maternal behavior

Frontiers in Neuroendocrinology

Volumn 36, Issue , 2015, Pages 178-196

  Bridges, Robert S ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

Epigenetics; Estrogens; Genes; Hormone receptors; Lactogenic hormones; Maternal behavior; Maternal experience; Neural networks; Neuropeptides; Progesterone

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; ESTRADIOL; NITRIC OXIDE SYNTHASE; NITROUS OXIDE; OXYTOCIN; PROGESTERONE; PROLACTIN; PROLACTIN RECEPTOR; VASOPRESSIN; VASOPRESSIN DERIVATIVE;

BOLD SIGNAL; CENTRAL NERVOUS SYSTEM; CHILD PARENT RELATION; EPIGENETICS; GABAERGIC SYSTEM; GESTATION PERIOD; LACTATION; MATERNAL BEHAVIOR; MATERNAL CARE; MEDIAL PREOPTIC AREA; MOTIVATION; NEUROBIOLOGY; NEUROENDOCRINE SYSTEM; NEUROIMAGING; NONHUMAN; NUCLEUS ACCUMBENS; PREGNANCY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; REVIEW; REWARD; STEROIDOGENESIS; ANIMAL; FEMALE; HUMAN; NEUROSECRETION; PHYSIOLOGY;

ANIMALS; FEMALE; HUMANS; MATERNAL BEHAVIOR; NEUROSECRETORY SYSTEMS; OXYTOCIN; VASOPRESSINS;

EID: 84923873939     PISSN: 00913022     EISSN: 10956808     Source Type: Journal    
DOI: 10.1016/j.yfrne.2014.11.007     Document Type: Review

References (184)

1. Akbari E.M., Shams S., Belay H.T., Kaiguo M., Razak Z., Kent C.F., Westwood T., Sokolowski M.B., Fleming A.S. The effects of parity and maternal behavior on gene expression in the medial preoptic area and the medial amygdala in postpartum and virgin female rats: a microarray study. Behav. Neurosci. 2013, 127:913-922.
2. Alenina N., Kikic D., Todiras M., Mosienko V., Qadri F., Plehm R., Boye P., Villanovitch L., Sohr R., Tenner K., Hortnagl H., Bader M. Growth retardation and altered autonomic control in mice lacking brain serotonin. Proc. Natl. Acad. Sci. USA 2009, 106:10332-10337.
3. Anderson G.M., Grattan D.R., van der Ancker W., Bridges R.S. Reproductive experience increases prolactin responsiveness in the medial preoptic area and arcuate nucleus of female rats. Endocrinology 2006, 147:4688-4694.
4. Augustine R.A., Kokay I.C., Andrews Z.B., Ladyman S.R., Grattan D.R. Quantitation of prolactin receptor mRNA in the maternal rat brain during pregnancy and lactation. J. Mol. Endocrinol. 2003, 31:221-232.
5. Barofsky A.-L., Taylor J., Massari V.J. Dorsal raphe-hypothalamic projections provide the stimulatory serotonergic input to suckling-induced prolactin release. Endocrinology 1983, 113:1894-1903.
6. Barofsky A.-L., Taylor J., Tizabi Y., Kumar R., Jones-Quartey K. Specific neurotoxin lesions of median raphe serotonergic neurons disrupt maternal behavior in the lactating rat. Endocrinology 1983, 113:1884-1893.
7. Barrett J., Fleming A.S. Annual research review: all mothers are not created equal: neural and psychobiological perspectives on mothering and the importance of individual differences. J. Child Psychol. Psychiatry 2011, 52:368-397.
8. Baum M.J. Failure of pituitary implants to facilitate the onset of maternal behavior in ovariectomized virgin rats. Physiol. Behav. 1978, 20:87-90.
9. Beach F.A., Wilson J.R. Effects of prolactin, progesterone and estrogen on reactions of nonpregnant rats to foster young. Psychol. Rep. 1963, 13:231-239.
10. Berridge K.C., Robinson T.E. What is the role of dopamine in reward: Hedonic impact, reward learning, or incentive salience?. Brain Res. Rev. 1998, 28:309-369.
11. Bosch O.J., Neumann I.D. Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action. Horm. Behav. 2012, 61:293-303.
12. Bosch O.J., Oliver J., Neumann I.D. Brain vasopressin is an important regulator of maternal behavior independent of dams' trait anxiety. Proc. Natl. Acad. Sci. USA 2008, 105:17139-17144.
13. Bridges R.S. Long-term effects of pregnancy and parturition upon maternal responsiveness in the rat. Physiol. Behav. 1975, 14:245-249.
14. Bridges R.S. Parturition: its role in the long-term retention of maternal behavior in the rat. Physiol. Behav. 1977, 18:487-490.
15. Bridges R.S. A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology 1984, 114:930-940.
16. Bridges R.S., Byrnes E.M. Neuroendocrine regulation of maternal behavior. Neuroendocrinology in Physiology and Medicine 1999, 301-315. The Humana Press Inc., Totawa, NJ.
