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Oxytocin changes primate paternal tolerance to offspring in food transfer

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Abstract

Oxytocin facilitates social recognition in rats and mice, onset of maternal behavior in virgin mice and formation of pair bonds without copulation in prairie voles. However, the relationship between this peptide and paternal behavior in primates remains largely unknown. We investigated whether oxytocin affects paternal behavior in common marmosets. In these primates, fathers as well as mothers take care of their infants, and transferring food to the infants is one of their more obvious caretaking behaviors. We tested whether oxytocin and an oxytocin receptor antagonist affect the transfer of food to offspirng by fathers. After intracerebroventricular infusion of the vehicle, oxytocin, or the oxytocin receptor antagonist, the fathers’ behavior, including picking up food, transferring food to the offspring, and refusing to transfer food to the offspring, was analyzed. Compared with the vehicle, oxytocin reduced the frequency of refusal. This was not caused by reduction of appetite. Although the oxytocin receptor antagonist did not change the frequency of refusal behavior of the fathers statistically significant manner, these observations suggest that the tolerance of the adult male marmoset toward its offspring as shown by the transfer of food is increased by oxytocin administered into the central nervous system.

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References

  • Arletti R, Benelli A, Bertolini A (1989) Influence of oxytocin on feeding behavior in the rat. Peptides 10:89–93

    Article  PubMed  CAS  Google Scholar 

  • Bakermans-Kranenburg MJ, van Ijzendoorn MH (2008) Oxytocin receptor (oxtr) and serotonin transporter (5-htt) genes associated with observed parenting. Soc Cogn Affect Neurosci 3:128–134

    Article  PubMed  Google Scholar 

  • Bales KL, Kim AJ, Lewis-Reese AD, Sue Carter C (2004) Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles. Horm Behav 45:354–361

    Article  PubMed  CAS  Google Scholar 

  • Baumgartner T, Heinrichs M, Vonlanthen A, Fischbacher U, Fehr E (2008) Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58:639–650

    Article  PubMed  CAS  Google Scholar 

  • Boccia ML, Panicker AK, Pedersen C, Petrusz P (2001) Oxytocin receptors in non-human primate brain visualized with monoclonal antibody. Neuroreport 12:1723–1726

    Article  PubMed  CAS  Google Scholar 

  • Boccia ML, Goursaud AP, Bachevalier J, Anderson KD, Pedersen CA (2007) Peripherally administered non-peptide oxytocin antagonist, l368, 899((r)), accumulates in limbic brain areas: a new pharmacological tool for the study of social motivation in non-human primates. Horm Behav 52:344–351

    Article  PubMed  CAS  Google Scholar 

  • Brown H, Prescott R (1999) Applied mixed models in medicine. Wiley, Chichester

    Google Scholar 

  • Brown GR, Almond REA, van Bergen Y (2004) Begging, stealing and offering: food transfer in non-human primates. Adv Study Behav 34:265–295

    Article  Google Scholar 

  • Brown GR, Almond RE, Bates NJ (2005) Adult–infant food transfer in common marmosets: an experimental study. Am J Primatol 65:301–312

    Article  PubMed  Google Scholar 

  • Burkart JM, van Shaik CP (2010) Cognitive consequences of cooperative breeding in primates? Anim Cognit 13:1–19

    Article  Google Scholar 

  • Burkart JM, Fehr E, Efferson C, van Schaik CP (2007) Other-regarding preferences in a non-human primate: common marmosets provision food altruistically. Proc Natl Acad Sci USA 104:19762–19766

    Article  PubMed  CAS  Google Scholar 

  • Dixson AF, George L (1982) Prolactin and parental behaviour in a male new world primate. Nature 299:551–553

    Article  PubMed  CAS  Google Scholar 

  • Domes G, Heinrichs M, Michel A, Berger C, Herpertz SC (2007) Oxytocin improves “mind-reading” in humans. Biol Psychiatry 61:731–733

