Oxytocin and Parental Behaviors

  • Chihiro Yoshihara
  • Michael NumanEmail author
  • Kumi O. KurodaEmail author
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 35)


The oxytocin/vasopressin ancestor molecule has been regulating reproductive and social behaviors for more than 500 million years. In all mammals, oxytocin is the hormone indispensable for milk-ejection during nursing (maternal milk provision to offspring), a process that is crucial for successful mammalian parental care. In laboratory mice, a remarkable transcriptional activation occurs during parental behavior within the anterior commissural nucleus (AC), the largest magnocellular oxytocin cell population within the medial preoptic area (although the transcriptional activation was limited to non-oxytocinergic neurons in the AC). Furthermore, there are numerous recent reports on oxytocin’s involvement in positive social behaviors in animals and humans. Given all those, the essential involvement of oxytocin in maternal/parental behaviors may seem obvious, but basic researchers are still struggling to pin down the exact role oxytocin plays in the regulation of parental behaviors. A major aim of this review is to more clearly define this role. The best conclusion at this moment is that OT can facilitate the onset of parental behavior, or parental behavior under stressful conditions.

In this chapter, we will first review the basics of rodent parental behavior. Next, the neuroanatomy of oxytocin systems with respect to parental behavior in laboratory mice will be introduced. Then, the research history on the functional relationship between oxytocin and parental behavior, along with advancements in various techniques, will be reviewed. Finally, some technical considerations in conducting behavioral experiments on parental behavior in rodents will be addressed, with the aim of shedding light on certain pitfalls that should be avoided, so that the progress of research in this field will be facilitated. In this age of populism, researchers should strive to do even more scholarly works with further attention to methodological details.


Parental care Maternal behavior Parent-infant attachment Oxytocin Rodents 



We are very grateful for expert peer reviewers for their insightful suggestions. We would appreciate if the readers kindly let us know of any corrections or comments on this chapter at:


  1. Akther S et al (2013) CD38 in the nucleus accumbens and oxytocin are related to paternal behavior in mice. Mol Brain 6:41. doi: 10.1186/1756-6606-6-41CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alexander GM et al (2009) Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 63:27–39. doi: 10.1016/j.neuron.2009.06.014CrossRefPubMedPubMedCentralGoogle Scholar
  3. Allen Institute (2015) Website: © 2015 Allen Institute for Brain Science. Allen Mouse Brain Atlas [Internet].
  4. Allen BD, Singer AC, Boyden ES (2015) Principles of designing interpretable optogenetic behavior experiments. Learn Mem 22:232–238. doi: 10.1101/lm.038026.114CrossRefPubMedPubMedCentralGoogle Scholar
  5. Alsina-Llanes M, De Brun V, Olazabal DE (2015) Development and expression of maternal behavior in naive female C57BL/6 mice. Dev Psychobiol 57:189–200. doi: 10.1002/dev.21276CrossRefPubMedGoogle Scholar
  6. Amano T, Shindo S, Yoshihara C, Tsuneoka Y, Uki H, Minami M, Kuroda KO (2016) Development-dependent behavioral change toward pups and synaptic transmission in the rhomboid nucleus of the bed nucleus of the stria terminalis. Behav Brain Res. doi: 10.1016/j.bbr.2016.10.029CrossRefPubMedGoogle Scholar
  7. Armstrong WE, Warach S, Hatton GI, McNeill TH (1980) Subnuclei in the rat hypothalamic paraventricular nucleus: a cytoarchitectural, horseradish peroxidase and immunocytochemical analysis. Neuroscience 5:1931–1958CrossRefPubMedGoogle Scholar
  8. Banerjee P, Joy KP, Chaube R (2016) Structural and functional diversity of nonapeptide hormones from an evolutionary perspective: a review. Gen Comp Endocrinol. doi: 10.1016/j.ygcen.2016.04.025CrossRefPubMedGoogle Scholar
  9. Bayer SA, Altman J (1987) Development of the preoptic area: time and site of origin, migratory routes, and settling patterns of its neurons. J Comp Neurol 265:65–95. doi: 10.1002/cne.902650106CrossRefPubMedGoogle Scholar