17. Bridges R.S., Grimm C.T. Reversal of morphine disruption of maternal behavior by concurrent treatment with the opiate antagonist naloxone. Science 1982, 218:166-168.
18. Bridges R.S., Hays L.E. Steroid-induced alterations in mRNA expression of the long-form of the prolactin receptor in the medial preoptic area of female rats: effects of exposure to a pregnancy-like regimen of progesterone and estradiol. Mol. Brain Res. 2005, 140:10-16.
19. Bridges R.S., Ronsheim P.M. Prolactin (PRL) regulation of maternal behavior in rats: bromocriptine treatment delays and PRL promotes the rapid onset of behavior. Endocrinology 1990, 126:837-848.
20. Bridges R.S., Scanlan V.F. Maternal memory in adult, nulliparous rats: effects of testing interval on the retention of maternal behavior. Dev. Psychobiol. 2005, 14:13-18.
21. Bridges R.S., Zarrow M.X., Denenberg V.H. The role of neonatal androgen in the expression of hormonally induced maternal responsiveness in the rat. Horm. Behav. 1973, 4:315-322.
22. Bridges R.S., Zarrow M.X., Goldman B.D., Denenberg V.H. A developmental study of maternal responsiveness in the rat. Physiol. Behav. 1974, 12:149-151.
23. Bridges R.S., Rosenblatt J.S., Feder H.H. Serum progesterone concentrations and maternal behavior in rats after pregnancy termination: behavioral stimulation following progesterone withdrawal and inhibition by progesterone treatment. Endocrinology 1978, 102:258-267.
24. Bridges R.S., Clifton D.K., Sawyer C.H. Postpartum luteinizing hormone release and maternal behavior in the rat after late-gestational depletion of hypothalamic norepinephrine. Neuroendocrinology 1982, 34:286-291.
25. Bridges R.S., DiBiase R., Loundes D.D., Doherty P.C. Prolactin stimulation of maternal behavior in female rats. Science 1985, 227:782-784.
26. Bridges R.S., Numan M., Ronsheim P.M., Mann P.E., Lupini C.E. Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats. Proc. Natl. Acad. Sci. USA 1990, 87(20):8003-8007.
27. Bridges R.S., Robertson M.C., Shiu R.P.C., Friesen H.G., Stuer A.M., Mann P.E. Endocrine communication between conceptus and mother: placental lactogen stimulation of maternal behavior. Neuroendocrinology 1996, 64:57-64.
28. Bridges R.S., Mann P.E., Coppeta J.S. Hypothalamic involvement in the regulation of maternal behavior in the rat: inhibitory roles for the ventromedial, dorsal and anterior hypothalamic areas. J. Neuroendocrinol. 1999, 11:259-266.
29. Bridges R.S., Rigero B.A., Byrnes E.M., Yang L., Walker A.M. Central infusions of the recombinant human prolactin antagonist, S179D-PRL, delay the onset of maternal behavior in steroid-primed, nulliparous female rats. Endocrinology 2001, 142:730-739.
30. Brown J.R., Ye H., Bronson R.T., Dikkes P., Greenberg M.E. A defect in nurturing in mice lacking the immediate early gene fosB. Cell 1996, 86:297-309.
31. Brus M., Meurisse M., Franceschini I., Keller M., Lévy F. Evidence for cell proliferation in the sheep brain and its down-regulation by parturition and interactions with the young. Horm. Behav. 2010, 58:737-746.
32. Brus M., Meurisse M., Gheusi G., Keller M., Liedo P.M., Lévy F. Dynamics of olfactory and hippocampal neurogenesis in adult sheep. J. Compar. Neurol. 2013, 52:169-188.
33. Buntin J.D. Neural and hormonal control of parental behavior in birds. Adv. Study Behav. 1996, 25:161-213.
34. Byrnes E.M., Rigero B.A., Bridges R.S. Opioid receptor antagonism during early lactation results in the increased duration of nursing bouts. Physiol. Behav. 2000, 70:211-216.
35. Byrnes E.M., Byrnes J.J., Bridges R.S. Increased sensitivity of dopamine systems following reproductive experience in rats. Pharmacol. Biochem. Behav. 2001, 68:481-489.
36. Byrnes E.M., Rigero B.A., Bridges R.S. Dopamine antagonists during parturition disrupt maternal care and the retention of maternal behavior in rats. Pharmacol. Biochem. Behav. 2002, 73:869-875.
37. Byrnes E.M., Babb J.A., Bridges R.S. Differential expression of oestrogen receptor α following reproductive experience in young and middle-aged female rats. J. Neuroendocrinol. 2009, 21:550-557.
38. Byrnes J.J., Gleason E.D., Schoen M.F., Carini L., Lovelock D.F., Byrnes E.M., Bridges R.S. Accelerated maternal responding after intra-VTA pertussis toxin treatment. Behav. Brain Res. 2011, 223:322-328.
39. Champagne F. Interplay between social experiences and the genome: epigenetic consequences for behavior. Adv. Genet. 2012, 77:33-57.
