1932

Abstract

Parental care is found in species across the animal kingdom, from small insects to large mammals, with a conserved purpose of increasing offspring survival. Yet enormous variability exists between different species and between the sexes in the pattern and level of parental investment. Here, we review the literature on the neurobiological mechanisms underlying maternal and paternal care, especially in rodents, and discuss the relationship between sex differences in behavior and sexual dimorphism in the brain. We argue that although several brain regions and circuits regulating parental care are shared by both sexes, some of the fundamental components comprising the maternal brain are innate and sex specific. Moreover, we suggest that a more comprehensive understanding of the underlying mechanisms can be achieved by expanding the methodological toolbox, applying ethologically relevant approaches such as nontraditional wild-derived animal models and complex seminatural experimental set-ups.

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2017-07-25
2024-03-28
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Literature Cited

  1. Agrati D, Zuluaga MJ, Fernández-Guasti A, Meikle A, Ferreira A. 2008. Maternal condition reduces fear behaviors but not the endocrine response to an emotional threat in virgin female rats. Horm. Behav. 53:232–40 [Google Scholar]
  2. Alenina N, Kikic D, Todiras M, Mosienko V, Qadri F. et al. 2009. Growth retardation and altered autonomic control in mice lacking brain serotonin. PNAS 106:10332–37 [Google Scholar]
  3. Alligood CA, Wheaton CJ, Forde HM, Smith KN, Daneault AJ. et al. 2008. Pup development and maternal behavior in captive Key Largo woodrats (Neotoma floridana smalli). Zoo Biol 27:394–405 [Google Scholar]
  4. Almond REA, Brown GR, Keverne EB. 2006. Suppression of prolactin does not reduce infant care by parentally experienced male common marmosets (Callithrix jacchus). Horm. Behav. 49:673–80 [Google Scholar]
  5. Arrati PG, Carmona C, Dominguez G, Beyer C, Rosenblatt JS. 2006. GABA receptor agonists in the medial preoptic area and maternal behavior in lactating rats. Physiol. Behav. 87:51–65 [Google Scholar]
  6. Arriaga-Avila V, Martínez-Abundis E, Cárdenas-Morales B, Mercado-Gómez O, Aburto-Arciniega E. et al. 2014. Lactation reduces stress-caused dopaminergic activity and enhances GABAergic activity in the rat medial prefrontal cortex. J. Mol. Neurosci. 52:515–24 [Google Scholar]
  7. Auclair Y, König B, Ferrari M, Perony N, Lindholm AK. 2014. Nest attendance of lactating females in a wild house mouse population: benefits associated with communal nesting. Anim. Behav. 92:143–49 [Google Scholar]
  8. Bales KL, Kim AJ, Lewis-Reese AD, Carter CS. 2004. Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles. Horm. Behav. 45:354–61 [Google Scholar]
  9. Bales KL, Kramer KM, Lewis-Reese AD, Carter CS. 2006. Effects of stress on parental care are sexually dimorphic in prairie voles. Physiol. Behav. 87:424–29 [Google Scholar]
  10. Bales KL, Saltzman W. 2016. Fathering in rodents: neurobiological substrates and consequences for offspring. Horm. Behav. 77:249–59 [Google Scholar]
  11. Bales KL, van Westerhuyzen JA, Lewis-Reese AD, Grotte ND, Lanter JA, Carter CS. 2007. Oxytocin has dose-dependent developmental effects on pair-bonding and alloparental care in female prairie voles. Horm. Behav. 52:274–79 [Google Scholar]
  12. Bamshad M, Novak MA, de Vries GJ. 1993. Sex and species differences in the vasopressin innervation of sexually naive and parental prairie voles, Microtus ochrogaster and meadow voles, Microtus pennsylvanicus. J. Neuroendocrinol. 5:247–55 [Google Scholar]
  13. Bamshad M, Novak MA, de Vries GJ. 1994. Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster). Physiol. Behav. 56:751–58 [Google Scholar]
  14. Barofsky A-L, Taylor J, Tizabi Y, Kumar R, Jones-Quartey K. 1983. Specific neurotoxin lesions of median raphe serotonergic neurons disrupt maternal behavior in the lactating rat. Endocrinology 113:1884–93 [Google Scholar]
  15. Barreto FS, Avise JC. 2008. Polygynandry and sexual size dimorphism in the sea spider Ammothea hilgendorfi (Pycnogonida: Ammotheidae), a marine arthropod with brood-carrying males. Mol. Ecol. 17:4164–75 [Google Scholar]
  16. Beach FA, Jaynes J. 1956. Studies of maternal retrieving in rats. III. Sensory cues involved in the lactating female's response to her young. Behaviour 10:104–24 [Google Scholar]
  17. Bedford NL, Hoekstra HE. 2015. Peromyscus mice as a model for studying natural variation. eLife 4:e06813 [Google Scholar]
  18. Beery AK, Zucker I. 2011. Sex bias in neuroscience and biomedical research. Neurosci. Biobehav. Rev. 35:565–72 [Google Scholar]
  19. Beny Y, Kimchi T. 2014. Innate and learned aspects of pheromone-mediated social behaviours. Anim. Behav. 97:301–11 [Google Scholar]
  20. Beny Y, Kimchi T. 2016. Conditioned odor aversion induces social anxiety towards females in wild-type and TrpC2 knockout male mice. Genes Brain Behav 15:722–32 [Google Scholar]
  21. Blanchard DC, Spencer RL, Weiss SM, Blanchard RJ, McEwen B, Sakai RR. 1995. Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology 20:117–34 [Google Scholar]
  22. Blanchard RJ, Hebert MA, Ferrari P, Palanza P, Figueira R. et al. 1998. Defensive behaviors in wild and laboratory (Swiss) mice: the mouse defense test battery. Physiol. Behav. 65:201–9 [Google Scholar]
  23. Bleier R, Byne W, Siggelkow I. 1982. Cytoarchitectonic sexual dimorphisms of the medial preoptic and anterior hypothalamic areas in guinea pig, rat, hamster, and mouse. J. Comp. Neurol. 212:118–30 [Google Scholar]
  24. Bosch OJ, Neumann ID. 2008. Brain vasopressin is an important regulator of maternal behavior independent of dams' trait anxiety. PNAS 105:17139–44 [Google Scholar]
  25. Bosch OJ, Neumann ID. 2010. Vasopressin released within the central amygdala promotes maternal aggression. Eur. J. Neurosci. 31:883–91 [Google Scholar]
  26. Bosch OJ, Pförtsch J, Beiderbeck DI, Landgraf R, Neumann ID. 2010. Maternal behaviour is associated with vasopressin release in the medial preoptic area and bed nucleus of the stria terminalis in the rat. J. Neuroendocrinol. 22:420–29 [Google Scholar]
  27. Brenowitz EA, Zakon HH. 2015. Emerging from the bottleneck: benefits of the comparative approach to modern neuroscience. Trends Neurosci 38:273–78 [Google Scholar]
  28. Bridges RS. 1977. Parturition: its role in the long term retention of maternal behavior in the rat. Physiol. Behav. 18:487–90 [Google Scholar]
  29. Bridges RS. 2015. Neuroendocrine regulation of maternal behavior. Front. Neuroendocrinol. 36:178–96 [Google Scholar]
  30. Bridges RS. 2016. Long-term alterations in neural and endocrine processes induced by motherhood in mammals. Horm. Behav. 77:193–203 [Google Scholar]
  31. Bridges RS, Clifton DK, Sawyer CH. 1982. Postpartum luteinizing hormone release and maternal behavior in the rat after late-gestational depletion of hypothalamic norepinephrine. Neuroendocrinology 34:286–91 [Google Scholar]