  10. Beets I et al (2012) Vasopressin/oxytocin-related signaling regulates gustatory associative learning in C. elegans. Science 338:543–545. doi: 10.1126/science.1226860CrossRefPubMedGoogle Scholar
  11. Blackshaw S, Scholpp S, Placzek M, Ingraham H, Simerly R, Shimogori T (2010) Molecular pathways controlling development of thalamus and hypothalamus: from neural specification to circuit formation. J Neurosci 30:14925–14930. doi: 10.1523/JNEUROSCI.4499-10.2010CrossRefPubMedGoogle Scholar
  12. Bolwerk EL, Swanson HH (1984) Does oxytocin play a role in the onset of maternal behaviour in the rat? J Endocrinol 101:353–357CrossRefPubMedGoogle Scholar
  13. Borrow AP, Cameron NM (2012) The role of oxytocin in mating and pregnancy. Horm Behav 61:266–276. doi: 10.1016/j.yhbeh.2011.11.001CrossRefPubMedGoogle Scholar
  14. Bosch OJ, Neumann ID (2008) Brain vasopressin is an important regulator of maternal behavior independent of dams’ trait anxiety. Proc Natl Acad Sci U S A 105:17139–17144CrossRefPubMedPubMedCentralGoogle Scholar
  15. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263–1268. doi: 10.1038/nn1525CrossRefPubMedGoogle Scholar
  16. Bridges RS (2015) Neuroendocrine regulation of maternal behavior. Front Neuroendocrinol 36:178–196. doi: 10.1016/j.yfrne.2014.11.007CrossRefPubMedGoogle Scholar
  17. Bridges RS, Numan M, Ronsheim PM, Mann PE, Lupini CE (1990) Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats. Proc Natl Acad Sci U S A 87:8003–8007CrossRefPubMedPubMedCentralGoogle Scholar
  18. Bridges RS, Robertson MC, Shiu RP, Sturgis JD, Henriquez BM, Mann PE (1997) Central lactogenic regulation of maternal behavior in rats: steroid dependence, hormone specificity, and behavioral potencies of rat prolactin and rat placental lactogen I. Endocrinology 138:756–763CrossRefPubMedGoogle Scholar
  19. Brunton PJ, Russell JA (2008) Keeping oxytocin neurons under control during stress in pregnancy. Prog Brain Res 170:365–377CrossRefPubMedGoogle Scholar
  20. Calamandrei G, Keverne EB (1994) Differential expression of Fos protein in the brain of female mice dependent on pup sensory cues and maternal experience. Behav Neurosci 108:113–120CrossRefPubMedGoogle Scholar
  21. Caldwell HK, Aulino EA, Freeman AR, Miller TV, Witchey SK (2016) Oxytocin and behavior: lessons from knockout mice. Dev Neurobiol. doi: 10.1002/dneu.22431CrossRefPubMedGoogle Scholar
  22. Castel M, Morris JF (1988) The neurophysin-containing innervation of the forebrain of the mouse. Neuroscience 24:937–966CrossRefPubMedGoogle Scholar
  23. Chalfin L et al (2014) Mapping ecologically relevant social behaviours by gene knockout in wild mice. Nat Commun 5:4569. doi: 10.1038/ncomms5569CrossRefPubMedGoogle Scholar
  24. Champagne FA (2008) Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29:386–397. doi: 10.1016/j.yfrne.2008.03.003CrossRefPubMedPubMedCentralGoogle Scholar
  25. Champagne FA (2009) Nurturing nature: social experiences and the brain. J Neuroendocrinol 21:867–868. doi: 10.1111/j.1365-2826.2009.01901.xCrossRefPubMedGoogle Scholar
  26. Champagne F, Meaney MJ (2001) Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 133:287–302CrossRefPubMedGoogle Scholar
  27. Champagne F, Diorio J, Sharma S, Meaney MJ (2001) Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci U S A 98:12736–12741CrossRefPubMedPubMedCentralGoogle Scholar
  28. Champagne FA, Curley JP, Swaney WT, Hasen NS, Keverne EB (2009) Paternal influence on female behavior: the role of Peg3 in exploration, olfaction, and neuroendocrine regulation of maternal behavior of female mice. Behav Neurosci 123:469–480CrossRefPubMedGoogle Scholar
  29. Collins FS, Tabak LA (2014) Policy: NIH plans to enhance reproducibility. Nature 505:612–613CrossRefPubMedPubMedCentralGoogle Scholar
  30. D’Cunha TM, King SJ, Fleming AS, Levy F (2011) Oxytocin receptors in the nucleus accumbens shell are involved in the consolidation of maternal memory in postpartum rats. Horm Behav 59:14–21. doi: 10.1016/j.yhbeh.2010.09.007CrossRefPubMedGoogle Scholar
  31. Denizot AL et al (2016) A novel mutant allele of Pw1/Peg3 does not affect maternal behavior or nursing behavior. PLoS Genet 12:e1006053. doi: 10.1371/journal.pgen.1006053CrossRefPubMedPubMedCentralGoogle Scholar
  32. Dolen G, Darvishzadeh A, Huang KW, Malenka RC (2013) Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 501:179–184. doi: 10.1038/nature12518CrossRefPubMedPubMedCentralGoogle Scholar