40. Champagne F., Diorio J., Sharma S., Meaney M.J. Variations in maternal care in the rat are associated with differences in estrogen-related changes in oxytocin receptor levels. Proc. Natl. Acad. Sci. USA 2001, 98:12736-12741.
41. Champagne F., Weaver I.C.G., Diorio J., Sharma S., Meaney M. Natural variations in maternal care are associated with estrogen receptor α expression and estrogen sensitivity in the medial preoptic area. Endocrinology 2003, 144:4720-4724.
42. Champagne F., Chretien P., Stevenson C.W., Zhang T.Y., Gratton A., Meaney M.J. Variations in nucleus accumbens dopamine associated with individual differences in maternal behavior in the rat. J. Neurosci. 2004, 24:4113-4123.
43. Champagne F., Weaver I.C.G., Diorio J., Dymov S., Szyf M., Meaney M. Maternal care associated with methylation of the estrogen receptor-α1b promoter and estrogen receptor-α expression in the medial preoptic area of female offspring. Endocrinology 2006, 147:2909-2915.
44. Cohen J., Bridges R.S. Retention of maternal behavior in nulliparous and primiparous rats: effects of duration of previous maternal experience. J. Compar. Physiol. Psychol. 1981, 95:450-459.
45. Cruz A.M., Maiorka P.C., Canteras N.S., Sukikara M.H., Felicio L.F. Morphine treatment during pregnancy modulates behavioral selection in lactating rats. Physiol. Behav. 2010, 101:40-44.
46. Cservenak M., Bodnar I., Usdin T.B., Palkovits M., Nagy G.M., Dobolyi A. Tuberoinfundibular peptide of 39 residues is activated during lactation and participates in the suckling-induced prolactin release in rat. Endocrinology 2010, 151:5830-5840.
47. Cservenak M., Szabo E.R., Bodnar I., Leko A., Palkovits M., Nagy G.M., Usdin T.B., Dobolyi A. Thalamic neuropeptide mediating the effects of nursing on lactation and maternal motivation. Psychoneuroendocrinology 2013, 38:3070-3084.
48. Dölen G., Darvishzadeh A., Huang K.W., Malenka R.C. Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 2013, 501:179-186.
49. Dorshkind E., Horseman N.D. The roles of prolactin, growth hormone, insulin-like growth factor-I, and thyroid hormones in lymphocyte development and function: insights from genetic models of hormone and hormone receptor deficiency. Endocr. Rev. 2000, 21:292-312.
50. Erskine M.S., Barfield R.J., Goldman B.D. Intraspecific fighting during late pregnancy and lactation in rats and effects of litter removal. Behav. Biol. 1978, 23:206-218.
51. Erskine M.S., Barfield R.J., Goldman B.D. Postpartum aggression in rats: I. Effects of hypophysectomy. J. Compar. Physiol. Psychol. 1980, 94:484-494.
52. Fahrbach S.E., Pfaff D.W. Effect of preoptic region implants of dilute estradiol on the maternal behavior of ovariectomized, nulliparous rats. Horm. Behav. 1986, 20:354-363.
53. Fahrbach S.E., Morrell J.I., Pfaff D.W. Possible role of endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 1985, 40:526-532.
54. Featherstone R.E., Fleming A.S. Plasticity in the maternal circuit: effects of experience and partum condition on brain astrocyte number in female rats. Behav. Neurosci. 2000, 114:158-172.
55. Feldman R. Oxytocin and social affiliation in humans. Horm. Behav. 2012, 61:380-391.
56. Feldman R., Gordon I., Schneiderman I., Weisman O., Zagoory-Sharon O. Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 2010, 35:1133-1141.
57. Fleming A.S., Vaccarino F., Luebke C. Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol. Behav. 1980, 25:731-743.
58. Fleming A.S., Cheung U.S., Barry M. Cycloheximide blocks the retention of maternal experience in postpartum rats. Behav. Neural Biol. 1990, 53:64-73.
59. Fleming A.S., Ruble D., Krieger H., Wong P.Y. Hormonal and experiential correlates of maternal responsiveness during pregnancy and the puerperium in human mothers. Horm. Behav. 1997, 31:145-158.
60. Fleming A.S., Steiner M., Corter C. Cortisol, hedonics, and maternal responsiveness in human mothers. Horm. Behav. 1997, 32:85-98.
61. Francis D.D., Diorio J., Liu D., Meaney M.J. Nongenomic transmission across generations in maternal behavior and stress responses in the rat. Science 1999, 286:1155-1158.
62. Freemark M., Driscoll P., Andrews J., Kelly P.A., Boyster M. Ontogenesis of prolactin receptor gene expression in the rat olfactory system: potential roles for lactogenic hormones in olfactory development. Endocrinology 1996, 137:934-942.
63. Furuta M., Bridges R.S. Effects of maternal behavior induction and pup exposure on neurogenesis in adult, virgin female rats. Brain Res. Bull. 2009, 80:408-413.
