Skip to main content
SpringerLink
Log in

Natural variation in paternal behavior is associated with central estrogen receptor alpha and oxytocin levels

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

In monogamous mammals paternal care plays an important role in the neural and behavioral development of offspring. However, the neuroendocrine mechanisms underlying paternal behavior remain poorly understood. Here, we investigate the association between natural variation in paternal responsiveness and central levels of oxytocin (OT) and estrogen receptor alpha (ERα). We used the frequency of licking and grooming behavior to distinguish low paternal responsiveness and high paternal responsiveness in virgin mandarin voles (Microtus mandarinus). Males that engaged in high paternal behavior had elevated levels of OT immunoreactive neurons in the paraventricular nuclei of the hypothalamus and supraoptic nuclei of the hypothalamus compared with males that displayed low paternal behavior. Likewise, males of high paternal responsiveness had more ERα immunoreactive neurons in the medial preoptic area, bed nucleus of the stria terminalis, arcuate nucleus of the hypothalamus and medial amygdaloid nucleus compared to low responsive males. The level of ERα immunoreactive neurons in the ventromedial hypothalamic nucleus was lower in highly paternal males compared to less paternal males. These results suggest that natural variation in paternal responsiveness may be directly related to variation in central OT and ERα.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ARC:

Arcuate nucleus of the hypothalamus

BNST:

Bed nucleus of the stria terminalis

ERα:

Estrogen receptor alpha

ERα-IRs:

Estrogen receptor alpha immunoreactive neurons

MeA:

Medial amygdaloid nucleus

MPOA:

Medial preoptic area

mRNA:

Mitochondrial RNA

OT:

Oxytocin

OT-IRs:

Oxytocin immunoreactive neurons

PVN:

Paraventricular nuclei of the hypothalamus

SON:

Supraoptic nuclei of the hypothalamus

VMH:

Ventromedial hypothalamic nucleus

References

  • Ahern TH, Young LJ (2009) The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (M. ochrogaster). Front Behav Neurosci 3:17

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bales KL, Kramer KM, Lewis-Reese AD, Carter CS (2006) Effects of stress on parental care are sexually dimorphic in prairie voles. Physiol Behav 87:424–429

    Article  CAS  PubMed  Google Scholar 

  • Bealer SL, Lipschitz DL, Ramoz G, Crowley WR (2006) Oxytocin receptor binding in the hypothalamus during gestation in rats. Am J Physiol Regul Integr Comp Physiol 291:R53–R58

    Article  CAS  PubMed  Google Scholar 

  • Betty M, Bemis WE, Francoise V (2014) Parental behaviour of prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus) in relation to sex of offspring. Behav 151:535–553

    Article  Google Scholar 

  • Bosch OJ, Neumann ID (2008) Maternal stress adaptations peripartum: mom’s innate anxiety determines maternal care and aggression. In: Bridges RS (ed) Neurobiology of the parental brain. Academic Press, San Diego, pp 115–130

    Google Scholar 

  • Bosch Oliver J, Neumann Inga D (2012) Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: From central release to sites of action. Horm Behav 61:293–303

    Article  CAS  PubMed  Google Scholar 

  • Bosch OJ, Meddle SL, Beiderbeck DI, Douglas AJ, Neumann ID (2005) Brain oxytocin correlates with maternal aggression: link to anxiety. J Neurosci 25:6807–6815

    Article  CAS  PubMed  Google Scholar 

  • Bosch OJ, Pfortsch J, Beiderbeck DI, Landgraf R, Neumann ID (2010) Maternal behavior is associated with vasopressin release in the medial preoptic area and bed nucleus of the stria terminalis in the rat. J Neuroendocrinol 22:420–429

    Article  CAS  PubMed  Google Scholar 

  • Bredy TW, Lee AW, Meaney MJ, Brown RE (2004) Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse. Horm Behav 46:30–38

    Article  PubMed  Google Scholar 

  • Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, Meaney MJ (1998) Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad of Sci USA 95:5335–5340

