In recent decades, human sociocultural changes have increased the numbers of fathers that are involved in direct caregiving in Western societies. This trend has led to a resurgence of interest in understanding the mechanisms and effects of paternal care. Across the animal kingdom, paternal caregiving has been found to be a highly malleable phenomenon, presenting with great variability among and within species. The emergence of paternal behaviour in a male animal has been shown to be accompanied by substantial neural plasticity and to be shaped by previous and current caregiving experiences, maternal and infant stimuli and ecological conditions. Recent research has allowed us to gain a better understanding of the neural basis of mammalian paternal care, the genomic and circuit-level mechanisms underlying paternal behaviour and the ways in which the subcortical structures that support maternal caregiving have evolved into a global network of parental care. In addition, the behavioural, neural and molecular consequences of paternal caregiving for offspring are becoming increasingly apparent. Future cross-species research on the effects of absence of the father and the transmission of paternal influences across generations may allow research on the neuroscience of fatherhood to impact society at large in a number of important ways.
Subscribe to Journal
Get full journal access for 1 year
only $22.08 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Feldman, R. The adaptive human parental brain: Implications for children’s social development. Trends Neurosci. 38, 387–399 (2015). This paper reviews all functional MRI studies of the human parental brain.
Feldman, R. The neurobiology of mammalian parenting and the biosocial context of human caregiving. Horm. Behav. 77, 3–17 (2016).
Braun, K. & Champagne, F. A. Paternal influences on offspring development: behavioural and epigenetic pathways. J. Neuroendocrinol. 26, 697–706 (2014).
Dulac, C., O’Connell, L. A. & Wu, Z. Neural control of maternal and paternal behaviors. Science 345, 765–770 (2014).
Abraham, E. et al. Father’s brain is sensitive to childcare experiences. Proc. Natl Acad. Sci. USA 111, 9792–9797 (2014). This paper describes the neural networks implicated in human fathering, their associations with father oxytocin and parenting behaviour and plasticity in cases of primary-caregiving fathering.
Bales, K. L. & Saltzman, W. Fathering in rodents: neurobiological substrates and consequences for offspring. Horm. Behav. 77, 249–259 (2016).
Gettler, L. T. Applying socioendocrinology to evolutionary models: fatherhood and physiology. Evol. Anthropol. 23, 146–160 (2014).
Rilling, J. K. & Young, L. J. The biology of mammalian parenting and its effect on offspring social development. Science 345, 771–776 (2014).
Curley, J. P., Mashoodh, R. & Champagne, F. A. Epigenetics and the origins of paternal effects. Horm. Behav. 59, 306–314 (2011).
Waxman, O. B. What it means to be a ‘good’ father in America has changed. Here’s how. TIME http://time.com/5312912/history-american-fathers/ (15 Jun 2018).
Steinbach, A. Children’s and parents’ well-being in joint physical custody: a literature review. Fam. Process https://doi.org/10.1111/famp.12372 (2018).
Lamb, M. E. The Role of the Father in Child Development (John Wiley & Sons, 2010). This edited volume summarizes human developmental and social research on fatherhood.
Abraham, E. & Feldman, R. The neurobiology of human allomaternal care; implications for fathering, coparenting, and children’s social development. Physiol. Behav. 193, 25–34 (2018).
Lamb, M. E. The Father’s Role: Cross Cultural Perspectives (Routledge, 2013).
Saltzman, W. & Ziegler, T. E. Functional significance of hormonal changes in mammalian fathers. J. Neuroendocrinol. 26, 685–696 (2014).
Gray, P. B. & Anderson, K. G. Fatherhood: Evolution and Human Paternal Behavior (Harvard Univ. Press, 2010).
Rosenbaum, S. & Gettler, L. T. With a little help from her friends (and family) part II: non-maternal caregiving behavior and physiology in mammals. Physiol. Behav. 193, 12–24 (2018).
Burkart, J. M., Van Schaik, C. & Griesser, M. Looking for unity in diversity: human cooperative childcare in comparative perspective. Proc. R. Soc. B 284, 20171184 (2017).