  33. Douglas AJ (2010) Baby love? Oxytocin-dopamine interactions in mother-infant bonding. Endocrinology 151:1978–1980. doi: 10.1210/en.2010-0259CrossRefPubMedGoogle Scholar
  34. Elwood RW (1977) Changes in the responses of male and female gerbils (Meriones unguiculatus) toward test pups during the pregnancy of the female. Anim Behav 25:46–51CrossRefGoogle Scholar
  35. Elwood RW (1983) Parental behaviour of rodents. Wiley, ChichesterGoogle Scholar
  36. Fahrbach SE, Morrell JI, Pfaff DW (1984) Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats. Horm Behav 18:267–286CrossRefPubMedGoogle Scholar
  37. Fahrbach SE, Morrell JI, Pfaff DW (1985) Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 40:526–532CrossRefPubMedGoogle Scholar
  38. Fahrbach SE, Morrell JI, Pfaff DW (1986) Effect of varying the duration of pre-test cage habituation on oxytocin induction of short-latency maternal behavior. Physiol Behav 37:135–139CrossRefPubMedGoogle Scholar
  39. Fisher AE (1956) Maternal and sexual behavior induced by intracranial chemical stimulation. Science 124:228–229CrossRefPubMedGoogle Scholar
  40. Fossey D (1984) Infanticide in mountain gorillas (Gorilla gorilla beringei) with comparative notes on chimpanzees. In: Hausfater G, Hrdy SB (eds) Infanticide: comparative and evolutionary perspectives. AJdine. Wenner-Gren Foundation for Anthropological Research, New York, pp 217–236Google Scholar
  41. Francis D, Diorio J, Liu D, Meaney MJ (1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155–1158CrossRefPubMedGoogle Scholar
  42. Garrison JL, Macosko EZ, Bernstein S, Pokala N, Albrecht DR, Bargmann CI (2012) Oxytocin/vasopressin-related peptides have an ancient role in reproductive behavior. Science 338:540–543. doi: 10.1126/science.1226201CrossRefPubMedPubMedCentralGoogle Scholar
  43. Gonzalez-Mariscal G, Caba M, Martinez-Gomez 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. doi: 10.1016/j.yhbeh.2015.05.011CrossRefPubMedGoogle Scholar
  44. Grinevich V, Akmayev I (1997) An accessory magnocellular nucleus, anterior commissural nucleus, in the rat hypothalamus: immunohistochemical, tract-tracing, in situ hybridization, and experimental studies. Biogenic Amines 13:333–348Google Scholar
  45. Gross GA et al (1998) Opposing actions of prostaglandins and oxytocin determine the onset of murine labor. Proc Natl Acad Sci U S A 95:11875–11879CrossRefPubMedPubMedCentralGoogle Scholar
  46. Herdegen T, Leah JD (1998) Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Brain Res Rev 28:370–490CrossRefPubMedGoogle Scholar
  47. Herrenkohl LR, Rosenberg PA (1972) Exteroceptive stimulation of maternal behavior in the naive rat. Physiol Behav 8:595–598CrossRefPubMedGoogle Scholar
  48. Herrenkohl LR, Rosenberg PA (1974) Effects of hypothalamic deafferentation late in gestation on lactation and nursing behavior in the rat. Horm Behav 5:33–41CrossRefPubMedGoogle Scholar
  49. Higashida H (2007) CD38-dependent oxytocin release on social and parental behavior. In: Parental brain conference, BostonGoogle Scholar
  50. Horsthemke B, Surani A, James T, Ohlsson R (1999) The mechanisms of genomic imprinting. Results Probl Cell Differ 25:91–118CrossRefPubMedGoogle Scholar
  51. Hrdy SB (1974) Male-male competition and infanticide among the langurs (Presbytis entellus) of Abu, Rajasthan. Folia Primatol (Basel) 22:19–58CrossRefGoogle Scholar
  52. Hrdy SB (1977) Infanticide as a primate reproductive strategy. Am Sci 65:40–49PubMedGoogle Scholar
  53. Insel TR (2010) The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65:768–779CrossRefPubMedPubMedCentralGoogle Scholar
  54. Insel TR, Harbaugh CR (1989) Lesions of the hypothalamic paraventricular nucleus disrupt the initiation of maternal behavior. Physiol Behav 45:1033–1041CrossRefPubMedGoogle Scholar
  55. Insel TR, Gingrich BS, Young LJ (2001) Oxytocin: who needs it? Prog Brain Res 133:59–66CrossRefPubMedGoogle Scholar
  56. Jakubowski M, Terkel J (1982) Infanticide and caretaking in non-lactating Mus musculus: influence of genotype, family group and sex. Anim Behav 30:1029–1035CrossRefGoogle Scholar
  57. Jin D et al (2007) CD38 is critical for social behaviour by regulating oxytocin secretion. Nature 446:41–45CrossRefPubMedGoogle Scholar