  32. Bridges RS, DiBiase R, Loundes DD, Doherty PC. 1985. Prolactin stimulation of maternal behavior in female rats. Science 227:782–84 [Google Scholar]
  33. Bridges RS, Numan M, Ronsheim PM, Mann PE, Lupini CE. 1990. Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats. PNAS 87:8003–7 [Google Scholar]
  34. Bridges RS, Rigero BA, Byrnes EM, Yang L, Walker AM. 2001. Central infusions of the recombinant human prolactin receptor antagonist, S179D-PRL, delay the onset of maternal behavior in steroid-primed, nulliparous female rats. Endocrinology 142:730–39 [Google Scholar]
  35. Bridges RS, Rosenblatt JS, Feder HH. 1978. Serum progesterone concentrations and maternal behavior in rats after pregnancy termination: behavioral stimulation after progesterone withdrawal and inhibition by progesterone maintenance. Endocrinology 102:258–67 [Google Scholar]
  36. Bridges RS, Zarrow MX, Gandelman R, Denenberg VH. 1972. Differences in maternal responsiveness between lactating and sensitized rats. Dev. Psychobiol. 5:123–27 [Google Scholar]
  37. Brooks PL, Vella ET, Wynne-Edwards KE. 2005. Dopamine agonist treatment before and after the birth reduces prolactin concentration but does not impair paternal responsiveness in Djungarian hamsters, Phodopus campbelli. Horm. Behav. 47:358–66 [Google Scholar]
  38. Brown RE. 1986. Social and hormonal factors influencing infanticide and its suppression in adult male Long-Evans rats (Rattus norvegicus). J. Comp. Psychol. 100:155–61 [Google Scholar]
  39. Brus M, Meurisse M, Franceschini I, Keller M, Lévy F. 2010. Evidence for cell proliferation in the sheep brain and its down-regulation by parturition and interactions with the young. Horm. Behav. 58:737–46 [Google Scholar]
  40. Brussaard AB, Devay P, Leyting-Vermeulen JL, Kits KS. 1999. Changes in properties and neurosteroid regulation of GABAergic synapses in the supraoptic nucleus during the mammalian female reproductive cycle. J. Physiol. 516:513–24 [Google Scholar]
  41. Byrnes EM, Rigero BA, Bridges RS. 2002. Dopamine antagonists during parturition disrupt maternal care and the retention of maternal behavior in rats. Pharmacol. Biochem. Behav. 73:869–75 [Google Scholar]
  42. Byrnes JJ, Gleason ED, Schoen MT, Lovelock DF, Carini LM. et al. 2011. Accelerated maternal responding following intra-VTA pertussis toxin treatment. Behav. Brain Res. 223:322–28 [Google Scholar]
  43. Campbell JC, Laugero KD, Van Westerhuyzen JA, Hostetler CM, Cohen JD, Bales KL. 2009. Costs of pair-bonding and paternal care in male prairie voles (Microtus ochrogaster). Physiol. Behav. 98:367–73 [Google Scholar]
  44. Canavan S, Mayes L, Treloar H. 2011. Changes in maternal gene expression in olfactory circuits in the immediate postpartum period. Front. Psychiatry 2:40 [Google Scholar]
  45. Chalfin L, Dayan M, Levy DR, Austad SN, Miller RA. et al. 2014. Mapping ecologically relevant social behaviours by gene knockout in wild mice. Nat. Commun. 5:4569 [Google Scholar]
  46. Champagne FA, Curley JP. 2016. Plasticity of the maternal brain across the lifespan. New Dir. Child Adolesc. Dev. 2016:9–21 [Google Scholar]
  47. Cohen L, Mizrahi A. 2015. Plasticity during motherhood: changes in excitatory and inhibitory layer 2/3 neurons in auditory cortex. J. Neurosci. 35:1806–15 [Google Scholar]
  48. Collado P, Guillamón A, Valencia A, Segovia S. 1990. Sexual dimorphism in the bed nucleus of the accessory olfactory tract in the rat. Dev. Brain Res. 56:263–68 [Google Scholar]
  49. Conrath CL, Conners ME. 2014. Aspects of the reproductive biology of the North Pacific giant octopus (Enteroctopus dofleini) in the Gulf of Alaska. Fishery Bull 112:253–60 [Google Scholar]
  50. Crawley JN. 2007. What's Wrong with My Mouse: Behavioral Phenotyping of Transgenic and Knockout Mice Hoboken, NJ: John Wiley & Sons
  51. Crenshaw BJ, de Vries GJ, Yahr P. 1992. Vasopressin innervation of sexually dimorphic structures of the gerbil forebrain under various hormonal conditions. J. Comp. Neurol. 322:589–98 [Google Scholar]
  52. Crowley WR. 2011. Neuroendocrine regulation of lactation and milk production. Compr. Physiol. 5:255–91 [Google Scholar]
  53. Cushing BS, Perry A, Musatov S, Ogawa S, Papademetriou E. 2008. Estrogen receptors in the medial amygdala inhibit the expression of male prosocial behavior. J. Neurosci. 28:10399–403 [Google Scholar]
  54. D'Anna KL, Gammie SC. 2009. Activation of corticotropin-releasing factor receptor 2 in lateral septum negatively regulates maternal defense. Behav. Neurosci. 123:356–68 [Google Scholar]
  55. D'Anna KL, Stevenson SA, Gammie SC. 2005. Urocortin 1 and 3 impair maternal defense behavior in mice. Behav. Neurosci. 119:1061–71 [Google Scholar]
  56. Darnaudéry M, Perez-Martin M, Del Favero F, Gomez-Roldan C, Garcia-Segura LM, Maccari S. 2007. Early motherhood in rats is associated with a modification of hippocampal function. Psychoneuroendocrinology 32:803–12 [Google Scholar]
  57. de Jong TR, Chauke M, Harris BN, Saltzman W. 2009. From here to paternity: neural correlates of the onset of paternal behavior in California mice (Peromyscus californicus). Horm. Behav. 56:220–31 [Google Scholar]
  58. de Jong TR, Measor KR, Chauke M, Harris BN, Saltzman W. 2010. Brief pup exposure induces Fos expression in the lateral habenula and serotonergic caudal dorsal raphe nucleus of paternally experienced male California mice (Peromyscus californicus). Neuroscience 169:1094–104 [Google Scholar]
  59. de Moura AC, Lazzari VM, Becker RO, Gil MS, Ruthschilling CA. et al. 2015. Gene expression in the CNS of lactating rats with different patterns of maternal behavior. Neurosci. Res. 99:8–15 [Google Scholar]
  60. de Vries GJ, Boyle PA. 1998. Double duty for sex differences in the brain. Behav. Brain Res. 92:205–13 [Google Scholar]
  61. de Vries GJ, Buds RM, Swaab DF. 1981. Ontogeny of the vasopressinergic neurons of the suprachiasmatic nucleus and their extrahypothalamic projections in the rat brain—presence of a sex difference in the lateral septum. Brain Res 218:67–78 [Google Scholar]
  62. de Vries GJ, Miller MA. 1999. Anatomy and function of extrahypothalamic vasopressin systems in the brain. Progress in Brain Research 119 Advances in Brain Vasopressin IJA Urban, JPH Burbach, D de Wied 3–20 Amsterdam: Elsevier [Google Scholar]
  63. de Vries GJ, Rissman EF, Simerly RB, Yang L-Y, Scordalakes EM. et al. 2002. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J. Neurosci. 22:9005–14 [Google Scholar]
  64. de Vries GJ, Södersten P. 2009. Sex differences in the brain: the relation between structure and function. Horm. Behav. 55:589–96 [Google Scholar]
  65. de Vries GJ, Villalba C. 1997. Brain sexual dimorphism and sex differences in parental and other social behaviors. Ann. N. Y. Acad. Sci. 807:273–86 [Google Scholar]