Swain, J. E. et al. Approaching the biology of human parental attachment: brain imaging, oxytocin and coordinated assessments of mothers and fathers. Brain Res. 1580, 78–101 (2014).
Zhong, J. et al. C-Fos expression in the paternal mouse brain induced by communicative interaction with maternal mates. Mol. Brain 7, 66 (2014).
Hofer, M. A. Early social relationships: a psychobiologist’s view. Child Dev. 58, 633–647 (1987).
Champagne, F. A. & Curley, J. P. How social experiences influence the brain. Curr. Opin. Neurobiol. 15, 704–709 (2005).
Storey, A. E. & Walsh, C. J. in Handbook of Father Involvement: Multidisciplinary Perspectives (eds Cabrera, N. J. & Tamis-LeMonda, C. S.) 3–22 (Routledge, 2013).
Lorenz, K. Der kumpan in der umwelt des vogels. J. Ornithol. 83, 289–413 (1935).
Darwin, C. On the Origin of Species by Means of Natural Selection (Murray, 1859).
Abraham, E. & Feldman, R. in International Handbook of Social Neuroendocrinology (eds Schultheiss, O. C. & Mehta, P. H.) 298–317 (Routledge, 2018).
Royle, N. J., Russell, A. F. & Wilson, A. J. The evolution of flexible parenting. Science 345, 776–781 (2014).
Westneat, D. F. & Sherman, P. W. Parentage and the evolution of parental behavior. Behav. Ecol. 4, 66–77 (1993).
Reynolds, J. D., Goodwin, N. B. & Freckleton, R. P. Evolutionary transitions in parental care and live bearing in vertebrates. Phil. Trans. R. Soc. B 357, 269–281 (2002).
Clutton-Brock, T. H. The Evolution of Parental Care (Princeton Univ. Press, 1991).
Møller, A. P. & Cuervo, J. J. The evolution of paternity and paternal care in birds. Behav. Ecol. 11, 472–485 (2000).
Fernandez-Duque, E., Valeggia, C. R. & Mendoza, S. P. The biology of paternal care in human and nonhuman primates. Annu. Rev. Anthropol. 38, 115–130 (2009).
Geary, D. C. Evolution and proximate expression of human paternal investment. Psychol. Bull. 126, 55–77 (2000). This integrative perspective discusses the evolution of paternal caregiving in mammals.
Kleiman, D. G. & Malcolm, J. R. in Parental Care in Mammals (ed. Gubernick, D. J.) 347–387 (Springer, 1981).
Kokko, H. & Jennions, M. D. Parental investment, sexual selection and sex ratios. J. Evol. Biol. 21, 919–948 (2008).
Sheldon, B. C. Relating paternity to paternal care. Phil. Trans. R. Soc. B 357, 341–350 (2002).
Emlen, S. T. An evolutionary theory of the family. Proc. Natl Acad. Sci. USA 92, 8092–8099 (1995).
Royle, N. J., Smiseth, P. T. & Kölliker, M. The Evolution of Parental Care (Oxford Univ. Press, 2012).
Dunbar, R. I. M. The mating system of callitrichid primates: I. Conditions for the coevolution of pair bonding and twinning. Anim. Behav. 50, 1057–1070 (1995).
Kokko, H. & Johnstone, R. A. Why is mutual mate choice not the norm? Operational sex ratios, sex roles and the evolution of sexually dimorphic and monomorphic signalling. Phil. Trans. R. Soc. B 357, 319–330 (2002).
Ihara, Y. A model for evolution of male parental care and female multiple mating. Am. Nat. 160, 235–244 (2002).
Lukas, D. & Clutton-Brock, T. H. The evolution of social monogamy in mammals. Science 341, 526–530 (2013). This paper traces the evolution of social monogamy and paternal caregiving in all mammalian species for which social structure is documented.
Kleiman, D. G. Monogamy in mammals. Q. Rev. Biol. 52, 39–69 (1977).
Gubernick, D. J. & Teferi, T. Adaptive significance of male parental care in a monogamous mammal. Proc. R. Soc. B 267, 147–150 (2000).
