Functional significance of hormonal changes in mammalian fathers

Journal of Neuroendocrinology

Volumn 26, Issue 10, 2014, Pages 685-696

  Saltzman, W ^a   Ziegler, T E ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

Author keywords

Anxiety; Biparental care; Energy balance; Neurogenesis; Paternal behaviour; Stress

Indexed keywords

ANDROGEN; ESTROGEN; GLUCOCORTICOID; NEUROPEPTIDE; OXYTOCIN; PROGESTERONE; PROLACTIN; TESTOSTERONE; VASOPRESSIN; HORMONE;

BODY COMPOSITION; COGNITION; EMOTIONALITY; ENERGY BALANCE; FATHER; FUNCTIONAL STATUS; HORMONAL REGULATION; NERVE CELL PLASTICITY; NONHUMAN; PATERNAL BEHAVIOR; PRIORITY JOURNAL; REVIEW; SMELLING; SPECIES DIFFERENCE; STRESS; ANIMAL; ANIMAL BEHAVIOR; MALE; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; FATHERS; HORMONES; MALE; NEURONAL PLASTICITY;

EID: 84925013734     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12176     Document Type: Review

References (106)

1. Freeman ME, Kanyicska B, Lerant A, Nagy G. Prolactin: structure, function, and regulation of secretion. Physiol Rev 2000; 80: 1523-1631.
2. Neumann ID. Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J Neuroendocrinol 2008; 20: 858-865.
3. Spencer TE, Bazer FW. Conceptus signals for establishment and maintenance of pregnancy. Reprod Biol Endocrinol 2004; 2: 49.
4. Numan M, Insel TR. The Neurobiology of Parental Behavior. New York, NY: Springer, 2003.
5. Ladyman SR, Augustine RA, Grattan DR. Hormone interactions regulating energy balance during pregnancy. J Neuroendocrinol 2010; 22: 5-817.
6. Woodside B, Budin R, Wellman MK, Abizaid A. Many mouths to feed: the control of food intake during lactation. Front Neuroendocrinol 2012; 33: 301-314.
7. Bouman A, Heineman MJ, Faas MM. Sex hormones and the immune response in humans. Hum Reprod Update 2005; 11: 411-423.
8. Kinsley CH, Lambert KG. Reproduction-induced neuroplasticity: natural behavioural and neuronal alterations associated with the production and care of offspring. J Neuroendocrinol 2008; 20: 515-525.
9. Leuner B, Glasper ER, Gould E. Parenting and plasticity. Trends Neurosci 2010; 33: 465-473.
10. Lévy F, Gheusi G, Keller M. Plasticity of the parental brain: a case for neurogenesis. J Neuroendocrinol 2011; 23: 984-993.
11. Galea LAM, Leuner B, Slattery D. Hippocampal plasticity during the peripartum period: influence of sex steroids, stress and ageing. J Neuroendocrinol (in press).
12. Macbeth AH, Luine VN. Changes in anxiety and cognition due to reproductive experience: a review of data from rodent and human mothers. Neurosci Biobehav Rev 2010; 34: 452-467.
13. Pawluski JL, Brummelte S, Barha CK, Crozier TM, Galea LAM. Effects of steroid hormones on neurogenesis in the hippocampus of the adult female rodent during the estrous cycle, pregnancy, lactation and aging. Front Neuroendocrinol 2009; 30: 343-357.
14. Miranda JA, Liu RC. Dissecting natural sensory plasticity: hormones and experience in a maternal context. Hear Res 2009; 252: 21-28.
15. Lonstein JS, Maguire J, Meinlschmidt G, Neumann I. Emotion and mood adaptations in the peripartum female: complementary contributions of gamma-aminobutyric acid and oxytocin. J Neuroendocrinol (in press).
16. Brunton PJ, Russell JA, Douglas AJ. Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation. J Neuroendocrinol 2008; 20: 764-776.
17. Kleiman DG, Malcolm JR. The evolution of male parental investment in mammals. In: Gubernick DJ, Klopfer PH, eds. Parental Care in Mammals. New York, NY: Plenum, 1981: 347-387.
18. Woodroffe R, Vincent A. Mother's little helpers: patterns of male care in mammals. Trends Ecol Evol 1994; 8: 294-297.
19. Fernandez-Duque E, Valeggia CR, Mendoza SP. The biology of paternal care in human and nonhuman primates. Annu Rev Anthropol 2009; 38: 115-130.
20. Kentner AC, Abizaid A, Bielajew C. Modeling dad: animal models of paternal behavior. Neurosci Biobehav Rev 2010; 34: 438-451.