64. Gammie S.C., Nelson R.J. Maternal aggression is reduced in neuronal nitric oxide synthase-deficient mice. J. Neurosci. 1999, 19:8027-8035.
65. Gammie S.C., Negron A., Newman S.M., Rhodes J.S. Corticotropin-releasing factor inhibits maternal aggression in mice. Behav. Neurosci. 2004, 118:805-814.
66. Gammie S.C., Hasen N.S., Stevenson S.A., Bale B.L., D'Anna K.D. Elevated stress sensitivity in corticotropin-releasing factor receptor 2 deficient mice decreases maternal, but not intermale aggression. Behav. Brain Res. 2005, 160:169-177.
67. Giordano A.L., Johnson A.E., Rosenblatt J.S. Haloperidol-induced disruptions of retrieval behavior and reversal with apomorphine in lactating rats. Physiol. Behav. 1990, 48:211-214.
68. Gordon I., Zagoory-Sharon O., Schneiderman I., Leckman J.F., Weller A., Feldman R. Oxytocin and cortisol in romantically unattached young adults; associations with bonding and psychological distress. Psychophysiology 2008, 45:349-352.
69. Gordon I., Zagoory-Sharon O., Leckman J.F., Felman R. Oxytocin and the development of parenting in humans. Biol. Psychiatry 2010, 68:377-382.
70. Hansen S., Ferreira A. Effects of bicuculline infusions in the ventromedial hypothalamus and amygdaloid complex on food intake and affective behavior in mother rats. Behav. Neurosci. 1986, 100:410-415.
71. Hansen S., Harthon C., Wallin E., Lofberg L., Svensson K. The effects of 6-OHDA-induced dopamine depletions in the ventral and dorsal striatum on maternal and sexual behavior in the female rat. Pharmacol., Bioochem. Behav. 1991, 39:71-79.
72. Horseman N.D., Zhao W., Montecino-Rodriguez E., Tanaka M., Nakashima K., Engle S.J., Smith F., Markoff E., Dorshkind K. Defective mammopoiesis, but normal hematopoiesis, in mice with a targeted disruption of the prolactin gene. EMBO J. 1997, 16:6926-6935.
73. Horton T.H., Schneider J.S., Jiminez M.A., Levine J.E. Fathers behaving badly: the role of progesterone receptors. Neurobiology of the Parental Brain 2008, 449-460. Academic Press, New York, NY. R.S. Bridges (Ed.).
74. Jin D., Liu H.X., Hirai H., Torashima T., Nagai T., Lopatina O., Shnayder N.A., Yamada K., Noda M., Seike T., Fujita K., Takasawa S., Yokoyama S., Koizumi K., Shiraishi Y., Tanaka S., Hashii M., Yoshihara T., Higashida K., Islam M.S., Yamada N., Hayashi K., Noguchi N., Kato I., Okamoto H., Matsushima A., Salmina A., Munesue T., Shimizu N., Mochida S., Asano M., Higashida H. CD 38 is critical for social behaviour by regulating oxytocin secretion. Nature 2007, 446:41-45.
75. Kessler M.S., Bosch O.J., Bunck M., Landgraf R., Neumann I.D. Maternal care differs in mice bred for high vs. low trait anxiety: impact of brain vasopressin and cross-fostering. Soc. Neurosci. 2011, 6:156-168.
76. Kinsley C.H., Bridges R.S. Morphine treatment and reproductive condition alter olfactory preferences for pup and adult odors in female rats. Dev. Psychobiol. 1990, 23:331-347.
77. Kinsley C.H., Miele J., Ghiraldi L., Konen C., Svare B. Intrauterine position modulates maternal behaviors in female mice. Physiol. Behav. 1986, 36:793-799.
78. Kokay I.C., Bull P.M., Davis R.L., Ludwig M., Grattan D.R. Expression of the long form of the prolactin receptor in magnocellular oxytocin neurons is associated with specific prolactin regulation of oxytocin neurons. Am. J. Regul. Integr. Comp. Physiol. 2006, 290:1216-1225.
79. Kuroda K.O., Tachikawa K., Yoshida S., Tsuneoka Y., Numan M. Neuromolecular basis of parental behavior in laboratory mice and rats: With special emphasis on technical issues of using mouse genetics. Neuro-Psychopharmacol. Biol. Psychiatr. 2011, 35:1205-1231.
80. Ladyman S.R., Grattan D.R. Suppression of leptin receptor messenger ribonucleic acid and leptin responsiveness in the ventromedial nucleus of the hypothalamus during pregnancy in the rat. Endocrinology 2005, 146:3868-3874.
81. Larsen C.M., Grattan D.R. Prolactin-induced mitogenesis in the subventricular zone of the maternal brain during early pregnancy is essential for normal postpartum behavioral responses in the mother. Endocrinology 2010, 151:3805-3814.
82. Lee A., Li M., Watchus J., Fleming A.S. Neuroanatomical basis of maternal memory in postpartum rats: selective role for the nucleus accumbens. Behav. Neurosci. 1999, 113:523-538.