  66. del Abril A, Segovia S, Guillamón A. 1987. The bed nucleus of the stria terminalis in the rat: regional sex differences controlled by gonadal steroids early after birth. Dev. Brain Res. 32:295–300 [Google Scholar]
  67. Del Cerro MCR, Izquierdo MAP, Collado P, Segovia S, Guillamón A. 1991. Bilateral lesions of the bed nucleus of the accessory olfactory tract facilitate maternal behavior in virgin female rats. Physiol. Behav. 50:67–71 [Google Scholar]
  68. Dewing P, Shi T, Horvath S, Vilain E. 2003. Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Mol. Brain Res. 118:82–90 [Google Scholar]
  69. Dewsbury DA. 1985. Paternal behavior in rodents. Am. Zoologist 25:841–52 [Google Scholar]
  70. Dixson AF, Fleming D. 1981. Parental behaviour and infant development in owl monkeys (Aotus trivirgatus griseimembra). J. Zool. 194:25–39 [Google Scholar]
  71. Driessen TM, Eisinger BE, Zhao C, Stevenson SA, Saul MC, Gammie SC. 2014. Genes showing altered expression in the medial preoptic area in the highly social maternal phenotype are related to autism and other disorders with social deficits. BMC Neurosci 15:11 [Google Scholar]
  72. Dugué R, Baras E, Gueye M, Avarre J-C, Combes Y. et al. 2014. Egg production in the euryhaline tilapia, Sarotherodon melanotheron heudelotii, experimentally maintained in fresh, sea and hypersaline waters. Aquat. Living Resour. 27:63–72 [Google Scholar]
  73. Dulac C, O'Connell LA, Wu Z. 2014. Neural control of maternal and paternal behaviors. Science 345:765–70 [Google Scholar]
  74. El Majdoubi M, Poulain DA, Theodosis DT. 1997. Lactation-induced plasticity in the supraoptic nucleus augments axodendritic and axosomatic GABAergic and glutamatergic synapses: an ultrastructural analysis using the disector method. Neuroscience 80:1137–47 [Google Scholar]
  75. Elwood RW. 1977. Changes in the responses of male and female gerbils (Meriones unguiculatus) towards test pups during the pregnancy of the female. Anim. Behav. 25:Pt. 146–51 [Google Scholar]
  76. Elwood RW. 1985. Inhibition of infanticide and onset of paternal care in male mice (Mus musculus). J. Comp. Psychol. 99:457–67 [Google Scholar]
  77. Fahrbach SE, Morrell JI, Pfaff DW. 1984. Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats. Horm. Behav. 18:267–86 [Google Scholar]
  78. Fahrbach SE, Morrell JI, Pfaff DW. 1985. Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 40:526–32 [Google Scholar]
  79. Fahrbach SE, Pfaff DW. 1986. Effect of preoptic region implants of dilute estradiol on the maternal behavior of ovariectomized, nulliparous rats. Horm. Behav. 20:354–63 [Google Scholar]
  80. Febo M. 2011. A bold view of the lactating brain: functional magnetic resonance imaging studies of suckling in awake dams. J. Neuroendocrinol. 23:1009–19 [Google Scholar]
  81. Febo M, Felix-Ortiz AC, Johnson TR. 2010. Inactivation or inhibition of neuronal activity in the medial prefrontal cortex largely reduces pup retrieval and grouping in maternal rats. Brain Res 1325:77–88 [Google Scholar]
  82. Feldman R. 2016. The neurobiology of mammalian parenting and the biosocial context of human caregiving. Horm. Behav. 77:3–17 [Google Scholar]
  83. Feldt-Rasmussen U, Mathiesen ER. 2011. Endocrine disorders in pregnancy: physiological and hormonal aspects of pregnancy. Best Pract. Res. Clin. Endocrinol. Metab. 25:875–84 [Google Scholar]
  84. Ferguson MW. 1985. Reproductive biology and embryology of the crocodilians. Biol. Reptil. 14:329–491 [Google Scholar]
  85. Ferreira A, Pereira M, Agrati D, Uriarte N, Fernández-Guasti A. 2002. Role of maternal behavior on aggression, fear and anxiety. Physiol. Behav. 77:197–204 [Google Scholar]
  86. Ferris CF, Kulkarni P, Sullivan JM, Harder JA, Messenger TL, Febo M. 2005. Pup suckling is more rewarding than cocaine: evidence from functional magnetic resonance imaging and three-dimensional computational analysis. J. Neurosci. 25:149–56 [Google Scholar]
  87. Fleming AS, Korsmit M, Deller M. 1994. Rat pups are potent reinforcers to the maternal animal: effects of experience, parity, hormones, and dopamine function. Psychobiology 22:44–53 [Google Scholar]
  88. Fleming AS, Vaccarino F, Tambosso L, Chee P. 1979. Vomeronasal and olfactory system modulation of maternal behavior in the rat. Science 203:372–74 [Google Scholar]
  89. Fone KCF, Porkess MV. 2008. Behavioural and neurochemical effects of post-weaning social isolation in rodents—relevance to developmental neuropsychiatric disorders. Neurosci. Biobehav. Rev. 32:1087–102 [Google Scholar]
  90. Fonio E, Golani I, Benjamini Y. 2012. Measuring behavior of animal models: faults and remedies. Nat. Methods 9:1167 [Google Scholar]
  91. Forger NG, Rosen GJ, Waters EM, Jacob D, Simerly RB, de Vries GJ. 2004. Deletion of Bax eliminates sex differences in the mouse forebrain. PNAS 101:13666–71 [Google Scholar]
  92. Förster S, Cords M. 2005. Socialization of infant blue monkeys (Cercopithecus mitis stuhlmanni): allomaternal interactions and sex differences. Behaviour 142:869–96 [Google Scholar]
  93. Fragaszy DM, Schwarz S, Shimosaka D. 1982. Longitudinal observations of care and development of infant titi monkeys (Callicebus moloch). Am. J. Primatol. 2:191–200 [Google Scholar]
  94. Francis CM, Anthony ELP, Brunton JA, Kunz TH. 1994. Lactation in male fruit bats. Nature 367:691–92 [Google Scholar]
  95. Gammie SC, Driessen TM, Zhao C, Saul MC, Eisinger BE. 2016. Genetic and neuroendocrine regulation of the postpartum brain. Front. Neuroendocrinol. 42:1–17 [Google Scholar]
  96. Gammie SC, Hasen NS, Awad TA, Auger AP, Jessen HM. et al. 2005. Gene array profiling of large hypothalamic CNS regions in lactating and randomly cycling virgin mice. Mol. Brain Res. 139:201–11 [Google Scholar]
  97. Gammie SC, Negron A, Newman SM, Rhodes JS. 2004. Corticotropin-releasing factor inhibits maternal aggression in mice. Behav. Neurosci. 118:805–14 [Google Scholar]
  98. Gettler LT, McDade TW, Feranil AB, Kuzawa CW. 2011. Longitudinal evidence that fatherhood decreases testosterone in human males. PNAS 108:16194–99 [Google Scholar]
  99. Giordano AL, Johnson AE, Rosenblatt JS. 1990. Haloperidol-induced disruption of retrieval behavior and reversal with apomorphine in lactating rats. Physiol. Behav. 48:211–14 [Google Scholar]
  100. Glasper ER, Kozorovitskiy Y, Pavlic A, Gould E. 2011. Paternal experience suppresses adult neurogenesis without altering hippocampal function in Peromyscus californicus. J. Comp. Neurol. 519:2271–81 [Google Scholar]
  101. Gleason ED, Marler CA. 2013. Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse. Proc. R. Soc. B 280:20130824 [Google Scholar]
  102. González-Mariscal G, Caba M, Martínez-Gómez M, Bautista A, Hudson R. 2016. Mothers and offspring: the rabbit as a model system in the study of mammalian maternal behavior and sibling interactions. Horm. Behav. 77:30–41 [Google Scholar]
  103. Gross AN, Richter SH, Engel AKJ, Würbel H. 2012. Cage-induced stereotypies, perseveration and the effects of environmental enrichment in laboratory mice. Behav. Brain Res. 234:61–68 [Google Scholar]