Huber, S., Millesi, E. & Dittami, J. P. Paternal effort and its relation to mating success in the European ground squirrel. Anim. Behav. 63, 157–164 (2002).
Smith, H. G. & Hardling, R. Clutch size evolution under sexual conflict enhances the stability of mating systems. Proc. R. Soc. B 267, 2163–2170 (2000).
Wright, H. W. Y. Paternal den attendance is the best predictor of offspring survival in the socially monogamous bat-eared fox. Anim. Behav. 71, 503–510 (2006).
Wright, S. L. & Brown, R. E. The importance of paternal care on pup survival and pup growth in Peromyscus californicus when required to work for food. Behav. Processes 60, 41–52 (2002).
Stockley, P. & Hobson, L. Paternal care and litter size coevolution in mammals. Proc. R. Soc. B 283, 20160140 (2016).
Hrdy, S. B. in Family Relationships: An Evolutionary Perspective (eds Salmon, C. A. & Shackelford, T. K.) 39–68 (Oxford Univ. Press, 2007).
Opie, C., Atkinson, Q. D., Dunbar, R. I. M. & Shultz, S. Male infanticide leads to social monogamy in primates. Proc. Natl Acad. Sci. USA 110, 13328–13332 (2013).
Paul, A., Preuschoft, S. & van Schaik, C. P. in Infanticide by Males and its Implications (eds van Schaick, C. P. & Janson, C. H.) 269–292 (Cambridge Univ. Press, 2000).
Wolovich, C. K., Evans, S. & French, J. A. Dads do not pay for sex but do buy the milk: food sharing and reproduction in owl monkeys (Aotus spp.). Anim. Behav. 75, 1155–1163 (2008).
Flinn, M. V. in Oxford Handbook of Evolutionary Family Psychology (eds Salmon, C. A. & Shackelford, T. K.) 12–32 (Oxford Univ. Press, 2011).
Hewlett, B. S. in Father-Child Relations: Cultural and Biosocial Contexts (ed. Hewlett, B. S.) 153–176 (Aldine de Gryte, 1992).
Meehan, C. L. in Handbook of Child Well-Being (eds Ben-Arieh, A., Casas, F., Frønes, I. & Korbin, J. E.) 1787–1816 (Springer, 2014).
McKenna, J. J. in Parenting Across the Life Span: Biosocial Dimensions (eds Lancaster, J. B., Altmann, J., Rossi, A. S., & Sherrod, L. R.) 143–184 (Aldine Publishing, 1987).
Kramer, K. L. Cooperative breeding and its significance to the demographic success of humans. Annu. Rev. Anthropol. 39, 417–436 (2010).
Geary, D. C. & Flinn, M. V. Evolution of human parental behavior and the human family. Parenting 1, 5–61 (2001).
Parker, G. & Simmons, L. W. Parental investment and the control of sexual selection: predicting the direction of sexual competition. Proc. R. Soc. B 263, 315–321 (1996).
Flinn, M. V. Correlates of reproductive success in a Caribbean village. Hum. Ecol. 14, 225–243 (1986).
Flinn, M. V. & Low, B. S. in Ecological Aspects of Social Evolution : Birds and Mammals (eds Rubenstein, D. I. & Wrangham, R. W.) 217–243 (Princeton Univ. Press, 1986).
Parker, K. & Liveingstone, G. 7 facts about American fathers. Pew Research Center http://www.pewresearch.org/fact-tank/2018/06/13/fathers-day-facts/ (13 Jun 2018).
Schober, P. S. Increasing father involvement in child care: what do we know about effects on child development? DIW Roundup https://www.econstor.eu/bitstream/10419/121162/1/836677870.pdf (29 Sep 2015).
American Psychological Association. The changing role of the modern day father. APA https://www.apa.org/pi/families/resources/changing-father.aspx (2010).
Horrell, N. D., Hickmott, P. W. & Saltzman, W. Neural regulation of paternal behavior in mammals;Sensory, neuroendocrine, and experiential influences on the paternal brain. Curr. Top. Behav. Neurosci. https://doi.org/10.1007/7854_2018_55 (2018).