  58. Kalinichev M, Rosenblatt JS, Morrell JI (2000) The medial preoptic area, necessary for adult maternal behavior in rats, is only partially established as a component of the neural circuit that supports maternal behavior in juvenile rats. Behav Neurosci 114:196–210CrossRefPubMedGoogle Scholar
  59. Kennedy HF, Elwood RW (1988) Strain differences in the inhibition of infanticide in male mice (Mus musculus). Behav Neural Biol 50:349–353CrossRefPubMedGoogle Scholar
  60. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8:e1000412. doi: 10.1371/journal.pbio.1000412CrossRefPubMedPubMedCentralGoogle Scholar
  61. Kirkpatrick B, Kim JW, Insel TR (1994) Limbic system fos expression associated with paternal behavior. Brain Res 658:112–118CrossRefPubMedGoogle Scholar
  62. Knobloch HS, Grinevich V (2014) Evolution of oxytocin pathways in the brain of vertebrates. Front Behav Neurosci 8:31. doi: 10.3389/fnbeh.2014.00031CrossRefPubMedPubMedCentralGoogle Scholar
  63. Krasnegor NA, Bridges RS (1990) Mammalian parenting: biochemical, neurobiological, and behavioral determinants. Oxford University Press, New YorkGoogle Scholar
  64. Kuroda KO, Tsuneoka Y (2013) Assessing postpartum maternal care, alloparental behavior, and infanticide in mice: with notes on chemosensory influences. Methods Mol Biol 1068:331–347. doi: 10.1007/978-1-62703-619-1_25CrossRefPubMedGoogle Scholar
  65. Kuroda KO, Meaney MJ, Uetani N, Fortin Y, Ponton A, Kato T (2007) ERK-FosB signaling in dorsal MPOA neurons plays a major role in the initiation of parental behavior in mice. Mol Cell Neurosci 36:121–131CrossRefPubMedGoogle Scholar
  66. Kuroda KO, Meaney MJ, Uetani N, Kato T (2008) Neurobehavioral basis of the impaired nurturing in mice lacking the immediate early gene FosB. Brain Res 1211:57–71CrossRefPubMedGoogle Scholar
  67. 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 Neuropsychopharmacol Biol Psychiatry 35:1205–1231. doi: 10.1016/j.pnpbp.2011.02.008CrossRefPubMedGoogle Scholar
  68. Larhammar D, Sundstrom G, Dreborg S, Daza DO, Larsson TA (2009) Major genomic events and their consequences for vertebrate evolution and endocrinology. Ann N Y Acad Sci 1163:201–208. doi: 10.1111/j.1749-6632.2008.03659.xCrossRefPubMedGoogle Scholar
  69. Leblond CP (1940) Extra-hormonal factors in maternal behavior. Proc Soc Exp Biol Med 38:66–70CrossRefGoogle Scholar
  70. Leblond CP, Nelson WO (1937) Maternal behavior in hypophysectomized male and female mice. Am J Physiol 120:167–172Google Scholar
  71. Lee AW, Brown RE (2002) Medial preoptic lesions disrupt parental behavior in both male and female California mice (Peromyscus californicus). Behav Neurosci 116:968–975CrossRefPubMedGoogle Scholar
  72. Lee HJ, Caldwell HK, Macbeth AH, Tolu SG, Young WS 3rd (2008) A conditional knockout mouse line of the oxytocin receptor. Endocrinology 149:3256–3263CrossRefPubMedPubMedCentralGoogle Scholar
  73. Lein ES et al (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168–176. doi: 10.1038/nature05453CrossRefPubMedGoogle Scholar
  74. Leng G, Ludwig M (2016) Intranasal oxytocin: myths and delusions biol. Psychiatry 79:243–250. doi: 10.1016/j.biopsych.2015.05.003CrossRefGoogle Scholar
  75. Li C, Chen P, Smith MS (1999a) Neural populations in the rat forebrain and brainstem activated by the suckling stimulus as demonstrated by cFos expression. Neuroscience 94:117–129CrossRefPubMedGoogle Scholar
  76. Li L, Keverne EB, Aparicio SA, Ishino F, Barton SC, Surani MA (1999b) Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science 284:330–333CrossRefPubMedGoogle Scholar
  77. Li K, Nakajima M, Ibanez-Tallon I, Heintz N (2016) A cortical circuit for sexually dimorphic oxytocin-dependent anxiety behaviors. Cell 167:60–72. e11. doi: 10.1016/j.cell.2016.08.067CrossRefPubMedPubMedCentralGoogle Scholar
  78. Lonstein JS, De Vries GJ (2000) Sex differences in the parental behavior of rodents. Neurosci Biobehav Rev 24:669–686CrossRefPubMedGoogle Scholar
  79. Lonstein JS, Fleming AS (2002) Parental behaviors in rats and mice. Curr Protoc Neurosci Chapter 8:8.15.11–18.15.26Google Scholar
  80. Lonstein JS, Simmons DA, Swann JM, Stern JM (1998) Forebrain expression of c-fos due to active maternal behaviour in lactating rats. Neuroscience 82:267–281CrossRefPubMedGoogle Scholar