  104. Gross MR, Sargent RC. 1985. The evolution of male and female parental care in fishes. Am. Zoologist 25:807–22 [Google Scholar]
  105. Gubernick DJ, Sengelaub DR, Kurz EM. 1993. A neuroanatomical correlate of paternal and maternal behavior in the biparental California mouse (Peromyscus californicus). Behav. Neurosci. 107:194–201 [Google Scholar]
  106. Guénet J-L, Bonhomme F. 2003. Wild mice: an ever-increasing contribution to a popular mammalian model. Trends Genet 19:24–31 [Google Scholar]
  107. Hansen S, Harthon C, Wallin E, Löfberg L, Svensson K. 1991a. The effects of 6-OHDA-induced dopamine depletions in the ventral or dorsal striatum on maternal and sexual behavior in the female rat. Pharmacol. Biochem. Behav. 39:71–77 [Google Scholar]
  108. Hansen S, Harthon C, Wallin E, Löfberg L, Svensson K. 1991b. Mesotelencephalic dopamine system and reproductive behavior in the female rat: effects of ventral tegmental 6-hydroxydopamine lesions on maternal and sexual responsiveness. Behav. Neurosci. 105:588–98 [Google Scholar]
  109. Harper JM. 2008. Wild-derived mouse stocks: an underappreciated tool for aging research. Age 30:135–45 [Google Scholar]
  110. Harris BN, Saltzman W. 2013. Effect of reproductive status on hypothalamic–pituitary–adrenal (HPA) activity and reactivity in male California mice (Peromyscus californicus). Physiol. Behav. 112–113:70–76 [Google Scholar]
  111. Hasen NS, Gammie SC. 2009. Trpc2 gene impacts on maternal aggression, accessory olfactory bulb anatomy and brain activity. Genes Brain Behav 8:639–49 [Google Scholar]
  112. Hauser H, Gandelman R. 1985. Lever pressing for pups: evidence for hormonal influence upon maternal behavior of mice. Horm. Behav. 19:454–68 [Google Scholar]
  113. Hayes LD. 2000. To nest communally or not to nest communally: a review of rodent communal nesting and nursing. Anim. Behav. 59:677–88 [Google Scholar]
  114. Heidenreich M, Zhang F. 2016. Applications of CRISPR-Cas systems in neuroscience. Nat. Rev. Neurosci. 17:36–44 [Google Scholar]
  115. Hendriks AJ, Mulder C. 2008. Scaling of offspring number and mass to plant and animal size: model and meta-analysis. Oecologia 155:705–16 [Google Scholar]
  116. Hillerer KM, Neumann ID, Couillard-Despres S, Aigner L, Slattery DA. 2014. Lactation-induced reduction in hippocampal neurogenesis is reversed by repeated stress exposure. Hippocampus 24:673–83 [Google Scholar]
  117. Hines M, Allen LS, Gorski RA. 1992. Sex differences in subregions of the medial nucleus of the amygdala and the bed nucleus of the stria terminalis of the rat. Brain Res 579:321–26 [Google Scholar]
  118. Hoekzema E, Barba-Müller E, Pozzobon C, Picado M, Lucco F. et al. 2016. Pregnancy leads to long-lasting changes in human brain structure. Nat. Neurosci. 20:287–96 [Google Scholar]
  119. Hoffman GE, Le WW, Schulterbrandt T, Legan SJ. 2005. Estrogen and progesterone do not activate Fos in AVPV or LHRH neurons in male rats. Brain Res 1054:116–24 [Google Scholar]
  120. Huck UW, Soltis RL, Coopersmith CB. 1982. Infanticide in male laboratory mice: effects of social status, prior sexual experience, and basis for discrimination between related and unrelated young. Anim. Behav. 30:1158–65 [Google Scholar]
  121. Hurst JL, Payne CE, Nevison CM, Marie AD, Humphries RE. et al. 2001. Individual recognition in mice mediated by major urinary proteins. Nature 414:631–34 [Google Scholar]
  122. Hutton LA, Gu G, Simerly RB. 1998. Development of a sexually dimorphic projection from the bed nuclei of the stria terminalis to the anteroventral periventricular nucleus in the rat. J. Neurosci. 18:3003–13 [Google Scholar]
  123. Insel TR. 1990. Regional changes in brain oxytocin receptors post-partum: time-course and relationship to maternal behaviour. J. Neuroendocrinol. 2:539–45 [Google Scholar]
  124. Izquierdo MAP, Collado P, Segovia S, Guillamón A, Del Cerro MCR. 1992. Maternal behavior induced in male rats by bilateral lesions of the bed nucleus of the accessory olfactory tract. Physiol. Behav. 52:707–12 [Google Scholar]
  125. Jackson G, Mooers , Dubman E, Hutchen J, Collard M. 2014. Basal metabolic rate and maternal energetic investment durations in mammals. BMC Evol. Biol. 14:194 [Google Scholar]
  126. Jakubowski M, Terkel J. 1982. Infanticide and caretaking in non-lactating Mus musculus: influence of genotype, family group and sex. Anim. Behav. 30:1029–35 [Google Scholar]
  127. Jannett FJ. 1978. The density-dependent formation of extended maternal families of the montane vole, Microtus montanus nanus. Behav. Ecol. Sociobiol. 3:245–63 [Google Scholar]
  128. Jonas W, Woodside B. 2016. Physiological mechanisms, behavioral and psychological factors influencing the transfer of milk from mothers to their young. Horm. Behav. 77:167–81 [Google Scholar]
  129. Jones JS, Wynne-Edwards KE. 2000. Paternal hamsters mechanically assist the delivery, consume amniotic fluid and placenta, remove fetal membranes, and provide parental care during the birth process. Horm. Behav. 37:116–25 [Google Scholar]
  130. Kalinichev M, Rosenblatt JS, Nakabeppu Y, Morrell JI. 2000. Induction of c-Fos-like and FosB-like immunoreactivity reveals forebrain neuronal populations involved differentially in pup-mediated maternal behavior in juvenile and adult rats. J. Comp. Neurol. 416:45–78 [Google Scholar]
  131. Keer SE, Stern JM. 1999. Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats. Physiol. Behav. 67:659–69 [Google Scholar]
  132. Kenkel WM, Suboc G, Carter CS. 2014. Autonomic, behavioral and neuroendocrine correlates of paternal behavior in male prairie voles. Physiol. Behav. 128:252–59 [Google Scholar]
  133. Kentner AC, Abizaid A, Bielajew C. 2010. Modeling Dad: animal models of paternal behavior. Neurosci. Biobehav. Rev. 34:438–51 [Google Scholar]
  134. Keyser-Marcus L, Stafisso-Sandoz G, Gerecke K, Jasnow A, Nightingale L. et al. 2001. Alterations of medial preoptic area neurons following pregnancy and pregnancy-like steroidal treatment in the rat. Brain Res. Bull. 55:737–45 [Google Scholar]
  135. Kimchi T, Xu J, Dulac C. 2007. A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 448:1009–14 [Google Scholar]
  136. Kinsley CH, Trainer R, Stafisso-Sandoz G, Quadros P, Marcus LK. et al. 2006. Motherhood and the hormones of pregnancy modify concentrations of hippocampal neuronal dendritic spines. Horm. Behav. 49:131–42 [Google Scholar]
  137. Kirkpatrick B, Kim JW, Insel TR. 1994. Limbic system fos expression associated with paternal behavior. Brain Res 658:112–18 [Google Scholar]
  138. Kleiman DG, Malcolm JR. 1981. The evolution of male parental investment in mammals. Parental Care in Mammals DJ Gubernick, PH Klopfer 347–87 Boston: Springer [Google Scholar]
  139. Klopfer PH. 1971. Mother love: What turns it on? Studies of maternal arousal and attachment in ungulates may have implications for man. Am. Sci. 59:404–7 [Google Scholar]
  140. Klug BJ, Barclay RMR. 2013. Thermoregulation during reproduction in the solitary, foliage-roosting hoary bat (Lasiurus cinereus). J. Mammal. 94:477 [Google Scholar]