    Article  CAS  Google Scholar 

  • Caldwell JD, Brooks PJ, Jirikowski GF, Barakat AS, Lund PK, Pedersen CA (1989) Estrogen alters oxytocin mRNA levels in the preoptic area. J Neuroendocrinol 1:273–278

    Article  CAS  PubMed  Google Scholar 

  • Carter CS, Keverne EB (2002) The neurobiology of social affiliation and pair bonding. In: Pfaff D (ed) Hormones, brain, and behavior, vol.1. Academic Press, San Diego, pp 299–337

    Chapter  Google Scholar 

  • Carter CS, Roberts RL (1997) The psychobiological basis of cooperative breeding in rodents. In: Solomon NG, French JA (eds) Cooperative Breeding in Mammals. Cambridge University Press, New York, pp 231–266

    Google Scholar 

  • Champagne FA, Francis DD, Mar A, Meaney MJ (2003) Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79:359–371

    Article  CAS  PubMed  Google Scholar 

  • Champagne FA, Weaver IC, Diorio J, Sharma S, Meaney MJ (2008) Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the medial preoptic area. Endocrinol 144:4720–4724

    Article  Google Scholar 

  • Cho MM, DeVries AC, Williams JR, Carter CS (1999) The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav Neurosci 113:1071–1079

    Article  CAS  PubMed  Google Scholar 

  • Cushing BS, Perry A, Musatov S, Ogawa S, Papademetriou E (2008) Estrogen receptors in the medial amygdala inhibit the expression of male prosocial behavior. J Neurosci 28:10399–10403

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • De Vries GJ, Villalba C (1997) Brain sexual dimorphism and sex differences in parental and other social behaviors. Ann NY Acad Sci 807:273–286

    Article  PubMed  Google Scholar 

  • Elwood RW, Broom DM (1978) The influence of litter size and parental behavior on the development of Mongolian gerbil pups. Anim Behav 26:438–454

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Francis DD, Young LJ, Meaney MJ, Insel TR (2002) Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J Neuroendocrinol 14:349–353

    Article  CAS  PubMed  Google Scholar 

  • Frazier CR, Trainor BC, Cravens CJ, Whitney TK, Marler CA (2006) Paternal behavior influences development of aggression and vasopressin expression in male California mouse offspring. Horm Behav 50:699–707

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez A, Lovic V, Ward GR, Wainwright PE, Fleming AS (2001) Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats. Dev Psychobiol 38:11–32

    Article  CAS  PubMed  Google Scholar 

  • Gray P, Brooks PJ (1984) Effect of lesion location within the medial– preoptic–anterior hypothalamic continuum on maternal and male sexual behaviors in female rats. Behav Neurosci 98:703–711

    Article  CAS  PubMed  Google Scholar 

  • Hatton Glenn I, Yupeng Wang (2008) Neural mechanisms underlying the milk ejection burst and reflex. Prog Brain Res 170:155–166

    Article  CAS  PubMed  Google Scholar 

  • Insel T, Harbaugh CR (1989) Lesions of the hypothalamic paraventricular nucleus disrupt the initiation of maternal behavior. Physiol Behav 45(5):1033–1041

    Article  CAS  PubMed  Google Scholar 

  • Jacobson CD, Terkel J, Gorski RA, Sawyer CH (1980) Effects of small medial preoptic area lesions on maternal behavior: retrieving and nest building in the rat. Brain Res 194:471–478

    Article  CAS  PubMed  Google Scholar 

  • Jia R, Tai FD, An SC, Zhang X, Broders H (2009) Effects of neonatal paternal deprivation or early deprivation on anxiety and social behaviors of the adults in mandarin voles. Behav Process 82:271–278

    Article  Google Scholar 

  • Jia R, Tai FD, An SC, Zhang X (2011) Neonatal paternal deprivation or early deprivation reduces adult parental behavior and central estrogen receptor α expression in mandarin voles(Microtus mandarinus). Behav Brain Res 224:279–289

    Article  CAS  PubMed  Google Scholar 

  • Johnson AE (1992) The regulation of oxytocin receptor binding in the ventromedial hypothalamic nucleus by gonadal steroids. Ann NY Acad Sci 652:357–373