83. Levine A., Zagoory-Sharon O., Feldman R., Weller A. Oxytocin during pregnancy and early postpartum: individual patterns and maternal-fetal attachment. Peptides 2007, 28:1162-1169.
84. Lévy F., Poindron P. The importance of amniotic fluids for the establishment of maternal behaviour in experienced and non-experienced ewes. Anim. Behav. 1987, 35:1188-1192.
85. Lévy F., Gervais R., Kinderman U., Orgeur P. Importance of β-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. Behav. Neurosci. 1990, 104:464-469.
86. Lévy F., Guevara-Guzman R., Hinton M.R., Kendrick K.M., Keverne E.B. Effects of parturition and maternal experience on noradrenaline and acetylcholine release in the olfactory bulb of sheep. Behav. Neurosci. 1993, 107:662-668.
87. Li M., Fleming A.S. The nucleus accumbens shell is critical for normal expression of pup-retrieval in postpartum female rats. Behav. Brain Res. 2003, 145:99-111.
88. Li M., Fleming A.S. Differential involvement of nucleus accumbens shell and core subregions in maternal memory in postpartum female rats. Behav. Neurosci. 2003, 117:426-445.
89. Lonstein J.S. Regulation of anxiety during the postpartum period. Front. Neuroendocrinol. 2007, 28:115-141.
90. Lonstein J.S., Gammie S.C. Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neurosci. Biobehav. Rev. 2002, 26:869-888.
91. Lott D.L., Fuchs S.S. Failure to induce retrieving by sensitization or the injection of prolactin. J. Compar. Physiol. Psychol. 1962, 65:111-113.
92. Lucas B.K., Ormandy C.J., Binart N., Bridges R.S., Kelly P.A. Null mutation of the prolactin receptor gene produces a defect in maternal behavior. Endocrinology 1998, 139:4102-4107.
93. Lydon J.P., DeMayo F.J., Funk C.R., Mani S.K., Hughes A.R., Montgomery C.A., Shyamala G., Conneely O.M., O'Malley B.W. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev. 1995, 9:2266-2278.
94. Mani S.K., Blaustein J.D., O'Malley B.W. Progesterone receptor function from a behavioral perspective. Horm. Behav. 1997, 31:244-255.
95. Mann P.E. Finasteride delays the onset of maternal behavior in primigravid rats. Physiol. Behav. 2006, 88:333-338.
96. Mann P.E., Bridges R.S. Neural and endocrine sensitivities to opioids decline as a function of multiparity in rats. Brain Res. 1992, 580:241-248.
97. Mann P.E., Kinsley C.H., Bridges R.S. Opioid receptor subtype involvement in maternal behavior in lactating rats. Neuroendocrinology 1991, 53:487-492.
98. Mayer A.D., Rosenblatt J.S. Prepartum changes in maternal responsiveness and nest-defense in Rattus norvegicus. J. Comp. Psychol. 1984, 98:177-188.
99. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 2001, 24:1161-1192.
100. Meaney M.J., Szyf M. Maternal care as a model for experience-dependent chromatin plasticity?. Trends Neurosci. 2005, 28:456-463.
101. Meurisse M., Gonzalez A., Delsol G., Caba M., Levy F., Poindron P. Estradiol receptor-α expression in hypothalamic and limbic regions of ewes is influenced by physiological state and maternal experience. Horm. Behav. 2005, 48:34-43.
102. 2 receptor antagonism in the preoptic area produces different effects on maternal behavior in lactating rats. Behav. Neurosci. 2005, 119:1072-1083.
103. Moltz H., Robbins D. Maternal behavior of primiparous and multiparous rats. J. Compar. Physiol. Psychol. 1965, 60:417-421.
104. Moltz H., Robbins D., Parks M. Caesarean delivery and maternal behavior of primiparous and multiparous rats. J. Compar. Physiol. Psychol. 1966, 61:455-460.
105. Moltz H., Lubin M., Leon M., Numan M. Hormonal induction of maternal behavior in the ovariectomized nulliparous rat. Physiol. Behav. 1970, 5:1373-1377.
106. Morice E., Denis C., Giros B., Nosten-Bertrand M. Phenotypic expression of the targeted null-mutation in the dopamine transporter gene varies as a function of the genetic background. Eur. J. Neurosci. 2004, 20:120-126.
107. Morishige W.K., Pepe G.J., Rothchild I. Serum luteinizing hormone, prolactin and progesterone levels during pregnancy in the rat. Endocrinology 1973, 92:1527-1530.
108. Nephew B.C., Bridges R.S. Arginine vasopressin V1a receptor antagonist impairs maternal memory in rats. Physiol. Behav. 2008, 95:182-186.
109. Nephew B.C., Bridges R.S. Central actions of arginine vasopressin and V1a receptor antagonist on maternal aggression, maternal behavior, and grooming in lactating rats. Pharmacol. Biochem. Behav. 2008, 91:77-83.
110. Nephew B.C., Bridges R.S., Lovelock D.F., Byrnes E.M. Enhanced maternal aggression and associated changes in neuropeptide gene expression in multiparous rats. Behav. Neurosci. 2009, 123:949-957.