  81. Lonstein JS, Levy F, Fleming AS (2015a) Common and divergent psychobiological mechanisms underlying maternal behaviors in non-human and human mammals. Horm Behav 73:156–185. doi: 10.1016/j.yhbeh.2015.06.011CrossRefPubMedPubMedCentralGoogle Scholar
  82. Lonstein JS, Pereira M, Morrell JI, Marler CA (2015b) Parental behavior. In: Plant TM, Zelenik AJ (eds) Knobil and Neill’s physiology of reproduction, 4th edn. Academic Press, WalthamGoogle Scholar
  83. Lopatina O, Inzhutova A, Pichugina YA, Okamoto H, Salmina AB, Higashida H (2011) Reproductive experience affects parental retrieval behaviour associated with increased plasma oxytocin levels in wild-type and CD38-knockout mice. J Neuroendocrinol 23:1125–1133. doi: 10.1111/j.1365-2826.2011.02136.xCrossRefPubMedGoogle Scholar
  84. Macbeth AH, Lee HJ, Edds J, Young WS 3rd (2009) Oxytocin and the oxytocin receptor underlie intrastrain, but not interstrain, social recognition. Genes Brain Behav 8:558–567. doi: 10.1111/j.1601-183X.2009.00506.xCrossRefPubMedPubMedCentralGoogle Scholar
  85. Macbeth AH, Stepp JE, Lee HJ, Young WS 3rd, Caldwell HK (2010) Normal maternal behavior, but increased pup mortality, in conditional oxytocin receptor knockout females. Behav Neurosci 124:677–685CrossRefPubMedPubMedCentralGoogle Scholar
  86. Marlin BJ, Mitre M, D'Amour JA, Chao MV, Froemke RC (2015) Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature 520:499–504. doi: 10.1038/nature14402CrossRefPubMedPubMedCentralGoogle Scholar
  87. McCarthy MM (1995) Estrogen modulation of oxytocin and its relation to behavior. Adv Exp Med Biol 395:235–245PubMedGoogle Scholar
  88. McCarthy MM, vom Saal FS (1985) The influence of reproductive state on infanticide by wild female house mice (Mus musculus). Physiol Behav 35:843–849CrossRefPubMedGoogle Scholar
  89. Mitre M et al (2016) A distributed network for social cognition enriched for oxytocin receptors. J Neurosci 36:2517–2535. doi: 10.1523/JNEUROSCI.2409-15.2016CrossRefPubMedPubMedCentralGoogle Scholar
  90. Murphy MR, MacLean PD, Hamilton SC (1981) Species-typical behavior of hamsters deprived from birth of the neocortex. Science 213:459–461CrossRefPubMedGoogle Scholar
  91. Nakajima M, Gorlich A, Heintz N (2014) Oxytocin modulates female sociosexual behavior through a specific class of prefrontal cortical interneurons. Cell 159:295–305. doi: 10.1016/j.cell.2014.09.020CrossRefPubMedPubMedCentralGoogle Scholar
  92. Neumann ID (2008) Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J Neuroendocrinol 20:858–865CrossRefPubMedGoogle Scholar
  93. Neumann ID, Landgraf R (2012) Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci 35:649–659. doi: 10.1016/j.tins.2012.08.004CrossRefPubMedPubMedCentralGoogle Scholar
  94. 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. Proc Natl Acad Sci U S A 93:11699–11704CrossRefPubMedPubMedCentralGoogle Scholar
  95. Noirot E (1972) The onset of maternal behavior in rats, hamsters, and mice a selective review. In: Lehrman DS, Hinde RA, Shaw E (eds) Advances in the study of behavior, vol 4. Elsevier, New York, pp 107–145Google Scholar
  96. Numan M (1974) Medial preoptic area and maternal behavior in the female rat. J Comp Physiol Psychol 87:746–759CrossRefPubMedGoogle Scholar
  97. Numan M (1994) Maternal behavior. In: Knobili E, Neill JD (eds) The physiology of reproduction, 2nd edn, vol 2. Raven, New York, pp 221–302Google Scholar
  98. Numan M (2015) Neurobiology of social behavior: toward an understanding of prosocial and antisocial brain. Elsevier, LondonGoogle Scholar
  99. Numan M (2017) Parental behavior. In: Reference module in neuroscience and biobehavioral psychology. Elsevier, AmsterdamGoogle Scholar
  100. Numan M, Corodimas KP (1985) The effects of paraventricular hypothalamic lesions on maternal behavior in rats. Physiol Behav 35:417–425CrossRefPubMedGoogle Scholar
  101. Numan M, Insel TR (2003) The neurobiology of parental behavior. Springer, New YorkGoogle Scholar
  102. Numan M, Numan MJ (1994) Expression of Fos-like immunoreactivity in the preoptic area of maternally behaving virgin and postpartum rats. Behav Neurosci 108:379–394CrossRefPubMedGoogle Scholar
  103. Numan M, Stolzenberg DS (2009) Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats. Front Neuroendocrinol 30:46–64. doi: 10.1016/j.yfrne.2008.10.002CrossRefPubMedGoogle Scholar