21. Champagne F, Braun K. Paternal influences on offspring development: behavioural and epigenetic pathways. J Neuroendocrinol (in press).
22. Campbell JC, Laugero KD, Van Westerhuyzen JA, Hostetler CM, Cohen JD, Bales KL. Costs of pair-bonding and paternal care in male prairie voles (Microtus ochrogaster). Physiol Behav 2009; 98: 367-373.
23. Wynne-Edwards KE, Timonin ME. Paternal care in rodents: weakening support of hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care. Horm Behav 2007; 52: 114-121.
24. Nunes S, Fite JE, Patera KJ, French JA. Interactions among paternal behavior, steroid hormones, and parental experience in male marmosets (Callithrix kuhlii). Horm Behav 2001; 39: 70-82.
25. Ziegler TE, Snowdon CT. Preparental hormone levels and parenting experience in male cotton-top tamarins, Saguinus oedipus. Horm Behav 2000; 38: 159-167.
26. Brown RE, Murdoch T, Murphy PR, Moger WH. Hormonal responses of male gerbils to stimuli from their mate and pups. Horm Behav 1995; 29: 474-491.
27. Gubernick DJ, Nelson RJ. Prolactin and paternal behavior in the biparental California mouse, Peromyscus californicus. Horm Behav 1989; 23: 203-210.
28. Reburn CJ, Wynne-Edwards KE. Hormonal changes in males of a naturally biparental and a uniparental mammal. Horm Behav 1999; 35: 163-176.
29. Ma E, Lau J, Grattan DR, Lovejoy DA, Wynne-Edwards KE. Male and female prolactin receptor mRNA expression in the brain of a biparental and a uniparental hamster, Phodopus, before and after the birth of a litter. J Neuroendocrinol 2005; 17: 81-90.
30. Ziegler TE, Wegner FH, Snowdon CT. Hormonal responses to parental and nonparental conditions in male cotton-top tamarins, Saguinus oedipus, a New World primate. Horm Behav 1996; 30: 287-297.
31. Ziegler TE, Prudom SL, Zahed SR, Parlow AF, Wegner F. Prolactin's mediative role in male parenting in parentally experienced marmosets (Callithrix jacchus). Horm Behav 2009; 56: 436-443.
32. Dixson AF, George L. Prolactin and parental behaviour in a male New World primate. Nature 1982; 299: 551-553.
33. Gettler LT, McDade TW, Feranil AB, Kuzawa CW. Prolactin, fatherhood, and reproductive behavior in human males. Am J Phys Anthropol 2012; 148: 362-370.
34. Ziegler TE, Washabaugh KF, Snowdon CT. Responsiveness of expectant male cotton-top tamarins, Saguinus oedipus, to mate's pregnancy. Horm Behav 2004; 45: 84-92.
35. Gettler LT, McDade TW, Feranil AB, Kuzawa CW. Longitudinal evidence that fatherhood decreases testosterone in human males. Proc Natl Acad Sci USA 2011; 108: 16194-16199.
36. Trainor BC, Bird IM, Alday NA, Schlinger BA, Marler CA. Variation in aromatase activity in the medial preoptic area and plasma progesterone is associated with the onset of paternal behavior. Neuroendocrinology 2003; 78: 36-44.
37. Schum JE, Wynne-Edwards KE. Estradiol and progesterone in paternal and non-paternal hamsters (Phodopus) becoming fathers: conflict with hypothesized roles. Horm Behav 2005; 47: 410-418.
38. Timonin ME, Cushing BS, Wynne-Edwards KE. In three brain regions central to maternal behaviour, neither male nor female Phodopus dwarf hamsters show changes in oestrogen receptor alpha distribution with mating or parenthood. J Neuroendocrinol 2008; 20: 1301-1309.
39. Song Z, Tai F, Yu C, Wu R, Zhang X, Broders H, He F, Guo R. Sexual or paternal experiences alter alloparental behavior and the central expression of ERα and OT in male mandarin voles (Microtus mandarinus). Behav Brain Res 2010; 214: 290-300.
40. Nunes S, Fite JE, French JA. Variations in steroid hormones associated with infant care behaviour and experience in male marmosets (Callithrix kuhlii). Anim Behav 2000; 60: 857-865.
41. Berg SJ, Wynne-Edwards KE. Salivary hormone concentrations in mothers and fathers becoming parents are not correlated. Horm Behav 2002; 42: 424-436.
42. Chauke M, Malisch JL, Robinson C, de Jong TR, Saltzman W. Effects of reproductive status on behavioral and endocrine responses to acute stress in a biparental rodent, the California mouse (Peromyscus californicus). Horm Behav 2011; 60: 128-138.