111. Nephew B.C., Byrnes E.M., Bridges R.S. Vasopressin mediates enhanced offspring protection in multiparous rats. Neuropharmacology 2010, 58:102-106.
112. Nishimori K., Young L.J., Guo Q., Wang Z., Insel T.R., Matzuk M.M. Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proc. Natl. Acad. Sci. USA 1996, 93:11699-16704.
113. Numan M. Medial preoptic area and maternal behavior in the female rat. J. Compar. Physiol. Psychol. 1974, 87:746-759.
114. Numan M. Progesterone inhibition of maternal behavior in the female rat. Horm. Behav. 1978, 11:209-231.
115. Numan M. Maternal behavior: neural circuits, stimulus valence, and motivational processes. Parent., Sci. Pract. 2012, 12:105-114.
116. Numan M., Callahan E.C. The connections of the medial preoptic region and maternal behavior in the rat. Physiol. Behav. 1980, 25:653-665.
117. Numan M., Smith H.G. Maternal behavior in rats: evidence for the involvement of preoptic projections to the ventral tegmental area. Behav. Neurosci. 1984, 98:712-727.
118. Numan M., Rosenblatt J.S., Komisauruk B.R. Medial preoptic area and onset of maternal behavior in the rat. J. Compar. Physiol. Psychol. 1977, 91:146-164.
119. Numan M., Roach J.K., del Cerro M.C.R., Guillamon A., Segovia S., Sheehan T.P., Numan M.J. Expression of intracellular progesterone receptors in the rat brain during different reproductive states, and involvement in maternal behavior. Brain Res. 1999, 830:358-371.
120. 2 receptor antagonism in the medial preoptic area, ventral pallidum, or nucleus accumbens on maternal retrieval response and other aspects of maternal behavior in rats. Behav. Neurosci. 2005, 119:1588-1604.
121. Ogawa S., Eng V., Taylor J., Lubahn D.B., Korach K.S., Pfaff D.W. Roles of estrogen receptor-α gene expression in reproduction-related behaviors in female mice. Endocrinology 1998, 139:5070-5081.
122. Ormandy C.J., Camus A., Barra J., Damotte D., Lucas B., Buteau H., Edery M., Brousse N., Babinet C., Binart N., Kelly P.A. Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev. 1997, 11:167-178.
123. Panksepp J., Nelson E., Siviy S. Brain opioids and mother-infant social motivation. Acta Paediatr. Suppl. 1994, 397:40-46.
124. Parada M., King S., Li M., Fleming A. The roles of accumbal dopamine D1 and D2 receptors in maternal memory in rats. Behav. Neurosci. 2008, 122:368-376.
125. Peake G.T., Buckman M.T., Davis L.E., Standefer J. Pituitary and placentally derived hormones in cerebrospinal fluid during normal human pregnancy. J. Clin. Endocrinol. Metab. 1983, 56:46-52.
126. Pedersen C., Boccia M. Oxytocin antagonism alters rat dams' oral grooming and upright posturing over pups. Physiol. Behav. 2003, 80:233-241.
127. Pedersen C.A., Asher J.A., Monroe Y.L., Prange A.J. Oxytocin induces maternal behavior in virgin female rats. Science 1982, 216:648-650.
128. Pedersen C.A., Caldwell J.D., Walker C., Ayers G., Mason G.A. Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav. Neurosci. 1994, 108:1163-1171.
129. Pedersen C.A., Vadlamudi S.V., Boccia M., Amico J.A. Maternal behavior deficits in nulliparous oxytocin knockout mice. Genes Brain Behav. 2006, 5:274-281.
130. Peña C.J., Neugut D., Champagne F.A. Developmental timing of the effects of maternal care on gene expression and epigenetic regulation of hormone receptor levels in female rats. Endocrinology 2013, 154:4340-4351.
131. Pereira M., Ferreira A. Demanding pups improve maternal behavior impairments in sensitized and haloperidol-treated lactating female rats. Behav. Brain Res. 2006, 175:139-148.
132. Pfaff D., Waters E., Khan Q., Zhang X., Numan M. Minireview: estrogen receptor-initiated mechanisms causal to mammalian reproductive behaviors. Endocrinology 2011, 152:1209-1217.
133. Pissonier D., Thiéry J.C., Fabre-Nys C., Poindron P., Keverne E.B. The importance of olfactory bulb noradrenalin for maternal recognition in sheep. Physiol. Behav. 1985, 35:361-364.
134. Poindron P., Levy F., Krehbiel D. Genital, olfactory and endocrine interactions in the development of maternal behaviour in the parturient ewe. Psychoneuroendocrinology 1988, 13:99-125.
135. Popeski N., Woodside B. Central nitric oxide synthase inhibition disrupts maternal behavior in the rat. Behav. Neurosci. 2004, 118:1305-1316.
136. Price A.K., Bridges R.S. The effects of bromocriptine treatment during early pregnancy on postpartum maternal behaviors in rats. Dev. Psychobiol. 2014, 56:1431-1437.