  104. Numan M, Young LJ (2016) Neural mechanisms of mother-infant bonding and pair bonding: similarities, differences, and broader implications. Horm Behav 77:98–112. doi: 10.1016/j.yhbeh.2015.05.015CrossRefPubMedGoogle Scholar
  105. Numan M, Rosenblatt JS, Komisaruk BR (1977) Medial preoptic area and onset of maternal behavior in the rat. J Comp Physiol Psychol 91:146–164CrossRefPubMedGoogle Scholar
  106. Numan M, Corodimas KP, Numan MJ, Factor EM, Piers WD (1988) Axon-sparing lesions of the preoptic region and substantia innominata disrupt maternal behavior in rats. Behav Neurosci 102:381–396CrossRefPubMedGoogle Scholar
  107. Oettl LL et al (2016) Oxytocin enhances social recognition by modulating cortical control of early olfactory processing. Neuron 90:609–621. doi: 10.1016/j.neuron.2016.03.033CrossRefPubMedPubMedCentralGoogle Scholar
  108. Olazabal DE, Alsina-Llanes M (2016) Are age and sex differences in brain oxytocin receptors related to maternal and infanticidal behavior in naive mice? Horm Behav 77:132–140. doi: 10.1016/j.yhbeh.2015.04.006CrossRefPubMedGoogle Scholar
  109. Onaka T, Takayanagi Y, Yoshida M (2012) Roles of oxytocin neurones in the control of stress, energy metabolism, and social behaviour. J Neuroendocrinol 24:587–598. doi: 10.1111/j.1365-2826.2012.02300.xCrossRefPubMedGoogle Scholar
  110. Owen SF, Tuncdemir SN, Bader PL, Tirko NN, Fishell G, Tsien RW (2013) Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons. Nature 500:458–462. doi: 10.1038/nature12330CrossRefPubMedPubMedCentralGoogle Scholar
  111. Packer C, Pusey AE (1984) Infanticide in carnivores. In: Hausfater G, Hrdy SB (eds) Infanticide: comparative and evolutionary perspectives. AJdine. Wenner-Gren Foundation for Anthropological Research, New York, pp 31–42Google Scholar
  112. Pagani JH et al (2015) Raphe serotonin neuron-specific oxytocin receptor knockout reduces aggression without affecting anxiety-like behavior in male mice only. Genes Brain Behav 14:167–176. doi: 10.1111/gbb.12202CrossRefPubMedPubMedCentralGoogle Scholar
  113. Parmigiani S, Palanza P, Rogers J, Ferrari PF (1999) Selection, evolution of behavior and animal models in behavioral neuroscience. Neurosci Biobehav Rev 23:957–969CrossRefPubMedGoogle Scholar
  114. Paxinos G (2004) The rat nervous system. Elsevier, San DiegoGoogle Scholar
  115. Paxinos G, Franklin KBJ (2013) The mouse brain in stereotaxic coordinates, 4th edn. Academic Press, San DiegoGoogle Scholar
  116. Pedersen CA, Prange AJ Jr (1979) Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci U S A 76:6661–6665CrossRefPubMedPubMedCentralGoogle Scholar
  117. Pedersen CA, Ascher JA, Monroe YL, Prange AJ (1982) Oxytocin induces maternal-behavior in virgin female rats. Science 216:648–650. doi: 10.1126/science.7071605CrossRefPubMedPubMedCentralGoogle Scholar
  118. Pedersen CA, Caldwell JD, Johnson MF, Fort SA, Prange AJ Jr (1985) Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior. Neuropeptides 6:175–182CrossRefPubMedGoogle Scholar
  119. Pedersen CA, Caldwell JD, Peterson G, Walker CH, Mason GA (1992) Oxytocin activation of maternal-behavior in the rat. Ann N Y Acad Sci 652:58–69. doi: 10.1111/j.1749-6632.1992.tb34346.xCrossRefPubMedGoogle Scholar
  120. 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 108:1163–1171CrossRefPubMedGoogle Scholar
  121. Pedersen CA, Vadlamudi SV, Boccia ML, Amico JA (2006) Maternal behavior deficits in nulliparous oxytocin knockout mice. Genes Brain Behav 5:274–281CrossRefPubMedGoogle Scholar
  122. Peterson RP (1966) Magnocellular neurosecretory centers in the rat hypothalamus. J Comp Neurol 128:181–190. doi: 10.1002/cne.901280205CrossRefPubMedGoogle Scholar
  123. Porteous R et al (2011) Kisspeptin neurons co-express met-enkephalin and galanin in the rostral periventricular region of the female mouse hypothalamus. J Comp Neurol 519:3456–3469. doi: 10.1002/cne.22716CrossRefPubMedGoogle Scholar
  124. Priestnall R, Young S (1978) An observational study of caretaking behavior of male and female mice housed together. Dev Psychobiol 11:23–30CrossRefPubMedGoogle Scholar
  125. Puelles L et al (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J Comp Neurol 424:409–438CrossRefPubMedGoogle Scholar
  126. Ragnauth AK et al (2005) Female oxytocin gene-knockout mice, in a semi-natural environment, display exaggerated aggressive behavior. Genes Brain Behav 4:229–239CrossRefPubMedGoogle Scholar