    Article  PubMed  CAS  Google Scholar 

  • Engelmann M, Ebner K, Wotjak CT, Landgraf R (1998) Endogenous oxytocin is involved in short-term olfactory memory in female rats. Behav Brain Res 90:89–94

    Article  PubMed  CAS  Google Scholar 

  • Epple G (1968) Comparative studies on vocalization in marmoset monkeys (hapalidae). Folia Primatol 8:1–40

    Article  PubMed  CAS  Google Scholar 

  • Feistner AT, Price EC (1990) Food-sharing in cotton-top tamarins (Saguinus oedipus). Folia Primatol (Basel) 54:34–45

    Article  CAS  Google Scholar 

  • Feistner AT, Price EC (2000) Food sharing in black lion tamarins (Leontopithecus chrysopygus). Am J Primatol 52:47–54

    Article  PubMed  CAS  Google Scholar 

  • Feldman R, Weller A, Zagoory-Sharon O, Levine A (2007) Evidence for a neuroendocrinological foundation of human affiliation: plasma oxytocin levels across pregnancy and the postpartum period predict mother–infant bonding. Psychol Sci 18:965–970

    Article  PubMed  Google Scholar 

  • Feldman R, Gordon I, Schneiderman I, Weisman O, Zgoory-Sharon O (2010) Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent–infant contact. Psychoneuroendocrinology 35:1133–1141

    Article  PubMed  CAS  Google Scholar 

  • Ferguson JN, Young LJ, Hearn EF, Matzuk MM, Insel TR, Winslow JT (2000) Social amnesia in mice lacking the oxytocin gene. Nat Genet 25:284–288

    Article  PubMed  CAS  Google Scholar 

  • Guastella AJ, Mitchell PB, Mathews F (2008) Oxytocin enhances the encoding of positive social memories in humans. Biol Psychiatry 64:256–258

    Article  PubMed  CAS  Google Scholar 

  • Heinrichs M, von Dawans B, Domes G (2009) Oxytocin, vasopressin, and human social behavior. Front Neuroendocrinol 30:548–557

    Article  PubMed  CAS  Google Scholar 

  • Holman SD, Goy RW (1995) Experiential and hormonal correlates of care-giving in rhesus macaques. In: Pryce CR, Martin RD, Skuse D (eds) Motherhood in human and nonhuman primates. Karger, Basel, pp 87–93

    Google Scholar 

  • Hrdy SB (2005) Evolutionary context of human development: the cooperative breeding model. In: Carter CS, Ahnert L, Grossmann KE, Hrdy SB, Lamb ME, Porges SW, Sachser N (eds) Attachment and bonding: a new synthesis, from the 92nd Dahlem workshop report. MIT Press, Cambridge, pp 9–32

    Google Scholar 

  • Ingram JC (1977) Interactions between parents and infants, and the development of independence in the common marmosets (Callithrix jacchus). Anim Behav 25:811–827

    Article  Google Scholar 

  • Insel TR, Hulihan TJ (1995) A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behav Neurosci 109:782–789

    Article  PubMed  CAS  Google Scholar 

  • Joyce SM, Snowdon CT (2007) Developmental changes in food transfers in cotton-top tamarins (Saguinus oedipus). Am J Primatol 69:955–965

    Article  PubMed  Google Scholar 

  • Kasper C, Voelkl B, Huber L (2008) Tolerated mouth-to-mouth food transfers in common marmosets. Primates 49:153–156

    Article  PubMed  Google Scholar 

  • Kosfeld M, Heinrichs M, Zak PL, Fischbacher U, Fehr E (2005) Oxytocin increases trust in humans. Nature 435:673–676

    Article  PubMed  CAS  Google Scholar 

  • Kozorovitskiy Y, Hughes M, Lee K, Gould E (2006) Fatherhood affects dendritic spines and vasopressin V1a receptors in the primate prefrontal cortex. Nat Neurosci 9:1094–1095