    Article  CAS  PubMed  Google Scholar 

  • Kenkel WM, Paredes J, Yee JR, Pournajafi-Nazarloo H, Bales KL, Carter CS (2012) Neuroendocrine and behavioural responses to exposure to an infant in male prairie voles. J Neuroendocrinol 24(6):874–876

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Kramer KM, Carr MS, Schmidt JV, Cushing BS (2006) Parental regulation of central patterns of estrogen receptor alpha. Neurosci 142:165–173

    Article  CAS  Google Scholar 

  • Lei K, Cushing BS, Musatov S, Ogawa S, Kramer KM (2010) Estrogen receptor-alpha in the bed nucleus of the stria terminalis regulates social affiliation in male prairie voles (Microtus ochrogaster). PLoS One 5:e8931

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A (1997) Maternal care, hippocampal glucocorticoid receptors and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659–1662

    Article  CAS  Google Scholar 

  • Liu D, Caldji C, Sharma S, Plotsky PM, Meaney MJ (2000) Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus. J Neuroendocrinol 12:5–12

    Article  PubMed  Google Scholar 

  • Lonstein JS (2007) Regulation of anxiety during the postpartum period. Front Neuroendocrinol 28(2–3):115–141

    Article  PubMed  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 

  • Manning M, Kruszynski M, Bankowski K, Olma A, Lammek B, Cheng LL, Klis WA, Seto J, Haldar J, Sawyer WH (1989) Solid-phase synthesis of 16 potent (selective and nonselective) in vivo antagonists of oxytocin. J Med Chem 32:382–391

    Article  CAS  PubMed  Google Scholar 

  • Marler CA, Bester-Meredith JK, Trainor BC (2003) Paternal behavior and aggression: endocrine mechanisms and nongenomic transmission of behavior. Adv Study Behav 32:263–323

    Article  Google Scholar 

  • Meddle SL, Bishop VR, Gkoumassi E, van Leeuwen FW, Douglas AJ (2007) Dynamic changes in oxytocin receptor expression and activation at parturition in the rat brain. Endocrinol 148:5095–5104

    Article  CAS  Google Scholar 

  • Moos F, Poulain DA, Rodriguez F, Guerne Y, Vincent JD, Richard P (1989) Release of oxytocin within the supraoptic nucleus during the milk ejection reflex in rats. Exp Brain Res 76:593–602

    Article  CAS  PubMed  Google Scholar 

  • Neumann I, Ludwig M, Engelmann M, Pittman QJ, Landgraf R (1993a) Simultaneous microdialysis in blood and brain–Oxytocin and vasopressin release in response to central and peripheral osmotic stimulation and suckling in the rat. Neuroendocrinol 58:637–645

    Article  CAS  Google Scholar 

  • Neumann I, Russell JA, Landgraf R (1993b) Oxytocin and vasopressin release within the supraoptic and paraventricular nuclei of pregnant, parturient and lactating rats–A microdialysis study. Neurosci 53:65–75

    Article  CAS  Google Scholar 

  • Neumann B, Kubicka P, Barlow DP (1995) Characteristics of imprinted genes. Nature Genet 9:12–13

    Article  CAS  PubMed  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 (2007) Motivational systems and the neural circuitry of maternal behavior in the rat. Dev Psychobiol 49:12–21

    Article  CAS  PubMed  Google Scholar 

  • Numan M, Corodimas KP (1985) The effects of paraventricular hypothalamic lesions on maternal behavior in rats. Physiol Behav 35(3):417–425

    Article  CAS  PubMed  Google Scholar 

  • Numan M, Insel TR (2003) The neurobiology of parental behavior. Springer, New York, pp 1–22

  • Numan M, Numan MJ (1995) The importance of pup-related sensory inputs and maternal performance for the expression of Fos-like immunoreactivity in the preoptic area and ventral bed nucleus of the stria terminalis of postpartum rats. Behav Neurosci 109:135–149

    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

    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 M, 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 

  • Ogawa S, Washburn T, Taylor J, Lebahn DB, Korach KS, Pfaff DW (1998) Modifications of testosterone—dependent behaviors by estrogen receptor-a gene disruption in male mice. Endocrinol 139:5058–5068