  127. Rhodes CH, Morrell JI, Pfaff DW (1981) Immunohistochemical analysis of magnocellular elements in rat hypothalamus: distribution and numbers of cells containing neurophysin, oxytocin, and vasopressin. J Comp Neurol 198:45–64. doi: 10.1002/cne.901980106CrossRefPubMedGoogle Scholar
  128. Ribeiro AC, Musatov S, Shteyler A, Simanduyev S, Arrieta-Cruz I, Ogawa S, Pfaff DW (2012) siRNA silencing of estrogen receptor-alpha expression specifically in medial preoptic area neurons abolishes maternal care in female mice. Proc Natl Acad Sci U S A 109:16324–16329. doi: 10.1073/pnas.1214094109CrossRefPubMedPubMedCentralGoogle Scholar
  129. Rich ME, deCardenas EJ, Lee HJ, Caldwell HK (2014) Impairments in the initiation of maternal behavior in oxytocin receptor knockout mice. PLoS One 9:e98839. doi: 10.1371/journal.pone.0098839CrossRefPubMedPubMedCentralGoogle Scholar
  130. Rilling JK, Young LJ (2014) The biology of mammalian parenting and its effect on offspring social development. Science 345:771–776. doi: 10.1126/science.1252723CrossRefPubMedPubMedCentralGoogle Scholar
  131. Rosenblatt JS (1967) Nonhormonal basis of maternal behavior in the rat. Science 156:1512–1514CrossRefPubMedGoogle Scholar
  132. Rosenblatt JS (1969) The development of maternal responsiveness in the rat. Am J Orthopsychiatry 39:36–56CrossRefPubMedGoogle Scholar
  133. Rosenblatt JS, Lehrman DS (1963) Maternal behavior of the laboratory rat. In: Rheingold HL (ed) Maternal behavior in mammals. Wiley, New York, pp 8–57Google Scholar
  134. Rosenblatt JS, Snowdon CT (eds) (1996) Parental care: evolution, mechanism, and adaptive significance, Advances in the study of behavior, vol 25. Academic Press, San DiegoGoogle Scholar
  135. Rossant J, McMahon A (1999) Creating mouse mutants-a meeting review on conditional mouse genetics. Genes Dev 13:142–145CrossRefPubMedGoogle Scholar
  136. Russell JA, Leng G (1998) Sex, parturition and motherhood without oxytocin? J Endocrinol 157:343–359. doi: 10.1677/joe.0.1570343CrossRefPubMedGoogle Scholar
  137. Schaller GB (1972) The Serengeti lion: a study of predator-prey relations. University of Chicago Press, ChicagoGoogle Scholar
  138. Schorscher-Petcu A et al (2010) Oxytocin-induced analgesia and scratching are mediated by the vasopressin-1A receptor in the mouse. J Neurosci 30:8274–8284. doi: 10.1523/JNEUROSCI.1594-10.2010CrossRefPubMedPubMedCentralGoogle Scholar
  139. Scott N, Prigge M, Yizhar O, Kimchi T (2015) A sexually dimorphic hypothalamic circuit controls maternal care and oxytocin secretion. Nature 525:519–522. doi: 10.1038/nature15378CrossRefPubMedGoogle Scholar
  140. Shahrokh DK, Zhang TY, Diorio J, Gratton A, Meaney MJ (2010) Oxytocin-dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology 151:2276–2286. doi: 10.1210/en.2009-1271CrossRefPubMedPubMedCentralGoogle Scholar
  141. Shen H (2015) Neuroscience: the hard science of oxytocin. Nature 522:410–412. doi: 10.1038/522410aCrossRefPubMedGoogle Scholar
  142. Simerly RB (2004) Anatomical substrates of hypothalamic integration. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier, San Diego, pp 336–368Google Scholar
  143. Simerly RB, Zee MC, Pendleton JW, Lubahn DB, Korach KS (1997) Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of the mouse. Proc Natl Acad Sci U S A 94:14077–14082CrossRefPubMedPubMedCentralGoogle Scholar
  144. Sofroniew MV (1985) Vasopressin- and neurophysin-immunoreactive neurons in the septal region, medial amygdala and locus coeruleus in colchicine-treated rats. Neuroscience 15:347–358CrossRefPubMedGoogle Scholar
  145. 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 36:1275–1281CrossRefGoogle Scholar
  146. Stolzenberg DS, Rissman EF (2011) Oestrogen-independent, experience-induced maternal behaviour in female mice. J Neuroendocrinol 23:345–354. doi: 10.1111/j.1365-2826.2011.02112.xCrossRefPubMedPubMedCentralGoogle Scholar
  147. Sugiyama Y (1965) On the social change of hanuman langurs (Presbytis entellus). Primates 6:381–418CrossRefGoogle Scholar
  148. 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 33:5120–5126. doi: 10.1523/JNEUROSCI.2364-12.2013CrossRefPubMedGoogle Scholar