43. Harris BN, Saltzman W. Effect of reproductive status on hypothalamic-pituitary-adrenal (HPA) activity and reactivity in male California mice (Peromyscus californicus). Physiol Behav 2013; 112-113: 70-76.
44. Fleming AS, Corter C, Stallings J, Steiner M. Testosterone and prolactin are associated with emotional responses to infant cries in new fathers. Horm Behav 2002; 42: 399-413.
45. Gray PB, Parking JC, Samms-Vaughan ME. Hormonal correlates of human paternal interactions: a hospital-based investigation in urban Jamaica. Horm Behav 2007; 52: 499-507.
46. Bamshad M, Novak MA, De Vries GJ. Sex and species differences in the vasopressin innervation of sexually naïve and parental prairie voles, Microtus ochrogaster and meadow voles, Microtus pennsylvanicus. J Neuroendocrinol 1993; 5: 247-255.
47. Bamshad M, Novak MA, De Vries GJ. Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster). Physiol Behav 1994; 56: 751-758.
48. Wang ZX, Liu Y, Young LJ, Insel TR. Hypothalamic vasopressin gene expression increases in both males and females postpartum in a biparental rodent. J Neuroendocrinol 2000; 12: 111-120.
49. De Jong TR, Harris BN, Perea-Rodriguez JP, Saltzman W. Physiological and neuroendocrine responses to chronic variable stress in male California mice (Peromyscus californicus): influence of social environment and paternal state. Psychoneuroendocrinology 2013; 38: 2023-2033.
50. Kozorovitskiy Y, Hughes M, Lee K, Gould E. Fatherhood affects dendritic spines and vasopressin V1a receptors in the primate prefrontal cortex. Nat Neurosci 2006; 9: 1094-1095.
51. Parker KJ, Kinney LF, Phillips KM, Lee TM. Paternal behavior is associated with central neurohormone receptor binding patterns in meadow voles (Microtus pennsylvanicus). Behav Neurosci 2001; 115: 1341-1348.
52. Gubernick DJ, Winslow JT, Jensen P, Jeanotte L, Bowen J. Oxytocin changes in males over the reproductive cycle in the monogamous, biparental California mouse, Peromyscus californicus. Horm Behav 1995; 29: 59-73.
53. Churchland PS, Winkielman P. Modulating social behavior with oxytocin: how does it work? What does it mean? Horm Behav 2012; 61: 392-399.
54. Brown RE. Hormonal and experiential factors influencing parental behaviour in male rodents: an integrative approach. Behav Processes 1993; 30: 1-28.
55. Roberts RL, Jenkins KT, Lawler T Jr, Wegner FH, Newman JD. Bromocriptine administration lowers serum prolactin and disrupts parental responsiveness in common marmosets (Callithrix j. jacchus). Horm Behav 2001; 39: 106-112.
56. Almond REA, Brown GR, Keverne EB. Suppression of prolactin does not reduce infant care by parentally experienced male common marmosets (Callithrix jacchus). Horm Behav 2006; 49: 673-680.
57. Sakaguchi K, Tanaka M, Ohkubo T, Doh-ura K, Fujikawa T, Sudo S, Nakashima K. Induction of brain prolactin receptor long-form mRNA expression and maternal behavior in pup-contacted male rats: promotion by prolactin administration and suppression by female contact. Neuroendocrinology 1996; 63: 559-568.
58. Brooks PL, Vella ET, Wynne-Edwards KE. Dopamine agonist treatment before and after the birth reduces prolactin concentration but does not impair paternal responsiveness in Djungarian hamsters, Phodopus campbelli. Horm Behav 2005; 47: 358-366.
59. Schradin C, Anzenberger G. Prolactin, the hormone of paternity. News Physiol Sci 1999; 14: 223-231.
60. Hume JM, Wynne-Edwards KE. Castration reduces male testosterone, estradiol, and territorial aggression, but not paternal behavior in biparental dwarf hamsters (Phodopus campbelli). Horm Behav 2005; 48: 303-310.
61. Lonstein JS, De Vries GJ. Sex differences in the parental behaviour of adult virgin prairie voles: independence from gonadal hormones and vasopressin. J Neuroendocrinol 1999; 11: 441-449.