    Article  PubMed  CAS  Google Scholar 

  • Mills DA, Windle CP, Baker HF, Ridley RM (2004) Analysis of infant carrying in large, well-established family groups of captive marmosets (Callithrix jacchus). Primates 45:259–265

    Article  PubMed  Google Scholar 

  • Mota MT, Sousa MB (2000) Prolactin levels of fathers and helpers related to alloparental care in common marmosets, Callithrix jacchus. Folia Primatol (Basel) 71:22–26

    Article  CAS  Google Scholar 

  • Mota MTD, Franci CR, de Sousa MB (2006) Hormonal changes related to paternal and alloparental care in common marmosets (Callithrix jacchus). Horm Behav 49:293–302

    Article  CAS  Google Scholar 

  • Nunes S, Fite JE, French JA (2000) Variation in steroid hormones associated with infant care behaviour and experience in male marmosets (Callithrix kuhlii). Anim Behav 60:857–865

    Article  PubMed  Google Scholar 

  • Nunes S, Fite JE, Patera KJ, French JA (2001) Interactions among paternal behavior, steroid hormones, and parental experience in male marmosets (Callithrix kuhlii). Horm Behav 39:70–82

    Article  PubMed  CAS  Google Scholar 

  • 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 115:1341–1348

    Article  PubMed  CAS  Google Scholar 

  • Pedersen CA, Prange AJ Jr (1979) Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci USA 76:6661–6665

    Article  PubMed  CAS  Google Scholar 

  • Pedersen CA, Ascher JA, Monroe YL, Prange AJ Jr (1982) Oxytocin induces maternal behavior in virgin female rats. Science 216:648–650

    Article  PubMed  CAS  Google Scholar 

  • Petrovic P, Kalisch R, Singer T, Dolan RJ (2008) Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity. J Neurosci 28:6607–6615

    Article  PubMed  CAS  Google Scholar 

  • Price EC, Feistner ATC (2001) Food sharing in pied bare-faced tamarins (Saguinus bicolor bicolor): development and individual differences. Int J Primatol 22:231–241

    Article  Google Scholar 

  • Rimmele U, Hediger K, Heinrichs M, Klaver P (2009) Oxytocin makes a face in memory familiar. J Neurosci 29:38–42

    Article  PubMed  CAS  Google Scholar 

  • Rothe H, Darms K, Koenig A, Radespiel U, Juenemann B (1993) Long-term study of infant-carrying behavior in captive common marmosets (Callithrix jacchus): effect of nonreproductive helpers on the parents’ carrying performance. Int J Primatol 14:79–93

    Article  Google Scholar 

  • Saito A, Izumi A, Nakamura K (2008) Food transfer in common marmosets: parents change their tolerance depending on the age of offspring. Am J Primatol 70:999–1002

    Article  PubMed  Google Scholar 

  • Schradin C, Reeder DM, Mendoza SP, Anzenberger G (2003) Prolactin and paternal care: comparison of three species of monogamous new world monkeys (Callicebus cupreus, Callithrix jacchus, and Callimico goeldii). J Comp Psychol 117:166–175

    Article  PubMed  Google Scholar 

  • Smith AS, Agmo A, Birnie AK, French JA (2010) Manipulation of the oxytocin system alters social behavior and attraction in pair-bonding primates, Callithrix penicillata. Horm Behav 57:255–262

    Article  PubMed  CAS  Google Scholar 

  • Theodoridou A, Rowe AC, Penton-Voak IS, Rogers PJ (2009) Oxytocin and social perception: oxytocin increases perceived facial trustworthiness and attractiveness. Horm Behav 56:128–132

    Article  PubMed  CAS  Google Scholar 

  • Toloczko DM, Young L, Insel TR (1997) Are there oxytocin receptors in the primate brain? Ann NY Acad Sci 807:506–509

    Article  PubMed  CAS  Google Scholar 

  • van Schaik CP, Paul A (1996) Male care in primates: does it ever reflect paternity? Evolutionary anthropology. Issues News Rev 5:152–156