  141. Kohl J, Autry AE, Dulac C. 2016. The neurobiology of parenting: a neural circuit perspective. BioEssays 39:1600159 [Google Scholar]
  142. Kohl J, Ostrovsky AD, Frechter S, Jefferis GSXE. 2013. A bidirectional circuit switch reroutes pheromone signals in male and female brains. Cell 155:1610–23 [Google Scholar]
  143. Kokay IC, Bull PM, Davis RL, Ludwig M, Grattan DR. 2006. Expression of the long form of the prolactin receptor in magnocellular oxytocin neurons is associated with specific prolactin regulation of oxytocin neurons. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290:R1216–25 [Google Scholar]
  144. Kopel H, Schechtman E, Groysman M, Mizrahi A. 2012. Enhanced synaptic integration of adult-born neurons in the olfactory bulb of lactating mothers. J. Neurosci. 32:7519–27 [Google Scholar]
  145. Kunz TH, Hosken DJ. 2009. Male lactation: Why, why not and is it care. ? Trends Ecol. Evol. 24:80–85 [Google Scholar]
  146. Kuroda KO, Tachikawa K, Yoshida S, Tsuneoka Y, Numan M. 2011. Neuromolecular basis of parental behavior in laboratory mice and rats: with special emphasis on technical issues of using mouse genetics. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 35:1205–31 [Google Scholar]
  147. Labov JB. 1980. Factors influencing infanticidal behavior in wild male house mice (Mus musculus). Behav. Ecol. Sociobiol. 6:297–303 [Google Scholar]
  148. Lambert KG, Franssen CL, Bardi M, Hampton JE, Hainley L. et al. 2011. Characteristic neurobiological patterns differentiate paternal responsiveness in two Peromyscus species. Brain Behav. Evol. 77:159–75 [Google Scholar]
  149. Larsen CM, Grattan DR. 2010. 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 151:3805–14 [Google Scholar]
  150. Leblond CP, Nelson WO. 1937. Maternal behavior in hypophysectomized male and female mice. Am. J. Physiol. 120:167–72 [Google Scholar]
  151. Lee AW, Brown RE. 2007. Comparison of medial preoptic, amygdala, and nucleus accumbens lesions on parental behavior in California mice (Peromyscus californicus). Physiol. Behav. 92:617–28 [Google Scholar]
  152. Lee G, Gammie SC. 2009. GABAA receptor signaling in the lateral septum regulates maternal aggression in mice. Behav. Neurosci. 123:1169–77 [Google Scholar]
  153. Lee PC. 1987. Allomothering among African elephants. Anim. Behav. 35:278–91 [Google Scholar]
  154. Lerch-Haner JK, Frierson D, Crawford LK, Beck SG, Deneris ES. 2008. Serotonergic transcriptional programming determines maternal behavior and offspring survival. Nat. Neurosci. 11:1001–3 [Google Scholar]
  155. Leuner B, Glasper ER, Gould E. 2010. Parenting and plasticity. Trends Neurosci 33:465–73 [Google Scholar]
  156. Leuner B, Gould E. 2010. Dendritic growth in medial prefrontal cortex and cognitive flexibility are enhanced during the postpartum period. J. Neurosci. 30:13499–503 [Google Scholar]
  157. Leuner B, Sabihi S. 2016. The birth of new neurons in the maternal brain: hormonal regulation and functional implications. Front. Neuroendocrinol. 41:99–113 [Google Scholar]
  158. Lévy F, Gervais R, Kindermann U, Orgeur P, Piketty V. 1990. Importance of β-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. Behav. Neurosci. 104:464 [Google Scholar]
  159. Li K, Nakajima M, Ibañez-Tallon I, Heintz N. 2016. A cortical circuit for sexually dimorphic oxytocin-dependent anxiety behaviors. Cell 167:60–72.e11 [Google Scholar]
  160. Lieberwirth C, Wang Y, Jia X, Liu Y, Wang Z. 2013. Fatherhood reduces the survival of adult-generated cells and affects various types of behavior in the prairie vole (Microtus ochrogaster). Eur. J. Neurosci. 38:3345–55 [Google Scholar]
  161. Liker A, Freckleton RP, Remeš V, Székely T. 2015. Sex differences in parental care: gametic investment, sexual selection, and social environment. Evolution 69:2862–75 [Google Scholar]
  162. Lodé T. 2012. Oviparity or viviparity? That is the question…. Reprod. Biol. 12:259–64 [Google Scholar]
  163. Lonstein JS. 2002. Effects of dopamine receptor antagonism with haloperidol on nurturing behavior in the biparental prairie vole. Pharmacol. Biochem. Behav. 74:11–19 [Google Scholar]
  164. Lonstein JS, de Vries GJ. 2000. Sex differences in the parental behavior of rodents. Neurosci. Biobehav. Rev. 24:669–86 [Google Scholar]
  165. Lonstein JS, Pereira M, Morrell JI, Marler CA. 2015. Parenting behavior. Knobil and Neill's Physiology of Reproduction TM Plant, AJ Zeleznik 2371–437 London: Acad. Press [Google Scholar]
  166. Lonstein JS, Wagner CK, de Vries GJ. 1999. Comparison of the “nursing” and other parental behaviors of nulliparous and lactating female rats. Horm. Behav. 36:242–51 [Google Scholar]
  167. 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 139:4102–7 [Google Scholar]
  168. Lynn SE. 2016. Endocrine and neuroendocrine regulation of fathering behavior in birds. Horm. Behav. 77:237–48 [Google Scholar]
  169. Macbeth AH, Scharfman HE, MacLusky NJ, Gautreaux C, Luine VN. 2008. Effects of multiparity on recognition memory, monoaminergic neurotransmitters, and brain-derived neurotrophic factor (BDNF). Horm. Behav. 54:7–17 [Google Scholar]
  170. MacLusky N, Naftolin F. 1981. Sexual differentiation of the central nervous system. Science 211:1294–302 [Google Scholar]
  171. Mak GK, Weiss S. 2010. Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat. Neurosci. 13:753–58 [Google Scholar]
  172. Mann J, Smuts BB. 1998. Natal attraction: allomaternal care and mother–infant separations in wild bottlenose dolphins. Anim. Behav. 55:1097–113 [Google Scholar]
  173. Manning CJ, Dewsbury DA, Wakeland EK, Potts WK. 1995. Communal nesting and communal nursing in house mice. Mus musculus domesticus. Anim. Behav. 50:741–51 [Google Scholar]
  174. Marlin BJ, Mitre M, D'amour JA, Chao MV, Froemke RC. 2015. Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature 520:499–504 [Google Scholar]
  175. Martín-Sánchez A, Valera-Marín G, Hernández-Martínez A, Lanuza E, Martínez-García F, Agustín-Pavón C. 2015. Wired for motherhood: induction of maternal care but not maternal aggression in virgin female CD1 mice. Front. Behav. Neurosci. 9:197 [Google Scholar]
  176. Matsushita N, Muroi Y, Kinoshita K, Ishii T. 2015. Comparison of c-Fos expression in brain regions involved in maternal behavior of virgin and lactating female mice. Neurosci. Lett. 590:166–71 [Google Scholar]
  177. McCarthy MM. 1990. Oxytocin inhibits infanticide in female house mice (Mus domesticus). Horm. Behav. 24:365–75 [Google Scholar]
  178. McCarthy MM, Bare JE, Vom Saal FS. 1986. Infanticide and parental behavior in wild female house mice: effects of ovariectomy, adrenalectomy and administration of oxytocin and prostaglandin F2α. . Physiol. Behav. 36:17–23 [Google Scholar]
  179. McCarthy MM, Vom Saal FS. 1985. The influence of reproductive state on infanticide by wild female house mice (Mus musculus). Physiol. Behav. 35:843–49 [Google Scholar]