137. Quadagno D.M., Rockwell J. The effect of gonadal hormones in infancy on maternal behavior in the adult rat. Horm. Behav. 1972, 3:55-62.
138. Ribeiro A.C., Musatov S., Shteyler A., Simanduyev S., Arrieta-Cruz I., Ogawa S., Pfaff D.W. SiRNA silencing of estrogen receptor expression specifically in the medial preoptic area neurons abolishes maternal care in female mice. Proc. Natl. Acad. Sci. USA 2012, 109:16324-16329.
139. Riddle O., Lahr E.L., Bates R.W. Maternal behavior induced in virgin rats by prolactin. Proc. Soc. Exp. Biol. Med. 1935, 32:730-734.
140. Riem M.M.E., Bakersman-Kranenburg M.J., Pieper S., Tops M., Boksem M.A.S., Vermeiren R.R.J.M., van IJzendoorn M.H., Rombouts S.A.R.B. Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial. Biol. Psychiatr. 2011, 70:291-297.
141. Rilling J.K., Young L.J. The biology of mammalian parenting and its effect on offspring social development. Science 2014, 345:771-776.
142. Robertson M.C., Friesen H.G. Two forms of placental lactogen revealed by radioimmunoassay. Endocrinology 1981, 108:2388-2390.
143. Rosenberg P., Halaris A., Moltz H. Effects of central norepinephrine depletion on the initiation and maintenance of maternal behavior in the rat. Pharmacol. Biochem. Behav. 1977, 6:21-24.
144. Rosenblatt J.S. Nonhormonal basis of maternal behavior in the rat. Science 1967, 156:1512-1513.
145. Rubin B.S., Bridges R.S. Disruption of ongoing maternal responsiveness in rats by central administration of morphine sulfate. Brain Res. 1984, 307:91-97.
146. Rumi M.A.K., Dhakal P., Kubota K., Chakraborty D., Lei T., Larson M.A., Wolfe M.W., Roby K.F., Vivian J.L., Soares M.J. Generation of ESR1 knockout rats using zinc finger nuclease-mediated genome editing. Endocrinology 2014, 155:1991-1999.
147. Ruppenthal G.C., Arling G.L., Harlow H.F., Sackett G.P., Suomi S.J. A 10-year perspective of motherless-mother behavior. J. Abnorm. Psychol. 1976, 85:341-349.
148. Salmina A.B., Lopatina O., Ekimova M.V., Mikhutkina S.V., Higashida H. CD 38/cyclic ADP-ribose system: a new player for oxytocin secretion and regulation of social behaviour. J. Neuroendocrinol. 2010, 22:380-392.
149. Scanlan V.F., Byrnes E.M., Bridges R.S. Reproductive experience and activation of maternal memory. Behav. Neurosci. 2006, 120:676-686.
150. Schechter M., Pinhasov A., Weller A., Fride E. Blocking the postpartum mouse dam's CB1 receptors impairs maternal behavior as well as offspring development and their adult social-emotional behavior. Behav. Brain Res. 2012, 226:481-492.
151. Shahrokh D.K., Zhang T.-Y., Diorio J., Gratton A., Meaney M.J. Oxytocin-dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology 2010, 151:2276-2286.
152. Shingo T., Gregg C., Enwere E., Fujiwawa H., Hassam R., Geary C., Cross J.C., Weiss S. Pregnancy-stimulated neurogenesis in the adult female forebrain. Science 2004, 299:117-120.
153. Siegel H.I., Rosenblatt J.S. Hormonal basis of hysterectomy-induced maternal behavior during pregnancy in the rat. Horm. Behav. 1975, 6:211-222.
154. Siegel H.I., Rosenblatt J.S. Estrogen-induced maternal behavior in hysterectomized-ovariectomized virgin rats. Physiol. Behav. 1975, 14:465-471.
155. Silva M.R., Bernardi M.M., Felicio L.F. Effects of dopamine receptor antagonists on ongoing maternal behavior in rats. Pharmacol. Biochem. Behav. 2001, 68:461-468.
156. Slotnick B.M., Carpenter M.L., Fusco R. Initiation of maternal behavior in pregnant nulliparous rats. Horm. Behav. 1973, 4:53-59.
157. Smith C.D., Holschback M.A., Olsewicz J., Lonstein J.S. Effects of noradrenergic alpha-2 receptor antagonism or noradrenergic lesions in the ventral bed nucleus of the stria terminalis and medial preoptic area on maternal care in female rats. Psychopharmacology 2012, 224:263-276.
158. Spielewoy C., Roubert C., Hamon M., Nosten-Bertrand M., Betancur C., Giros B. Behavioural disturbances associated with hyperdopaminergia in dopamine-transporter knockout mice. Behav. Pharmacol. 2000, 11:279-290.
159. Steele M.K., Rowland D., Moltz H. Initiation of maternal behavior in the rat: possible involvement of limbic norepinephrine. Pharmacol. Biochem. Behav. 1979, 11:123-130.