    Google Scholar 

  • Voelkl B, Huber L (2000) True imitation in marmosets. Anim Behav 60:195–202

    Article  PubMed  Google Scholar 

  • Voelkl B, Huber L (2007) Imitation as faithful copying of a novel technique in marmoset monkeys. PLoS ONE 2:e611

    Article  PubMed  Google Scholar 

  • Wang Z, Ferris CF, De Vries GJ (1994) Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). Proc Natl Acad Sci USA 91:400–404

    Article  PubMed  CAS  Google Scholar 

  • Washabaugh K, Snowdon CT, Ziegler TE (2002) Variations in care for cottontop tamarin, Saguinus oedipus, infants as a function of parental experience and group size. Anim Behav 63:1163–1174

    Article  Google Scholar 

  • Whiten PL (1987) Infants and adult males. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. The University of Chicago Press, Chicago, pp 343–357

    Google Scholar 

  • Williams JR, Insel TR, Harbaugh CR, Carter CS (1994) Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J Neuroendocrinol 6:247–250

    Article  PubMed  CAS  Google Scholar 

  • Winslow JT, Insel TR (1991) Social-status in pairs of male squirrel-monkeys determines the behavioral-response to central oxytocin administration. J Neurosci 11:2032–2038

    PubMed  CAS  Google Scholar 

  • Wright JW, Morseth SL, Abhold RH, Harding JW (1985) Pressor action and dipsogenicity induced by angiotensin II and III in rats. Am J Physiol 249:R514–R521

    PubMed  CAS  Google Scholar 

  • Yamamoto ME (1993) From dependence to sexual maturity: the behavioural ontogeny of Callitrichidae. In: Rylands AB (ed) Marmosets and tamarins: systematics, behavior, and ecology. Oxford University Press, Oxford, pp 235–254

    Google Scholar 

  • Young LJ, Wang Z, Insel TR (1998) Neuroendocrine bases of monogamy. Trends Neurosci 21:71–75

    Article  PubMed  CAS  Google Scholar 

  • Zak PJ, Stanton AA, Ahmadi S (2007) Oxytocin increases generosity in humans. PLoS ONE 2:e1128

    Article  PubMed  Google Scholar 

  • Ziegler TE, Jacoris S, Snowdon CT (2004) Sexual communication between breeding male and female cotton-top tamarins (Saguinus oedipus), and its relationship to infant care. Am J Primatol 64:57–69

    Article  PubMed  Google Scholar 

  • 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 56:436–443

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was performed in accordance with the ethical guidelines of the National Institute of Neuroscience, NCNP, under experimental license nos. 2005003 and 2008003 issued by the ethical committee for primate research of NCNP, and adhered to the legal requirements of Japan. This work was supported by the Japan Society for the Promotion of Science, no. 18-04743 (A.S.), CREST, the Japan Science and Technology Agency and a Research Grant (20B-10) for Nervous and Mental Disorders from the Ministry of Health, Labour and Welfare (K.N.).

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  1. Katsuki Nakamura

    Present address: Section of Cognitive Neuroscience, Department of Behavioral and Brain Sciences, Primate Research Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi, 484-8506, Japan

Authors and Affiliations

  1. Department of Cognitive and Behavioral Science, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, 153-8902, Japan

    Atsuko Saito

  2. JSPS, Tokyo, 102-8471, Japan

    Atsuko Saito

  3. National Institute of Neuroscience, NCNP, Kodaira, 187-8502, Japan

    Atsuko Saito & Katsuki Nakamura

  4. CREST, JST, Kawaguchi, 332-0012, Japan

    Katsuki Nakamura

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  1. Atsuko Saito
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Correspondence to Katsuki Nakamura.

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Saito, A., Nakamura, K. Oxytocin changes primate paternal tolerance to offspring in food transfer. J Comp Physiol A 197, 329–337 (2011). https://doi.org/10.1007/s00359-010-0617-2

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