62. Clark MM, Galef BG Jr. A testosterone-mediated trade-off between parental and sexual effort in male Mongolian gerbils (Meriones unguiculatus). J Comp Psychol 1999; 113: 388-395.
63. Wang Z, De Vries GJ. Testosterone effects on paternal behavior and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster). Brain Res 1993; 631: 156-160.
64. Trainor BC, Marler CA. Testosterone, paternal behavior, and aggression in the monogamous California mouse (Peromyscus californicus). Horm Behav 2001; 40: 32-42.
65. Trainor BC, Marler CA. Testosterone promotes paternal behaviour in a monogamous via conversion to oestrogen. Proc Biol Sci 2002; 269: 823-829.
66. Kirkpatrick B, Kim JW, Insel TR. Limbic system fos expression associated with paternal behavior. Brain Res 1994; 658: 112-118.
67. Lee AW, Brown RE. Medial preoptic lesions disrupt parental behavior in both male and female California mice (Peromyscus californicus). Behav Neurosci 2002; 116: 968-975.
68. Schneider JS, Stone MK, Wynne-Edwards KE, Horton TH, Lydon J, O'Malley B, Levine JE. Progesterone receptors mediate male aggression toward infants. Proc Natl Acad Sci USA 2003; 100: 2951-2956.
69. Schneider JS, Burgess C, Horton TH, Levine JE. Effects of progesterone on male-mediated infant-directed aggression. Behav Brain Res 2009; 199: 340-344.
70. Harris BN, Perea-Rodriguez JP, Saltzman W. Acute effects of corticosterone injection on paternal behavior in California mouse (Peromyscus californicus) fathers. Horm Behav 2011; 60: 666-675.
71. Santema P, Teitel Z, Manser M, Bennett N, Clutton-Brock T. Effects of cortisol administration on cooperative behavior in meerkat helpers. Behav Ecol 2013; 24: 1122-1127.
72. Harris BN, de Jong TR, Yang V, Saltzman W. Chronic variable stress in fathers alters paternal and social behavior but not pup development in the biparental California mouse (Peromyscus californicus). Horm Behav 2013; 64: 799-811.
73. Bester-Meredith JK, Young LJ, Marler CA. Species differences in paternal behavior and aggression in Peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm Behav 1999; 36: 25-38.
74. Insel TR, Gelhard R, Shapiro LE. The comparative distribution of forebrain receptors for neurohypophyseal peptides in mongamous and polygamous mice. Neuroscience 1991; 43: 623-630.
75. Wang Z, Ferris CF, De Vries GJ. Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). Proc Natl Acad Sci USA 1994; 91: 400-404.
76. Parker KJ, Lee TM. Central vasopressin administration regulates the onset of facultative paternal behavior in Microtus pennsylvanicus (meadow voles). Horm Behav 2001; 39: 285-294.
77. Naber F, van Ijzendoorn MH, Deschamps P, van Engeland H, Bakermans-Kranenburg MJ. Intranasal oxytocin increases fathers' observed responsiveness during play with their children: a double-blind within-subject experiment. Psychoneuroendocrinology 2010; 35: 1583-1586.
78. 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.
79. Weisman O, Zagoory-Sharon O, Feldman R. Oxytocin administration, salivary testosterone, and father-infant social behavior. Prog Neuropsychopharmacol Biol Psychiatry 2014; 49: 47-52.
80. Bales KL, Kim AJ, Lewis-Reese AD, Carter CS. Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles. Horm Behav 2004; 45: 354-361.
81. Madden JR, Clutton-Brock TH. Experimental peripheral administration of oxytocin elevates a suite of cooperative behaviours in a wild social mammal. Proc Biol Sci 2011; 278: 1189-1194.
82. Boland MP, Lonergan P, O'Callaghan D. Effect of nutrition on endocrine parameters, ovarian physiology, and oocyte and embryo development. Theriogenology 2001; 55: 1323-1340.
83. Speakman JR. The physiological costs of reproduction in small mammals. Philos Trans R Soc Lond B Biol Sci 2008; 363: 375-398.
84. Tardif SD, Ziegler TE, Power M, Layne DG. Endocrine changes in full-term pregnancies and pregnancy loss due to energy restriction in the common marmoset (Callithrix jacchus). J Clin Endocrinol Metab 2005; 90: 335-339.