  180. Meehan AP. 1984. Rats and Mice: Their Biology and Control East Grinstead, UK: Rentokil Ltd.
  181. Mennella JA, Moltz H. 1988. Infanticide in the male rat: the role of the vomeronasal organ. Physiol. Behav. 42:303–6 [Google Scholar]
  182. Miller RA, Harper JM, Dysko RC, Durkee SJ, Austad SN. 2002. Longer life spans and delayed maturation in wild-derived mice. Exp. Biol. Med. 227:500–8 [Google Scholar]
  183. Miller SM, Lonstein JS. 2005. Dopamine D1 and D2 receptor antagonism in the preoptic area produces different effects on maternal behavior in lactating rats. Behav. Neurosci. 119:1072–83 [Google Scholar]
  184. Moe Y, Kyi-Tha-Thu C, Tanaka T, Ito H, Yahashi S. et al. 2016. A sexually dimorphic area of the dorsal hypothalamus in mice and common marmosets. Endocrinology 157:4817–28 [Google Scholar]
  185. Moffat SD, Suh EJ, Fleming AS. 1993. Noradrenergic involvement in the consolidation of maternal experience in postpartum rats. Physiol. Behav. 53:805–11 [Google Scholar]
  186. Moltz H, Lubin M, Leon M, Numan M. 1970. Hormonal induction of maternal behavior in the ovariectomized nulliparous rat. Physiol. Behav. 5:1373–77 [Google Scholar]
  187. Nakajima M, Görlich A, Heintz N. 2014. Oxytocin modulates female sociosexual behavior through a specific class of prefrontal cortical interneurons. Cell 159:295–305 [Google Scholar]
  188. Nephew BC, Bridges RS. 2008. Central actions of arginine vasopressin and a V1a receptor antagonist on maternal aggression, maternal behavior, and grooming in lactating rats. Pharmacol. Biochem. Behav. 91:77–83 [Google Scholar]
  189. Nishimori K, Young LJ, Guo Q, Wang Z, Insel TR, Matzuk MM. 1996. Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. PNAS 93:11699–704 [Google Scholar]
  190. Nottebohm F, Arnold A. 1976. Sexual dimorphism in vocal control areas of the songbird brain. Science 194:211–13 [Google Scholar]
  191. Nowak R, Keller M, Lévy F. 2011. Mother–young relationships in sheep: a model for a multidisciplinary approach of the study of attachment in mammals. J. Neuroendocrinol. 23:1042–53 [Google Scholar]
  192. Numan M, Insel TR. 2003. The Neurobiology of Parental Behavior New York: Springer
  193. Numan M, Numan MJ. 1994. Expression of Fos-like immunoreactivity in the preoptic area of maternally behaving virgin and postpartum rats. Behav. Neurosci. 108:379–94 [Google Scholar]
  194. Numan M, Numan MJ, English JB. 1993. Excitotoxic amino acid injections into the medial amygdala facilitate maternal behavior in virgin female rats. Horm. Behav. 27:56–81 [Google Scholar]
  195. Numan M, Numan MJ, Pliakou N, Stolzenberg DS, Mullins OJ. et al. 2005a. The effects of D1 or D2 dopamine receptor antagonism in the medial preoptic area, ventral pallidum, or nucleus accumbens on the maternal retrieval response and other aspects of maternal behavior in rats. Behav. Neurosci. 119:1588–604 [Google Scholar]
  196. Numan M, Numan MJ, Schwarz JM, Neuner CM, Flood TF, Smith CD. 2005b. Medial preoptic area interactions with the nucleus accumbens–ventral pallidum circuit and maternal behavior in rats. Behav. Brain Res. 158:53–68 [Google Scholar]
  197. Numan M, Rosenblatt JS, Komisaruk BR. 1977. Medial preoptic area and onset of maternal behavior in the rat. J. Comp. Physiol. Psychol. 91:146–64 [Google Scholar]
  198. Numan M, Young LJ. 2016. Neural mechanisms of mother–infant bonding and pair bonding: similarities, differences, and broader implications. Horm. Behav. 77:98–112 [Google Scholar]
  199. O'Connell LA, Matthews BJ, Hofmann HA. 2012. Isotocin regulates paternal care in a monogamous cichlid fish. Horm. Behav. 61:725–33 [Google Scholar]
  200. Ogawa S, Eng V, Taylor J, Lubahn DB, Korach KS, Pfaff DW. 1998. Roles of estrogen receptor-α gene expression in reproduction-related behaviors in female mice. Endocrinology 139:5070–81 [Google Scholar]
  201. Ohayon S, Avni O, Taylor AL, Perona P, Egnor SR. 2013. Automated multi-day tracking of marked mice for the analysis of social behaviour. J. Neurosci. Methods 219:10–19 [Google Scholar]
  202. Oren-Suissa M, Bayer EA, Hobert O. 2016. Sex-specific pruning of neuronal synapses in Caenorhabditis elegans. Nature 533:206–11 [Google Scholar]
  203. Ormandy CJ, Camus A, Barra J, Damotte D, Lucas B. et al. 1997. Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev 11:167–78 [Google Scholar]
  204. Parada M, King S, Li M, Fleming AS. 2008. The roles of accumbal dopamine D1 and D2 receptors in maternal memory in rats. Behav. Neurosci. 122:368–76 [Google Scholar]
  205. Parker KJ, Kinney LF, Phillips KM, Lee TM. 2001. Paternal behavior is associated with central neurohormone receptor binding patterns in meadow voles (Microtus pennsylvanicus). Behav. Neurosci. 115:1341–48 [Google Scholar]
  206. Parker KJ, Lee TM. 2001. Central vasopressin administration regulates the onset of facultative paternal behavior in Microtus pennsylvanicus (meadow voles). Horm. Behav. 39:285–94 [Google Scholar]
  207. Pawluski JL, Galea LAM. 2006. Hippocampal morphology is differentially affected by reproductive experience in the mother. J. Neurobiol. 66:71–81 [Google Scholar]
  208. Pawluski JL, Galea LAM. 2007. Reproductive experience alters hippocampal neurogenesis during the postpartum period in the dam. Neuroscience 149:53–67 [Google Scholar]
  209. Pedersen C, Ascher J, Monroe Y, Prange A. 1982. Oxytocin induces maternal behavior in virgin female rats. Science 216:648–50 [Google Scholar]
  210. Pedersen CA, Caldwell JD, Johnson MF, Fort SA, Prange AJ Jr.. 1985. Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior. Neuropeptides 6:175–82 [Google Scholar]
  211. Pedersen CA, Caldwell JD, Walker C, Ayers G, Mason GA. 1994. Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav. Neurosci. 108:1163–71 [Google Scholar]
  212. Pedersen CA, Prange AJ Jr.. 1979. Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. PNAS 76:6661–65 [Google Scholar]
  213. Perea-Rodriguez JP, Takahashi EY, Amador TM, Hao RC, Saltzman W, Trainor BC. 2015. Effects of reproductive experience on central expression of progesterone, oestrogen α, oxytocin and vasopressin receptor mRNA in male California mice (Peromyscus californicus). J. Neuroendocrinol. 27:245–52 [Google Scholar]
  214. Pereira M. 2016. Structural and functional plasticity in the maternal brain circuitry. New Dir. Child Adolesc. Dev. 2016:23–46 [Google Scholar]
  215. Perrigo G, Bryant WC, Vom Saal FS. 1989. Fetal, hormonal and experiential factors influencing the mating-induced regulation of infanticide in male house mice. Physiol. Behav. 46:121–28 [Google Scholar]
  216. Peters SM, Pothuizen HHJ, Spruijt BM. 2015. Ethological concepts enhance the translational value of animal models. Eur. J. Pharmacol. 759:42–50 [Google Scholar]
  217. Pi X, Grattan D. 1999. Increased expression of both short and long forms of prolactin receptor mRNA in hypothalamic nuclei of lactating rats. J. Mol. Endocrinol. 23:13–22 [Google Scholar]
  218. Polston EK, Gu G, Simerly RB. 2004. Neurons in the principal nucleus of the bed nuclei of the stria terminalis provide a sexually dimorphic GABAergic input to the anteroventral periventricular nucleus of the hypothalamus. Neuroscience 123:793–803 [Google Scholar]
  219. Price EO. 1999. Behavioral development in animals undergoing domestication. Appl. Anim. Behav. Sci. 65:245–71 [Google Scholar]
  220. Prum RO. 2008. Who's your daddy?. Science 322:1799–800 [Google Scholar]
  221. Ragnauth AK, Devidze N, Moy V, Finley K, Goodwillie A. et al. 2005. Female oxytocin gene-knockout mice, in a semi-natural environment, display exaggerated aggressive behavior. Genes Brain Behav 4:229–39 [Google Scholar]
  222. Rapaport LG. 2006. Provisioning in wild golden lion tamarins (Leontopithecus rosalia): benefits to omnivorous young. Behav. Ecol. 17:212–21 [Google Scholar]
  223. Rasia-Filho AA, Fabian C, Rigoti KM, Achaval M. 2004. Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method. Neuroscience 126:839–47 [Google Scholar]
  224. Ray S, Tzeng R-Y, DiCarlo LM, Bundy JL, Vied C. et al. 2016. An examination of dynamic gene expression changes in the mouse brain during pregnancy and the postpartum period. G3: Genes Genom. Genet. 6:221–33 [Google Scholar]
  225. Reburn CJ, Wynne-Edwards KE. 1999. Hormonal changes in males of a naturally biparental and a uniparental mammal. Horm. Behav. 35:163–76 [Google Scholar]
