Oxytocin and Parental Behaviors

  • Chapter
  • First Online:
Behavioral Pharmacology of Neuropeptides: Oxytocin

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 35))

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
EUR 29.95
Price includes VAT (Germany)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 192.59
Price includes VAT (Germany)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
EUR 246.09
Price includes VAT (Germany)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
EUR 246.09
Price includes VAT (Germany)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Akther S et al (2013) CD38 in the nucleus accumbens and oxytocin are related to paternal behavior in mice. Mol Brain 6:41. doi:10.1186/1756-6606-6-41

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.2009.06.014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Allen Institute (2015) Website: © 2015 Allen Institute for Brain Science. Allen Mouse Brain Atlas [Internet]. http://mouse.brain-map.org

  • Allen BD, Singer AC, Boyden ES (2015) Principles of designing interpretable optogenetic behavior experiments. Learn Mem 22:232–238. doi:10.1101/lm.038026.114

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.21276

    Article  PubMed  Google Scholar 

  • 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.2016.10.029

    Article  PubMed  Google Scholar 

  • Armstrong WE, Warach S, Hatton GI, McNeill TH (1980) Subnuclei in the rat hypothalamic paraventricular nucleus: a cytoarchitectural, horseradish peroxidase and immunocytochemical analysis. Neuroscience 5:1931–1958

    Article  CAS  PubMed  Google Scholar 

  • 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.2016.04.025

    Article  PubMed  CAS  Google Scholar 

  • 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.902650106

    Article  PubMed  CAS  Google Scholar 

  • Beets I et al (2012) Vasopressin/oxytocin-related signaling regulates gustatory associative learning in C. elegans. Science 338:543–545. doi:10.1126/science.1226860

    Article  PubMed  CAS  Google Scholar 

  • 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.4499-10.2010

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bolwerk EL, Swanson HH (1984) Does oxytocin play a role in the onset of maternal behaviour in the rat? J Endocrinol 101:353–357

    Article  CAS  PubMed  Google Scholar 

  • Borrow AP, Cameron NM (2012) The role of oxytocin in mating and pregnancy. Horm Behav 61:266–276. doi:10.1016/j.yhbeh.2011.11.001

    Article  PubMed  CAS  Google Scholar 

  • 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 105:17139–17144

    Article  PubMed  PubMed Central  Google Scholar 

  • 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/nn1525

    Article  PubMed  CAS  Google Scholar 

  • Bridges RS (2015) Neuroendocrine regulation of maternal behavior. Front Neuroendocrinol 36:178–196. doi:10.1016/j.yfrne.2014.11.007

    Article  PubMed  CAS  Google Scholar 

  • 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 87:8003–8007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 138:756–763

    Article  CAS  PubMed  Google Scholar 

  • Brunton PJ, Russell JA (2008) Kee** oxytocin neurons under control during stress in pregnancy. Prog Brain Res 170:365–377

    Article  CAS  PubMed  Google Scholar 

  • 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 108:113–120

    Article  CAS  PubMed  Google Scholar 

  • Caldwell HK, Aulino EA, Freeman AR, Miller TV, Witchey SK (2016) Oxytocin and behavior: lessons from knockout mice. Dev Neurobiol. doi:10.1002/dneu.22431

    Article  PubMed  CAS  Google Scholar 

  • Castel M, Morris JF (1988) The neurophysin-containing innervation of the forebrain of the mouse. Neuroscience 24:937–966

    Article  CAS  PubMed  Google Scholar 

  • Chalfin L et al (2014) Map** ecologically relevant social behaviours by gene knockout in wild mice. Nat Commun 5:4569. doi:10.1038/ncomms5569

    Article  PubMed  CAS  Google Scholar 

  • Champagne FA (2008) Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29:386–397. doi:10.1016/j.yfrne.2008.03.003

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Champagne FA (2009) Nurturing nature: social experiences and the brain. J Neuroendocrinol 21:867–868. doi:10.1111/j.1365-2826.2009.01901.x

    Article  PubMed  CAS  Google Scholar 

  • Champagne F, Meaney MJ (2001) Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 133:287–302

    Article  CAS  PubMed  Google Scholar 

  • 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 98:12736–12741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 123:469–480

    Article  PubMed  Google Scholar 

  • Collins FS, Tabak LA (2014) Policy: NIH plans to enhance reproducibility. Nature 505:612–613