160. Stjernholm-Vladic Y., Wang H., Stygar D., Ekman G., Sahlin L. Differential regulation of the progesterone receptor A and B in the human uterine cervix at parturition. Gynecol. Endocrinol. 2004, 18:41-46.
161. 1 receptor stimulation of the nucleus accumbens or the medial preoptic area promotes the onset of maternal behavior in pregnancy-terminated rats. Behav. Neurosci. 2007, 121:907-919.
162. Stolzenberg D.S., Stevens J.S., Rissman E.F. Experience-facilitated improvements in pup retrieval: evidence for an epigenetic effect. Horm. Behav. 2012, 62:128-135.
163. Sukikara M.H., Platero M.D., Canteras N.S., Felicio L.F. Opiate regulation of behavioral selection during lactation. Pharmacol. Biochem. Behav. 2007, 87:315-320.
164. Svare B.B. Maternal aggression: hormonal, genetic, and developmental determinants. Mammalian Parenting: Biochemical, Neurobiological and Behavioral Determinants 1990, 118-132. Oxford University Press, New York, NY.
165. Swain J.E., Leckman J.F., Mayes L.C., Feldman R., Hoyt E., Kang H., Kim P., Schultz R.T. Baby cry and picture activations of parent brains vary with gender, experience, and dyadic relationship. Biol. Psychiatry 2007, 61:S103.
166. Swain J.E., Kim P., Ho S.S. Neuroendocrinology of parental response to baby-cry. J. Neuroendocrinol. 2011, 23:1036-1041.
167. Takayanagi Y., Yoshida M., Bielsky I.F., Ross H.E., Kawamata M., Onaka T., Yanagisawa T., Kimura T., Matzuk M.M., Young L.J., Nishimori K. Pervasive social deficits, but normal parturition, in oxytocin receptor deficient mice. Proc. Natl. Acad. Sci. USA 2005, 102:16096-16101.
168. Terkel J., Rosenblatt J.S. Aspects of nonhormonal maternal behavior in the rat. Horm. Behav. 1971, 2:161-171.
169. Terkel J., Rosenblatt J.S. Humoral factors underlying maternal behavior at parturition: cross transfusion between freely moving rats. J. Compar. Physiol. Psychol. 1972, 80:365-371.
170. Thijssen J.H.H. Progesterone receptors in the human uterus and their possible role in parturition. J. Steroid Biochem. Mol. Biol. 2005, 97:397-400.
171. Thomas S.A., Palmiter R.D. Impaired maternal behavior in mice lacking norepinephrine and epinephrine. Cell 1997, 91:583-592.
172. Tindal J.S., Knaggs G.S. Pathways in the forebrain of the rat concerned with the release of prolactin. Brain Res. 1977, 119:211-221.
173. Vom saal F.S., Bronson F.H. In utero proximity of female mouse fetuses to males: effect on reproductive performance during later life. Biol. Reprod. 1978, 19:842-853.
174. Walsh R.J., Slaby F.J., Posner B.I. A receptor-mediated mechanism for the transport of prolactin from blood to cerebrospinal fluid. Endocrinology 1987, 120:1846-1850.
175. Wamboldt M.Z., Insel T.R. The ability of oxytocin to induce short latency maternal behavior is dependent on peripheral anosmia. Behav. Neurosci. 1987, 101:439-441.
176. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Secki J.R., Dymov S., Szyf M., Meaney M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7:847-854.
177. Weaver I.C., Diorio J., Secki J.R., Szyr M., Meaney M.J. Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of intracellular mediators and potential genomic trigger sites. Annals New York Acad. Sci. 2004, 1024:182-212.
178. Weisman O., Delaherche E., Rondeau M., Chetouani M., Cohen D., Feldman R. Oxytocin shapes parental motion during father-infant interaction. Biol. Lett. 2013, 9:20130828.
179. Wu Z., Autry A.E., Bergan J.F., Watabe-Uchida M., Dulac C.G. Galanin neurons in the medial preoptic area govern parental behaviour. Nature 2014, 509:325-330.
180. Young W.S., Shepard E., Amico J., Hennighausen L., Wagner K.U., LaMarca M.E., McKinney C., Ginns E.I. Deficiency in mouse oxytocin prevents milk ejection, but not fertility or parturition. J. Neuroendocrinol. 1996, 8:847-853.
181. Young L.J., Wang Z., Insel T.R. Neuroendocrine bases of monogamy. Trends Neurosci. 1998, 21:71-75.
182. Zakar T., Hertelendy F. Progesterone withdrawal: key to parturition. Am. J. Obstet. Gynecol. 2007, 196:289-296.
183. Zarrow M.X., Gandelman R., Denenberg V.H. Prolactin: is it an essential hormone for maternal behavior in mammals?. Horm. Behav. 1971, 2:343-354.
184. Zwain I.H., Yen S.S. Neurosteroidogenesis in astrocytes, oligodendrocytes, and neurons of cerebral cortex of rat brain. Endocrinology 1999, 140:3843-3852.