  226. Reynolds JD, Goodwin NB, Freckleton RP. 2002. Evolutionary transitions in parental care and live bearing in vertebrates. Philos. Trans. R. Soc. B 357:269–81 [Google Scholar]
  227. Ribeiro AC, Musatov S, Shteyler A, Simanduyev S, Arrieta-Cruz I. et al. 2012. siRNA silencing of estrogen receptor-α expression specifically in medial preoptic area neurons abolishes maternal care in female mice. PNAS 109:16324–29 [Google Scholar]
  228. Rich ME, deCárdenas EJ, Lee H-J, Caldwell HK. 2014. Impairments in the initiation of maternal behavior in oxytocin receptor knockout mice. PLOS ONE 9:e98839 [Google Scholar]
  229. Rilling JK, Young LJ. 2014. The biology of mammalian parenting and its effect on offspring social development. Science 345:771–76 [Google Scholar]
  230. Roland AB, O'Connell LA. 2015. Poison frogs as a model system for studying the neurobiology of parental care. Curr. Opin. Behav. Sci. 6:76–81 [Google Scholar]
  231. Rosenberg KM. 1974. Effects of pre- and postpubertal castration and testosterone on pup-killing behavior in the male rat. Physiol. Behav. 13:159–61 [Google Scholar]
  232. Rosenblatt JS. 1967. Nonhormonal basis of maternal behavior in the rat. Science 156:1512–13 [Google Scholar]
  233. Rosenblatt JS. 1969. The development of maternal responsiveness in the rat. Am. J. Orthopsychiatry 39:36–56 [Google Scholar]
  234. Rosenblatt JS, Ceus K. 1998. Estrogen implants in the medial preoptic area stimulate maternal behavior in male rats. Horm. Behav. 33:23–30 [Google Scholar]
  235. Rosenblatt JS, Hazelwood S, Poole J. 1996. Maternal behavior in male rats: effects of medial preoptic area lesions and presence of maternal aggression. Horm. Behav. 30:201–15 [Google Scholar]
  236. Royle NJ, Smiseth PT, Kölliker M. 2012. The Evolution of Parental Care Oxford, UK: Oxford Univ. Press
  237. Russell EM. 1982. Patterns of parental care and parental investment in marsupials. Biol. Rev. 57:423–86 [Google Scholar]
  238. Salais-López H, Lanuza E, Agustín-Pavón C, Martínez-García F. 2016. Tuning the brain for motherhood: prolactin-like central signalling in virgin, pregnant, and lactating female mice. Brain Struct. Funct. 222:895–921 [Google Scholar]
  239. Salmaso N, Quinlan MG, Brake WG, Woodside B. 2011. Changes in dendritic spine density on layer 2/3 pyramidal cells within the cingulate cortex of late pregnant and postpartum rats. Horm. Behav. 60:65–71 [Google Scholar]
  240. Salzberg HC, Lonstein JS, Stern JM. 2002. GABAA receptor regulation of kyphotic nursing and female sexual behavior in the caudal ventrolateral periaqueductal gray of postpartum rats. Neuroscience 114:675–87 [Google Scholar]
  241. Sammut M, Cook SJ, Nguyen KCQ, Felton T, Hall DH. et al. 2015. Glia-derived neurons are required for sex-specific learning in C. elegans. Nature 526:385–90 [Google Scholar]
  242. Samuels MH, Bridges RS. 1983. Plasma prolactin concentrations in parental male and female rats: effects of exposure to rat young. Endocrinology 113:1647–54 [Google Scholar]
  243. Schneider JS, Stone MK, Wynne-Edwards KE, Horton TH, Lydon J. et al. 2003. Progesterone receptors mediate male aggression toward infants. PNAS 100:2951–56 [Google Scholar]
  244. Schultz LA, Lore RK. 1993. Communal reproductive success in rats (Rattus norvegicus): effects of group composition and prior social experience. J. Comp. Psychol. 107:216–22 [Google Scholar]
  245. Scott N, Prigge M, Yizhar O, Kimchi T. 2015. A sexually dimorphic hypothalamic circuit controls maternal care and oxytocin secretion. Nature 525:519–22 [Google Scholar]
  246. Segovia S, Orensanz LM, Valencia A, Guillamón A. 1984. Effects of sex steroids on the development of the accessory olfactory bulb in the rat: a volumetric study. Dev. Brain Res. 16:312–14 [Google Scholar]
  247. Shams S, Pawluski JL, Chatterjee-Chakraborty M, Oatley H, Mastroianni A, Fleming AS. 2012. Dendritic morphology in the striatum and hypothalamus differentially exhibits experience-dependent changes in response to maternal care and early social isolation. Behav. Brain Res. 233:79–89 [Google Scholar]
  248. Sheehan T, Numan M. 2002. Estrogen, progesterone, and pregnancy termination alter neural activity in brain regions that control maternal behavior in rats. Neuroendocrinology 75:12–23 [Google Scholar]
  249. Shemesh Y, Sztainberg Y, Forkosh O, Shlapobersky T, Chen A, Schneidman E. 2013. High-order social interactions in groups of mice. eLife 2:e00759 [Google Scholar]
  250. Sherman PW, Lacey EA, Reeve HK, Keller L. 1995. Forum: the eusociality continuum. Behav. Ecol. 6:102–8 [Google Scholar]
  251. Shine R. 1988. Parental care in reptiles. Biol. Reptil. 16:275–330 [Google Scholar]
  252. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R. et al. 2003. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299:117–20 [Google Scholar]
  253. Siegel HI, Rosenblatt JS. 1975a. Estrogen-induced maternal behavior in hysterectomized-ovariectomized virgin rats. Physiol. Behav. 14:465–71 [Google Scholar]
  254. Siegel HI, Rosenblatt JS. 1975b. Hormonal basis of hysterectomy-induced maternal behavior during pregnancy in the rat. Horm. Behav. 6:211–22 [Google Scholar]
  255. Silva MRP, Bernardi MM, Cruz-Casallas PE, Felicio LF. 2003. Pimozide injections into the nucleus accumbens disrupt maternal behaviour in lactating rats. Pharmacol. Toxicol. 93:42–47 [Google Scholar]
  256. Silva MRP, Bernardi MM, Felicio LF. 2001. Effects of dopamine receptor antagonists on ongoing maternal behavior in rats. Pharmacol. Biochem. Behav. 68:461–68 [Google Scholar]
  257. Simerly RB. 2002. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci. 25:507–36 [Google Scholar]
  258. Simerly RB, Swanson LW, Gorski RA. 1985. The distribution of monoaminergic cells and fibers in a periventricular preoptic nucleus involved in the control of gonadotropin release: immunohistochemical evidence for a dopaminergic sexual dimorphism. Brain Res 330:55–64 [Google Scholar]
  259. Simerly RB, Zee MC, Pendleton JW, Lubahn DB, Korach KS. 1997. Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of themouse. PNAS 94:14077–82 [Google Scholar]
  260. Slattery DA, Hillerer KM. 2016. The maternal brain under stress: consequences for adaptive peripartum plasticity and its potential functional implications. Front. Neuroendocrinol. 41:114–28 [Google Scholar]
  261. Smith CD, Holschbach MA, Olsewicz J, Lonstein JS. 2012. 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 224:263–76 [Google Scholar]
  262. Song Z, Tai F, Yu C, Wu R, Zhang X. et al. 2010. Sexual or paternal experiences alter alloparental behavior and the central expression of ERα and OT in male mandarin voles (Microtus mandarinus). Behav. Brain Res. 214:290–300 [Google Scholar]
  263. Soroker V, Terkel J. 1988. Changes in incidence of infanticidal and parental responses during the reproductive cycle in male and female wild mice Mus musculus. Anim. Behav. 36:1275–81 [Google Scholar]
  264. Spruijt BM, Peters SM, de Heer RC, Pothuizen HHJ, van der Harst JE. 2014. Reproducibility and relevance of future behavioral sciences should benefit from a cross fertilization of past recommendations and today's technology: “Back to the future.”. J. Neurosci. Methods 234:2–12 [Google Scholar]
  265. Stockinger P, Kvitsiani D, Rotkopf S, Tirián L, Dickson BJ. 2005. Neural circuitry that governs Drosophila male courtship behavior. Cell 121:795–807 [Google Scholar]
  266. Stölting KN, Wilson AB. 2007. Male pregnancy in seahorses and pipefish: beyond the mammalian model. BioEssays 29:884–96 [Google Scholar]
  267. Stolzenberg DS, Champagne FA. 2016. Hormonal and non-hormonal bases of maternal behavior: the role of experience and epigenetic mechanisms. Horm. Behav. 77:204–10 [Google Scholar]
  268. Stolzenberg DS, McKenna JB, Keough S, Hancock R, Numan MJ, Numan M. 2007. Dopamine D1 receptor stimulation of the nucleus accumbens or the medial preoptic area promotes the onset of maternal behavior in pregnancy-terminated rats. Behav. Neurosci. 121:907–19 [Google Scholar]
  269. Stolzenberg DS, Rissman EF. 2011. Oestrogen-independent, experience-induced maternal behaviour in female mice. J. Neuroendocrinol. 23:345–54 [Google Scholar]
  270. Stowers L, Logan DW. 2010. Sexual dimorphism in olfactory signaling. Curr. Opin. Neurobiol. 20:770–75 [Google Scholar]
  271. Sussman RW. 1999. Primate Ecology and Social Structure 1 Lorises, Lemurs and Tarsiers Needham Heights, MA: Pearson Cust. Publ.