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.2010.09.007

    Article  PubMed  CAS  Google Scholar 

  • 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.1006053

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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/nature12518

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Douglas AJ (2010) Baby love? Oxytocin-dopamine interactions in mother-infant bonding. Endocrinology 151:1978–1980. doi:10.1210/en.2010-0259

    Article  PubMed  CAS  Google Scholar 

  • 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 25:46–51

    Article  Google Scholar 

  • Elwood RW (1983) Parental behaviour of rodents. Wiley, Chichester

    Google Scholar 

  • Fahrbach SE, Morrell JI, Pfaff DW (1984) Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats. Horm Behav 18:267–286

    Article  CAS  PubMed  Google Scholar 

  • Fahrbach SE, Morrell JI, Pfaff DW (1985) Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 40:526–532

    Article  CAS  PubMed  Google Scholar 

  • 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 37:135–139

    Article  CAS  PubMed  Google Scholar 

  • Fisher AE (1956) Maternal and sexual behavior induced by intracranial chemical stimulation. Science 124:228–229

    Article  CAS  PubMed  Google Scholar 

  • 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 217–236

    Google Scholar 

  • Francis D, Diorio J, Liu D, Meaney MJ (1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155–1158

    Article  CAS  PubMed  Google Scholar 

  • 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.1226201

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.2015.05.011

    Article  PubMed  CAS  Google Scholar 

  • 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 13:333–348

    CAS  Google Scholar 

  • Gross GA et al (1998) Opposing actions of prostaglandins and oxytocin determine the onset of murine labor. Proc Natl Acad Sci U S A 95:11875–11879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 28:370–490

    Article  CAS  PubMed  Google Scholar 

  • Herrenkohl LR, Rosenberg PA (1972) Exteroceptive stimulation of maternal behavior in the naive rat. Physiol Behav 8:595–598

    Article  CAS  PubMed  Google Scholar 

  • Herrenkohl LR, Rosenberg PA (1974) Effects of hypothalamic deafferentation late in gestation on lactation and nursing behavior in the rat. Horm Behav 5:33–41

    Article  CAS  PubMed  Google Scholar 

  • Higashida H (2007) CD38-dependent oxytocin release on social and parental behavior. In: Parental brain conference, Boston

    Google Scholar 

  • Horsthemke B, Surani A, James T, Ohlsson R (1999) The mechanisms of genomic imprinting. Results Probl Cell Differ 25:91–118

    Article  CAS  PubMed  Google Scholar 

  • Hrdy SB (1974) Male-male competition and infanticide among the langurs (Presbytis entellus) of Abu, Rajasthan. Folia Primatol (Basel) 22:19–58

    Article  CAS  Google Scholar 

  • Hrdy SB (1977) Infanticide as a primate reproductive strategy. Am Sci 65:40–49

    PubMed  CAS  Google Scholar 

  • Insel TR (2010) The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65:768–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Insel TR, Harbaugh CR (1989) Lesions of the hypothalamic paraventricular nucleus disrupt the initiation of maternal behavior. Physiol Behav 45:1033–1041

    Article  CAS  PubMed  Google Scholar 

  • Insel TR, Gingrich BS, Young LJ (2001) Oxytocin: who needs it? Prog Brain Res 133:59–66

    Article  CAS  PubMed  Google Scholar 

  • Jakubowski M, Terkel J (1982) Infanticide and caretaking in non-lactating Mus musculus: influence of genotype, family group and sex. Anim Behav 30:1029–1035

    Article  Google Scholar 

  • ** D et al (2007) CD38 is critical for social behaviour by regulating oxytocin secretion. Nature 446:41–45

    Article  CAS  PubMed  Google Scholar 

  • 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 114:196–210

    Article  CAS  PubMed  Google Scholar 

  • Kennedy HF, Elwood RW (1988) Strain differences in the inhibition of infanticide in male mice (Mus musculus). Behav Neural Biol 50:349–353

    Article  CAS  PubMed  Google Scholar 

  • 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.1000412

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kirkpatrick B, Kim JW, Insel TR (1994) Limbic system fos expression associated with paternal behavior. Brain Res 658:112–118

    Article  CAS  PubMed  Google Scholar 

  • Knobloch HS, Grinevich V (2014) Evolution of oxytocin pathways in the brain of vertebrates. Front Behav Neurosci 8:31. doi:10.3389/fnbeh.2014.00031