    CAS  Google Scholar 

  • Olazabal DE, Young LJ (2006a) Oxytocin receptors in the nucleus accumbens facilitate spontaneous maternal behavior in adult female prairie voles. Neurosci 141(2):559–568

    Article  CAS  Google Scholar 

  • Olazabal DE, Young LJ (2006b) Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum. Horm Behav 49(5):681–687

    Article  CAS  PubMed  Google Scholar 

  • Ovtscharoff WJr, Helmeke C, Braun C (2006) Lack of paternal care affects synaptic development in the anterior cingulate cortex. Brain Res 16:58–63

    Article  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  CAS  PubMed  Google Scholar 

  • Pedersen CA, Boccia ML (2003) Oxytocin antagonism alters rat dams’ oral grooming and upright posturing over pups. Physiol Behav 80:233–241

    Article  CAS  PubMed  Google Scholar 

  • Pfaff DW, Schwartz-Giblin S, McCarthy MM, Kow LM (1994) Cellular and molecular mechanisms of female reproductive behaviors. In: Knobil E, Neill JD (eds) The physiology of reproduction, vol 2. Raven Press, New York, pp 107–220

    Google Scholar 

  • Piovanotti MR, Vieira ML (2004) Presence of the father and parental experience have differentiated effects on pup development in Mongolian gerbils (Meriones unguiculatus). Behav Process 66:107–117

    Article  Google Scholar 

  • Richards S, Mychasiuk R, Kolb B, Gibb R (2012) Tactile stimulation during development alters behaviour and neuroanatomical organization of normal rats. Behav Brain Res 231:86–91

    Article  CAS  PubMed  Google Scholar 

  • Roberts RL, Williams JR, Wang AK, Carter CS (1998) Cooperative breeding and monogamy in prairie voles: influence of the sire and geographical variation. Anim Behav 55:1131–1140

    Article  PubMed  Google Scholar 

  • Rosenblatt JS, Ceus K (1998) Estrogen implants in the medial preoptic area stimulate maternal behavior in male rats. Horm Behav 33:23–30

    Article  CAS  PubMed  Google Scholar 

  • Rosenblatt JS, Wagner CK, Morrell JI (1994) Hormonal priming and triggering of maternal behavior in the rat with special reference to the relations between estrogen receptor binding and ER mRNA in specific brain regions. Psychoneuroendocrinol 19:543–552

    Article  CAS  Google Scholar 

  • Rosenblatt JS, Hazelwood S, Poole J (1996) Maternal behavior in male rats: effects of medial preoptic area lesions and presence of maternal aggression. Horm Behav 30:201–215

    Article  CAS  PubMed  Google Scholar 

  • Saito A, Nakamura K (2011) Oxytocin changes primate paternal tolerance to offspring in food transfer. J Com Physiol 197:329–337

    Article  CAS  Google Scholar 

  • Song ZZ, Tai FD, Yu CJ, Wu RY, Zhang X, Broders H, He FQ, Guo R (2010) Sexual or paternal experiences alter alloparental behavior and the central expression of ERα and OT in male mandarin voles (Microtus mandarinus). Behav Brain Res 214:290–300

    Article  CAS  PubMed  Google Scholar 

  • Stern JM, Johnson SK (1990) Ventral somatosensory determinants of nursing behavior in Norway rats: I. effects of variations in the quality and quantity of pup stimuli. Physiol Behav 47:993–1011

    Article  CAS  PubMed  Google Scholar 

  • Tai FD, Wang TZ (2001) Social organization of mandarin voles in burrow system. Acta Theriol Sinica 21:50–56

    Google Scholar 

  • Tai FD, Wang TZ, Zhao YJ (2001) Mating system of mandarin vole (Microtus mandarinus). Acta Zoologica Sinica 47:260–267

    Google Scholar 

  • Trainor BC, Marler CA (2002) Testosterone promotes paternal behaviour in a monogamous mammal via conversion to oestrogen. Process Biol Sci 269:823–829