85. Augustine RA, Ladyman SR, Grattan DR. From feeding one to feeding many: hormone-induced changes in bodyweight homeostasis during pregnancy. J Physiol 2008; 586: 387-397.
86. Wade GN, Gray JM. Gonadal effects on food intake and adiposity: a metabolic hypothesis. Physiol Behav 1979; 22: 583-593.
87. Asarian L, Geary N. Cyclic estradiol treatment normalizes body weight and restores physiological patterns of spontaneous feeding and sexual receptivity in ovariectomized rats. Horm Behav 2002; 42: 461-471.
88. Grueso E, Rocha M, Puerta M. Plasma and cerebrospinal fluid leptin levels are maintained despite enhanced food intake in progesterone-treated rats. Eur J Endocrinol 2001; 144: 659-665.
89. Abizaid A, Schiavo L, Diano S. Hypothalamic and pituitary expression of ghrelin receptor message is increased during lactation. Neurosci Lett 2008; 440: 206-210.
90. Kunz TH, Hosken DJ. Male lactation: why, why not and is it care? Trends Ecol Evol 2008; 24: 80-85.
91. Ziegler TE, Prudom SL, Schultz-Darken NJ, Kurian AV, Snowdon CT. Pregnancy weight gain: marmoset and tamarin dads show it too. Biol Lett 2006; 2: 181-183.
92. Sánchez Rodríguez SM, Peláez del Hierro F, Fidalgo de las Heras AM, Morcilla Pimento A, Caperos Montalbán JM. Body weight increase in expectant males and helpers of cotton-top tamarins (Saguinus oedipus): a symptom of the couvade syndrome? Psicotherma 2008; 20: 825-829.
93. Achenbach GG, Snowdon CT. Costs of caregiving: weight loss in captive adult male cotton-top tamarins (Saguinus oedipus) following the birth of infants. Int J Primatol 2002 2002; 23: 179-189.
94. Glasper ER, Kozorovitskiy Y, Pavlic A, Gould E. Paternal experience suppresses adult neurogenesis without altering hippocampal function in Peromyscus californicus. J Comp Neurol 2011; 519: 2271-2281.
95. Franssen CL, Bardi M, Shea EA, Hampton JE, Franssen RA, Kinsley CH, Lambert KG. Fatherhood alters behavioural and neural responsiveness in a spatial task. J Neuroendocrinol 2011; 23: 1177-1187.
96. Lieberwirth C, Wang Y, Jia X, Liu Y, Wang Z. Fatherhood reduces the survival of adult-generated cells and affects various types of behavior in the prairie vole (Microtus ochrogaster). Behav Neurosci 2013; 38: 3345-3355.
97. Ruscio MG, Sweeny TD, Hazelton JL, Suppatkul P, Boothe E, Carter CS. Pup exposure elicits hippocampal cell proliferation in the prairie vole. Behav Brain Res 2008; 187: 9-16.
98. Mak GK, Weiss S. Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat Neurosci 2010; 13: 753-758.
99. Lightman SL, Windle RJ, Wood SA, Kershaw YM, Shanks N, Ingram CD. Peripartum plasticity within the hypothalamo-pituitary-adrenal axis. Prog Brain Res 2001; 133: 111-129.
100. Slattery DA, Neumann ID. No stress please! Mechanisms of stress hyporesponsiveness of the maternal brain. J Physiol 2008; 586: 377-385.
101. Lonstein JS. Regulation of anxiety during the postpartum period. Front Neuroendocrinol 2007; 28: 115-141.
102. Carter CS, Altemus M, Chrousos GP. Neuroendocrine and emotional changes in the post-partum period. Prog Brain Res 2001; 133: 241-249.
103. Woller MJ, Sosa ME, Chiang Y, Prudom SL, Keelty P, Moore JE, Ziegler TE. Differential hypothalamic secretion of neurocrines in male common marmosets: parental experience effects? J Neuroendocrinol 2011; 24: 413-421.
104. Chauke M, de Jong TR, Garland T Jr, Saltzman W. Paternal responsiveness is associated with, but not mediated by reduced neophobia in male California mice (Peromyscus californicus). Physiol Behav 2012; 107: 65-75.
105. Bardi M, Franssen CL, Hampton JE, Shea EA, Fanean AP, Lambert KG. Paternal experience and stress responses in California mice (Peromyscus californicus). Comp Med 2011; 61: 20-30.
106. Schradin C. Comments to K.E. Wynne-Edwards and M.E. Timonin, 2007. Paternal care in rodents: weakening support of hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care. Horm Behav 52: 114-121. Horm Behav 2007; 52: 557-559.