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Krasnegor NA, Bridges RS (1990) Mammalian parenting: biochemical, neurobiological, and behavioral determinants. Oxford University Press, New York

    Google Scholar 

  • 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_25

    Article  PubMed  CAS  Google Scholar 

  • 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 36:121–131

    Article  CAS  PubMed  Google Scholar 

  • 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 1211:57–71

    Article  CAS  PubMed  Google Scholar 

  • 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.2011.02.008

    Article  PubMed  CAS  Google Scholar 

  • 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.x

    Article  PubMed  CAS  Google Scholar 

  • Leblond CP (1940) Extra-hormonal factors in maternal behavior. Proc Soc Exp Biol Med 38:66–70

    Article  Google Scholar 

  • Leblond CP, Nelson WO (1937) Maternal behavior in hypophysectomized male and female mice. Am J Physiol 120:167–172

    Google Scholar 

  • Lee AW, Brown RE (2002) Medial preoptic lesions disrupt parental behavior in both male and female California mice (Peromyscus californicus). Behav Neurosci 116:968–975

    Article  PubMed  Google Scholar 

  • Lee HJ, Caldwell HK, Macbeth AH, Tolu SG, Young WS 3rd (2008) A conditional knockout mouse line of the oxytocin receptor. Endocrinology 149:3256–3263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lein ES et al (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168–176. doi:10.1038/nature05453

    Article  PubMed  CAS  Google Scholar 

  • Leng G, Ludwig M (2016) Intranasal oxytocin: myths and delusions biol. Psychiatry 79:243–250. doi:10.1016/j.biopsych.2015.05.003

    Article  CAS  Google Scholar 

  • 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 94:117–129

    Article  CAS  PubMed  Google Scholar 

  • 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 284:330–333

    Article  CAS  PubMed  Google Scholar 

  • 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.2016.08.067

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lonstein JS, De Vries GJ (2000) Sex differences in the parental behavior of rodents. Neurosci Biobehav Rev 24:669–686

    Article  CAS  PubMed  Google Scholar 

  • Lonstein JS, Fleming AS (2002) Parental behaviors in rats and mice. Curr Protoc Neurosci Chapter 8:8.15.11–18.15.26

    Google Scholar 

  • Lonstein JS, Simmons DA, Swann JM, Stern JM (1998) Forebrain expression of c-fos due to active maternal behaviour in lactating rats. Neuroscience 82:267–281

    Article  CAS  PubMed  Google Scholar 

  • 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.2015.06.011

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, Waltham

    Google Scholar 

  • 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.x

    Article  PubMed  CAS  Google Scholar 

  • 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.x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 124:677–685

    Article  PubMed  PubMed Central  Google Scholar 

  • 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/nature14402

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McCarthy MM (1995) Estrogen modulation of oxytocin and its relation to behavior. Adv Exp Med Biol 395:235–245

    PubMed  CAS  Google Scholar 

  • McCarthy MM, vom Saal FS (1985) The influence of reproductive state on infanticide by wild female house mice (Mus musculus). Physiol Behav 35:843–849

    Article  CAS  PubMed  Google Scholar 

  • Mitre M et al (2016) A distributed network for social cognition enriched for oxytocin receptors. J Neurosci 36:2517–2535. doi:10.1523/JNEUROSCI.2409-15.2016

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Murphy MR, MacLean PD, Hamilton SC (1981) Species-typical behavior of hamsters deprived from birth of the neocortex. Science 213:459–461

    Article  CAS  PubMed  Google Scholar 

  • 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.2014.09.020

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Neumann ID (2008) Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J Neuroendocrinol 20:858–865

    Article  CAS  PubMed  Google Scholar 

  • 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.2012.08.004

    Article  PubMed  CAS  Google Scholar 

  • 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 93:11699–11704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 107–145

    Google Scholar 

  • Numan M (1974) Medial preoptic area and maternal behavior in the female rat. J Comp Physiol Psychol 87:746–759

    Article  CAS  PubMed  Google Scholar 

  • Numan M (1994) Maternal behavior. In: Knobili E, Neill JD (eds) The physiology of reproduction, 2nd edn, vol 2. Raven, New York, pp 221–302