    Article  CAS  Google Scholar 

  • Trainor BC, Greiwe KM, Nelson RJ (2006) Individual differences in estrogen receptor alpha in select brain nuclei are associated with individual differences in aggression. Horm Behav 50:338–345

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • van Leengoed E, Kerker E, Swanson HH (1987) Inhibition of post-partum maternal behaviour in the rat by injecting an oxytocin antagonist into the cerebral ventricles. J Endocrinol 112(2):275–282

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, De Vries GJ (1993) Testosterone effects on paternal behavior and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster). Brain Res 631:156–160

    Article  CAS  PubMed  Google Scholar 

  • Wang ZX, Novak MA (1992) Influence of the social environment on parental behavior and pup development of meadow voles (Microtus pennsylvanicus) and prairie voles (Microtus ochrogaster). J Com Psychol 106:163–171

    Article  Google Scholar 

  • Wang JL, Ma YP, Yan XF (2011) Effects of litter size and presence of the father on body weight development in mandarin vole (Microtus madarinus) offspring. Sichuan J Zool 30:377–381

    Google Scholar 

  • Wei B, Tai FD, Liu X, Ma LG, Yang XP, Jia R, Zhang X (2013) Neonatal tactile stimulation alleviates the negative effects of neonatal isolation on novel object recognition, sociability and neuroendocrine levels inmale adultmandarin voles (Microtus mandarinus). Physiol Behav 112–113:14–22

    Article  CAS  PubMed  Google Scholar 

  • Witt DM (1997) Regulatory mechanisms of oxytocin-mediated sociosexual behavior. Ann NY Acad Sci 807:287–301

    Article  CAS  PubMed  Google Scholar 

  • Witt DM, Carter CS, Walton DM (1990) Central and peripheral effects of oxytocin administration in prairie voles (Microtus ochrogaster). Pharmacol Biochem Behav 37:63–69

    Article  CAS  PubMed  Google Scholar 

  • Witt DM, Winslow JT, Insel TR (1992) Enhanced social interactions in rats following chronic, centrally infused oxytocin. Pharmacol Biochem Behav 43:855–861

    Article  CAS  PubMed  Google Scholar 

  • Wu RY, Song ZZ, Tai FD, An XL, Yu P, Li YN (2013) The effect of alloparental experience and care on anxiety-like, social and parental behaviour in adult mandarin voles. Anim Behav 85:61–69

    Article  Google Scholar 

  • Yu P, An SC, Tai FD, Zhang X, He FQ, Wang JL, An XL, Wu RY (2012) The effects of neonatal paternal deprivation on pair bonding, NAcc dopamine receptor mRNA expression and serum corticosterone in mandarin voles. Horm Behav 61:669–677

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Ruiyong Wu, Ping Hao and Xufeng Qiao for assistance with the experiment and care for voles. This research was supported by the National Natural Science Foundation of China (31372213 and 31170377) and Fundamental Research Funds for Central University (GK201305009). All procedures were in accordance with the Guide for the Care and Use of Laboratory Animals of China and were reviewed by the Institutional Animal Care and Use Committee at Shaanxi Normal University.

Author information

Authors and Affiliations

  1. Institute of Brain and Behavioral Sciences, College of Life Sciences, Shaanxi Normal University, Xi’an, Shaanxi, 710062, China

    Yani Li, Zhenmin Lian, Bo Wang, Fadao Tai, Ruiyong Wu, Ping Hao & Xufeng Qiao

  2. College of Energy and Environmental engineering, Yan’an University, Yan’an, Shaanxi, 716000, China

    Yani Li

  3. College of Biological Technology, Xi’an University, Xi’an, Shaanxi, 710062, China

    Bo Wang

Authors
  1. Yani Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhenmin Lian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bo Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fadao Tai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ruiyong Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ping Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xufeng Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zhenmin Lian or Fadao Tai.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Lian, Z., Wang, B. et al. Natural variation in paternal behavior is associated with central estrogen receptor alpha and oxytocin levels. J Comp Physiol A 201, 285–293 (2015). https://doi.org/10.1007/s00359-015-0979-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-015-0979-6

Keywords

Search

Navigation