  149. Takayanagi Y et al (2005) Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc Natl Acad Sci U S A 102:16096–16101CrossRefPubMedPubMedCentralGoogle Scholar
  150. Terkel J, Bridges RS, Sawyer CH (1979) Effects of transecting lateral neural connections of the medial preoptic area on maternal behavior in the rat: nest building, pup retrieval and prolactin secretion. Brain Res 169:369–380CrossRefPubMedGoogle Scholar
  151. Thackare H, Nicholson HD, Whittington K (2006) Oxytocin – its role in male reproduction and new potential therapeutic uses. Hum Reprod Update 12:437–448. doi: 10.1093/humupd/dmk002CrossRefPubMedGoogle Scholar
  152. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871-1971. Aldine-Atherton, Chicago, pp 136–172Google Scholar
  153. Tsuneoka Y, Maruyama T, Yoshida S, Nishimori K, Kato T, Numan M, Kuroda KO (2013) Functional, anatomical, and neurochemical differentiation of medial preoptic area subregions in relation to maternal behavior in the mouse. J Comp Neurol 521:1633–1663. doi: 10.1002/cne.23251CrossRefPubMedGoogle Scholar
  154. Tsuneoka Y et al (2015) Distinct preoptic-BST nuclei dissociate paternal and infanticidal behavior in mice. EMBO J 34:2652–2670. doi: 10.15252/embj.201591942CrossRefPubMedPubMedCentralGoogle Scholar
  155. Tsuneoka Y et al (under submission) Genetic targeting of oxytocin and vasopressin receptors and the pup-directed behaviors in miceGoogle Scholar
  156. Vanleengoed E, Kerker E, Swanson HH (1987) Inhibition of postpartum maternal-behavior in the rat by injecting an oxytocin antagonist into the cerebral-ventricles. J Endocrinol 112:275–282. doi: 10.1677/joe.0.1120275CrossRefGoogle Scholar
  157. Viviani D et al (2011) Oxytocin selectively gates fear responses through distinct outputs from the central amygdala. Science 333:104–107. doi: 10.1126/science.1201043CrossRefPubMedGoogle Scholar
  158. vom Saal FS (1985) Time-contingent change in infanticide and parental behavior induced by ejaculation in male mice. Physiol Behav 34:7–15CrossRefGoogle Scholar
  159. vom Saal FS, Howard LS (1982) The regulation of infanticide and parental behavior: implications for reproductive success in male mice. Science 215:1270–1272CrossRefGoogle Scholar
  160. Wakerley JB (2005) Milk ejection and its control. In: Neill JD (ed) Knobil and Neill’s physiology of reproduction, vol 1, 3rd edn. Elsevier, pp 3129–3190CrossRefGoogle Scholar
  161. Wamboldt MZ, Insel TR (1987) The ability of oxytocin to induce short latency maternal behavior is dependent on peripheral anosmia. Behav Neurosci 101:439–441CrossRefPubMedGoogle Scholar
  162. Wiesner BP, Sheard NM (1933) Maternal behaviour in the rat. Oliver and Boyd, LondonGoogle Scholar
  163. Winslow JT, Hearn EF, Ferguson J, Young LJ, Matzuk MM, Insel TR (2000) Infant vocalization, adult aggression, and fear behavior of an oxytocin null mutant mouse. Horm Behav 37:145–155CrossRefPubMedGoogle Scholar
  164. Wright SL, Brown RE (2000) Maternal behavior, paternal behavior, and pup survival in CD-1 albino mice (Mus musculus) in three different housing conditions. J Comp Psychol 114:183–192CrossRefPubMedGoogle Scholar
  165. Wu Z, Autry AE, Bergan JF, Watabe-Uchida M, Dulac CG (2014) Galanin neurons in the medial preoptic area govern parental behaviour. Nature 509:325–330. doi: 10.1038/nature13307CrossRefPubMedPubMedCentralGoogle Scholar
  166. Yoshida M, Takayanagi Y, Inoue K, Kimura T, Young LJ, Onaka T, Nishimori K (2009) Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice. J Neurosci 29:2259–2271CrossRefPubMedGoogle Scholar
  167. Young WS 3rd et al (1996) Deficiency in mouse oxytocin prevents milk ejection, but not fertility or parturition. J Neuroendocrinol 8:847–853CrossRefPubMedGoogle Scholar
  168. Zhao W et al (2016) Oxytocin blurs the self-other distinction during trait judgments and reduces medial prefrontal cortex responses. Hum Brain Mapp 37:2512–2527. doi: 10.1002/hbm.23190CrossRefPubMedGoogle Scholar
  169. Zheng JJ, Li SJ, Zhang XD, Miao WY, Zhang D, Yao H, Yu X (2014) Oxytocin mediates early experience-dependent cross-modal plasticity in the sensory cortices. Nat Neurosci 17:391–399. doi: 10.1038/nn.3634CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Laboratory for Affiliative Social BehaviorRIKEN Brain Science InstituteSaitamaJapan
  2. 2.Department of PsychologyUniversity of New MexicoAlbuquerqueUSA

Personalised recommendations