    Google Scholar 

  • Numan M (2015) Neurobiology of social behavior: toward an understanding of prosocial and antisocial brain. Elsevier, London

    Google Scholar 

  • Numan M (2017) Parental behavior. In: Reference module in neuroscience and biobehavioral psychology. Elsevier, Amsterdam

    Google Scholar 

  • Numan M, Corodimas KP (1985) The effects of paraventricular hypothalamic lesions on maternal behavior in rats. Physiol Behav 35:417–425

    Article  CAS  PubMed  Google Scholar 

  • Numan M, Insel TR (2003) The neurobiology of parental behavior. Springer, New York

    Google Scholar 

  • Numan M, Numan MJ (1994) Expression of Fos-like immunoreactivity in the preoptic area of maternally behaving virgin and postpartum rats. Behav Neurosci 108:379–394

    Article  CAS  PubMed  Google Scholar 

  • 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.2008.10.002

    Article  PubMed  CAS  Google Scholar 

  • 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.2015.05.015

    Article  CAS  PubMed  Google Scholar 

  • Numan M, Rosenblatt JS, Komisaruk BR (1977) Medial preoptic area and onset of maternal behavior in the rat. J Comp Physiol Psychol 91:146–164

    Article  CAS  PubMed  Google Scholar 

  • 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 102:381–396

    Article  CAS  PubMed  Google Scholar 

  • 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.2016.03.033

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.2015.04.006

    Article  PubMed  CAS  Google Scholar 

  • 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.x

    Article  PubMed  CAS  Google Scholar 

  • 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/nature12330

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 31–42

    Google Scholar 

  • 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.12202

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parmigiani S, Palanza P, Rogers J, Ferrari PF (1999) Selection, evolution of behavior and animal models in behavioral neuroscience. Neurosci Biobehav Rev 23:957–969

    Article  CAS  PubMed  Google Scholar 

  • Paxinos G (2004) The rat nervous system. Elsevier, San Diego

    Google Scholar 

  • Paxinos G, Franklin KBJ (2013) The mouse brain in stereotaxic coordinates, 4th edn. Academic Press, San Diego

    Google Scholar 

  • 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 76:6661–6665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.7071605

    Article  PubMed  CAS  Google Scholar 

  • Pedersen CA, Caldwell JD, Johnson MF, Fort SA, Prange AJ Jr (1985) Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior. Neuropeptides 6:175–182

    Article  CAS  PubMed  Google Scholar 

  • 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.x

    Article  PubMed  CAS  Google Scholar 

  • 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 108:1163–1171

    Article  CAS  PubMed  Google Scholar 

  • Pedersen CA, Vadlamudi SV, Boccia ML, Amico JA (2006) Maternal behavior deficits in nulliparous oxytocin knockout mice. Genes Brain Behav 5:274–281

    Article  CAS  PubMed  Google Scholar 

  • Peterson RP (1966) Magnocellular neurosecretory centers in the rat hypothalamus. J Comp Neurol 128:181–190. doi:10.1002/cne.901280205

    Article  PubMed  CAS  Google Scholar 

  • 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.22716

    Article  PubMed  CAS  Google Scholar 

  • Priestnall R, Young S (1978) An observational study of caretaking behavior of male and female mice housed together. Dev Psychobiol 11:23–30

    Article  CAS  PubMed  Google Scholar 

  • 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 424:409–438

    Article  CAS  PubMed  Google Scholar 

  • Ragnauth AK et al (2005) Female oxytocin gene-knockout mice, in a semi-natural environment, display exaggerated aggressive behavior. Genes Brain Behav 4:229–239

    Article  CAS  PubMed  Google Scholar 

  • 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.901980106

    Article  PubMed  CAS  Google Scholar 

  • 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.1214094109

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.0098839

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.1252723

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rosenblatt JS (1967) Nonhormonal basis of maternal behavior in the rat. Science 156:1512–1514

    Article  CAS  PubMed  Google Scholar 

  • Rosenblatt JS (1969) The development of maternal responsiveness in the rat. Am J Orthopsychiatry 39:36–56

    Article  CAS  PubMed  Google Scholar 

  • Rosenblatt JS, Lehrman DS (1963) Maternal behavior of the laboratory rat. In: Rheingold HL (ed) Maternal behavior in mammals. Wiley, New York, pp 8–57