  272. Svare B, Mann M. 1981. Infanticide: genetic, developmental and hormonal influences in mice. Physiol. Behav. 27:921–27 [Google Scholar]
  273. Swaab D, Bao A-M. 2013. Sexual differentiation of the human brain in relation to gender-identity, sexual orientation, and neuropsychiatric disorders. Neuroscience in the 21st Century: From Basic to Clinical DW Pfaff 2973–98 New York: Springer [Google Scholar]
  274. Swaab D, Fliers E. 1985. A sexually dimorphic nucleus in the human brain. Science 228:1112–15 [Google Scholar]
  275. Swanson LJ, Campbell CS. 1979. Induction of maternal behavior in nulliparous golden hamsters (Mesocricetus auratus). Behav. Neural Biol. 26:364–71 [Google Scholar]
  276. Tachikawa KS, Yoshihara Y, Kuroda KO. 2013. Behavioral transition from attack to parenting in male mice: a crucial role of the vomeronasal system. J. Neurosci. 33:5120–26 [Google Scholar]
  277. Takahashi A, Nishi A, Ishii A, Shiroishi T, Koide T. 2008. Systematic analysis of emotionality in consomic mouse strains established from C57BL/6J and wild-derived MSM/Ms. Genes Brain Behav 7:849–58 [Google Scholar]
  278. Takayanagi Y, Yoshida M, Bielsky IF, Ross HE, Kawamata M. et al. 2005. Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. PNAS 102:16096–101 [Google Scholar]
  279. Tanaeva KK, Dobryakova YV, Dubynin VA. 2014. Maternal behavior: a novel experimental approach and detailed statistical analysis. J. Neurosci. Neuroeng. 3:52–61 [Google Scholar]
  280. Terkel J, Rosenblatt JS. 1968. Maternal behavior induced by maternal blood plasma injected into virgin rats. J. Comp. Physiol. Psychol. 65:479 [Google Scholar]
  281. Thomas SA, Palmiter RD. 1997. Impaired maternal behavior in mice lacking norepinephrine and epinephrine. Cell 91:583–92 [Google Scholar]
  282. Thonhauser KE, Raveh S, Penn DJ. 2014. Multiple paternity does not depend on male genetic diversity. Anim. Behav. 93:135–41 [Google Scholar]
  283. Thoß M, Enk V, Yu H, Miller I, Luzynski KC. et al. 2016. Diversity of major urinary proteins (MUPs) in wild house mice. Sci. Rep. 6:38378 [Google Scholar]
  284. Thoß M, Ilmonen P, Musolf K, Penn DJ. 2011. Major histocompatibility complex heterozygosity enhances reproductive success. Mol. Ecol. 20:1546–57 [Google Scholar]
  285. Tomizawa K, Iga N, Lu Y-F, Moriwaki A, Matsushita M. et al. 2003. Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade. Nat. Neurosci. 6:384–90 [Google Scholar]
  286. 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. 15:1381–89 [Google Scholar]
  287. Trainor BC, Bird IM, Alday NA, Schlinger BA, Marler CA. 2003. Variation in aromatase activity in the medial preoptic area and plasma progesterone is associated with the onset of paternal behavior. Neuroendocrinology 78:36–44 [Google Scholar]
  288. Trivers RL. 1972. Parental investment and sexual selection. Sexual Selection and the Descent of Man B Campbell 136–79 Chicago: Aldine Publ. [Google Scholar]
  289. Turner AK, Paterson S. 2013. Wild rodents as a model to discover genes and pathways underlying natural variation in infectious disease susceptibility. Parasite Immunol 35:386–95 [Google Scholar]
  290. Unger EK, Burke KJ, Yang CF, Bender KJ, Fuller PM, Shah NM. 2015. Medial amygdalar aromatase neurons regulate aggression in both sexes. Cell Rep 10:453–62 [Google Scholar]
  291. van Leengoed E, Kerker E, Swanson HH. 1987. Inhibition of post-partum maternal behaviour in the rat by injecting an oxytocin antagonist into the cerebral ventricles. J. Endocrinol. 112:275–82 [Google Scholar]
  292. van Noordwijk MA, van Schaik CP. 2005. Development of ecological competence in Sumatran orangutans. Am. J. Phys. Anthropol. 127:79–94 [Google Scholar]
  293. Vom Saal FS. 1985. Time-contingent change in infanticide and parental behavior induced by ejaculation in male mice. Physiol. Behav. 34:7–15 [Google Scholar]
  294. von Philipsborn AC, Jörchel S, Tirian L, Demir E, Morita T. et al. 2014. Cellular and behavioral functions of fruitless isoforms in Drosophila courtship. Curr. Biol 24:242–51 [Google Scholar]
  295. Wang B, Li Y, Wu R, Zhang S, Tai F. 2015. Behavioral responses to pups in males with different reproductive experiences are associated with changes in central OT, TH and OTR, D1R, D2R mRNA expression in mandarin voles. Horm. Behav. 67:73–82 [Google Scholar]
  296. Wang Z, Ferris CF, de Vries GJ. 1994a. Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). PNAS 91:400–4 [Google Scholar]
  297. Wang Z, Smith W, Major DE, de Vries GJ. 1994b. Sex and species differences in the effects of cohabitation on vasopressin messenger RNA expression in the bed nucleus of the stria terminalis in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus). Brain Res 650:212–18 [Google Scholar]
  298. Weissbrod A, Shapiro A, Vasserman G, Edry L, Dayan M. et al. 2013. Automated long-term tracking and social behavioural phenotyping of animal colonies within a semi-natural environment. Nat. Commun. 4:2018 [Google Scholar]
  299. Werling DM, Parikshak NN, Geschwind DH. 2016. Gene expression in human brain implicates sexually dimorphic pathways in autism spectrum disorders. Nat. Commun. 7:10717 [Google Scholar]
  300. Wolfe JL, Barnett SA. 1977. Effects of cold on nest‐building by wild and domestic mice, Mus musculus L. Biol. J. Linn. Soc. 9:73–85 [Google Scholar]
  301. Wu Z, Autry AE, Bergan JF, Watabe-Uchida M, Dulac CG. 2014. Galanin neurons in the medial preoptic area govern parental behavior. Nature 509:325–30 [Google Scholar]
  302. Würbel H. 2001. Ideal homes? Housing effects on rodent brain and behaviour. Trends Neurosci 24:207–11 [Google Scholar]
  303. Xerri C, Stern J, Merzenich M. 1994. Alterations of the cortical representation of the rat ventrum induced by nursing behavior. J. Neurosci. 14:1710–21 [Google Scholar]
  304. Xu X, Coats JK, Yang CF, Wang A, Ahmed OM. et al. 2012. Modular genetic control of sexually dimorphic behaviors. Cell 148:596–607 [Google Scholar]
  305. Yang CF, Shah NM. 2014. Representing sex in the brain, one module at a time. Neuron 82:261–78 [Google Scholar]
  306. Yang X, Schadt EE, Wang S, Wang H, Arnold AP. et al. 2006. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res 16:995–1004 [Google Scholar]
  307. Young LJ, Muns S, Wang Z, Insel TR. 1997. Changes in oxytocin receptor mRNA in rat brain during pregnancy and the effects of estrogen and interleukin‐6. J. Neuroendocrinol. 9:859–65 [Google Scholar]
  308. Zala SM, Bilak A, Perkins M, Potts WK, Penn DJ. 2015. Female house mice initially shun infected males, but do not avoid mating with them. Behav. Ecol. Sociobiol. 69:715–22 [Google Scholar]
  309. Zhao C, Driessen T, Gammie SC. 2012. Glutamic acid decarboxylase 65 and 67 expression in the lateral septum is up-regulated in association with the postpartum period in mice. Brain Res 1470:35–44 [Google Scholar]
  310. Zhao C, Li M. 2009. The receptor mechanisms underlying the disruptive effects of haloperidol and clozapine on rat maternal behavior: a double dissociation between dopamine D2 and 5-HT2A/2C receptors. Pharmacol. Biochem. Behav. 93:433–42 [Google Scholar]
  311. Ziegler TE, Prudom SL, Zahed SR, Parlow AF, Wegner F. 2009. Prolactin's mediative role in male parenting in parentally experienced marmosets (Callithrix jacchus). Horm. Behav. 56:436–43 [Google Scholar]
  312. Zilkha N, Sofer Y, Beny Y, Kimchi T. 2016. From classic ethology to modern neuroethology: overcoming the three biases in social behavior research. Curr. Opin. Neurobiol. 38:96–108 [Google Scholar]
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