    Google Scholar 

  • Rosenblatt JS, Snowdon CT (eds) (1996) Parental care: evolution, mechanism, and adaptive significance, Advances in the study of behavior, vol 25. Academic Press, San Diego

    Google Scholar 

  • Rossant J, McMahon A (1999) Creating mouse mutants-a meeting review on conditional mouse genetics. Genes Dev 13:142–145

    Article  CAS  PubMed  Google Scholar 

  • Russell JA, Leng G (1998) Sex, parturition and motherhood without oxytocin? J Endocrinol 157:343–359. doi:10.1677/joe.0.1570343

    Article  PubMed  CAS  Google Scholar 

  • Schaller GB (1972) The Serengeti lion: a study of predator-prey relations. University of Chicago Press, Chicago

    Google Scholar 

  • 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.1594-10.2010

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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/nature15378

    Article  PubMed  CAS  Google Scholar 

  • 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.2009-1271

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shen H (2015) Neuroscience: the hard science of oxytocin. Nature 522:410–412. doi:10.1038/522410a

    Article  PubMed  CAS  Google Scholar 

  • Simerly RB (2004) Anatomical substrates of hypothalamic integration. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier, San Diego, pp 336–368

    Google Scholar 

  • 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 94:14077–14082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sofroniew MV (1985) Vasopressin- and neurophysin-immunoreactive neurons in the septal region, medial amygdala and locus coeruleus in colchicine-treated rats. Neuroscience 15:347–358

    Article  CAS  PubMed  Google Scholar 

  • 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 36:1275–1281

    Article  Google Scholar 

  • 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.x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sugiyama Y (1965) On the social change of hanuman langurs (Presbytis entellus). Primates 6:381–418

    Article  Google Scholar 

  • 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.2364-12.2013

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Takayanagi Y et al (2005) Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc Natl Acad Sci U S A 102:16096–16101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 169:369–380

    Article  CAS  PubMed  Google Scholar 

  • 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/dmk002

    Article  PubMed  CAS  Google Scholar 

  • 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 136–172

    Google Scholar 

  • 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.23251

    Article  PubMed  CAS  Google Scholar 

  • 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.201591942

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tsuneoka Y et al (under submission) Genetic targeting of oxytocin and vasopressin receptors and the pup-directed behaviors in mice

    Google Scholar 

  • 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.0.1120275

    Article  CAS  Google Scholar 

  • 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.1201043

    Article  PubMed  CAS  Google Scholar 

  • vom Saal FS (1985) Time-contingent change in infanticide and parental behavior induced by ejaculation in male mice. Physiol Behav 34:7–15

    Article  Google Scholar 

  • vom Saal FS, Howard LS (1982) The regulation of infanticide and parental behavior: implications for reproductive success in male mice. Science 215:1270–1272

    Article  Google Scholar 

  • 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 3129–3190

    Chapter  Google Scholar 

  • Wamboldt MZ, Insel TR (1987) The ability of oxytocin to induce short latency maternal behavior is dependent on peripheral anosmia. Behav Neurosci 101:439–441

    Article  CAS  PubMed  Google Scholar 

  • Wiesner BP, Sheard NM (1933) Maternal behaviour in the rat. Oliver and Boyd, London

    Google Scholar 

  • 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 37:145–155

    Article  CAS  PubMed  Google Scholar 

  • 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 114:183–192

    Article  CAS  PubMed  Google Scholar 

  • 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/nature13307

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoshida M, Takayanagi Y, Inoue K, Kimura T, Young LJ, Onaka T, Nishimori K (2009) Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice. J Neurosci 29:2259–2271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young WS 3rd et al (1996) Deficiency in mouse oxytocin prevents milk ejection, but not fertility or parturition. J Neuroendocrinol 8:847–853

    Article  CAS  PubMed  Google Scholar 

  • 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.23190

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.3634

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

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: oyako@brain.riken.jp.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Michael Numan or Kumi O. Kuroda .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Yoshihara, C., Numan, M., Kuroda, K.O. (2017). Oxytocin and Parental Behaviors. In: Hurlemann, R., Grinevich, V. (eds) Behavioral Pharmacology of Neuropeptides: Oxytocin. Current Topics in Behavioral Neurosciences, vol 35. Springer, Cham. https://doi.org/10.1007/7854_2017_11

Download citation

Publish with us

Policies and ethics

Navigation