Lonstein, J. S. & De Vries, G. J. Influence of gonadal hormones on the development of parental behavior in adult virgin prairie voles (Microtus ochrogaster). Behav. Brain Res. 114, 79–87 (2000).
Kim, P. et al. Neural plasticity in fathers of human infants. Soc. Neurosci. 9, 522–535 (2014). This longitudinal fMRI study shows grey matter changes in a father’s brain from the first to fourth postpartum month.
Kozorovitskiy, Y., Hughes, M., Lee, K. & Gould, E. Fatherhood affects dendritic spines and vasopressin V1a receptors in the primate prefrontal cortex. Nat. Neurosci. 9, 1094–1095 (2006). In this study, marmoset biparental fathers show greater densities of dendritic spines on pyramidal neurons in the PFC than shown by non-fathers and more vasopressin V1a receptors, indicating neural plasticity associated with paternal care.
Hyer, M. M. et al. Estrogen-dependent modifications to hippocampal plasticity in paternal California mice (peromyscus californicus). Horm. Behav. 96, 147–155 (2017).
Atzil, S., Hendler, T., Zagoory-Sharon, O., Winetraub, Y. & Feldman, R. Synchrony and specificity in the maternal and the paternal brain: relations to oxytocin and vasopressin. J. Am. Acad. Child Adolesc. Psychiatry 51, 798–811 (2012).
Lambert, K. G. et al. Characteristic neurobiological patterns differentiate paternal responsiveness in two peromyscus species. Brain. Behav. Evol. 77, 159–175 (2011).
Corona, R. et al. Exposure to young preferentially activates adult-born neurons in the main olfactory bulb of sheep mothers. Brain Struct. Funct. 222, 1219–1229 (2017).
Kim, P. et al. The plasticity of human maternal brain: Longitudinal changes in brain anatomy during the early postpartum period. Behav. Neurosci. 124, (695–700 (2010).
Storey, A. E. & Ziegler, T. E. Primate paternal care: interactions between biology and social experience. Horm. Behav. 77, 260–271 (2016). This paper reviews research on hormonal changes associated with fatherhood in rodents, non-human primates and humans.
Wu, Z., Autry, A. E., Bergan, J. F., Watabe-Uchida, M. & Dulac, C. G. Galanin neurons in the medial preoptic area govern parental behaviour. Nature 509, 325–330 (2014). This molecular study shows that a subset of galanin-expressing neurons in the MPOA specifically activates during male and female parenting and that optogenetic activation of these neurons in virgin males induces paternal behaviour.
Kohl, J. et al. Functional circuit architecture underlying parental behaviour. Nature 556, 326–331 (2018). This circuit-level study indicates that galanin-expressing neurons in the MPOA integrate inputs from several brain areas distinctly in mothers and fathers to coordinate paternal behaviour.
Bendesky, A. et al. The genetic basis of parental care evolution in monogamous mice. Nature 544, 434–439 (2017).
Hoekzema, E. et al. Pregnancy leads to long-lasting changes in human brain structure. Nat. Neurosci. 20, 287–296 (2017).
Feldman, R. The neurobiology of human attachments. Trends Cogn. Sci. 21, 80–99 (2017).
Numan, M. & Young, L. J. Neural mechanisms of mother–infant bonding and pair bonding: similarities, differences, and broader implications. Horm. Behav. 77, 98–112 (2016).
Romero-Fernandez, W., Borroto-Escuela, D. O., Agnati, L. F. & Fuxe, K. Evidence for the existence of dopamine d2-oxytocin receptor heteromers in the ventral and dorsal striatum with facilitatory receptor-receptor interactions. Mol. Psychiatry 18, 849–850 (2013).
Numan, M. & Stolzenberg, D. S. 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 (2009).
Numan, M. & Smith, H. G. Maternal behavior in rats: evidence for the involvement of preoptic projections to the ventral tegmental area. Behav. Neurosci. 98, 712–727 (1984).
Dobolyi, A., Grattan, D. R. & Stolzenberg, D. S. Preoptic inputs and mechanisms that regulate maternal responsiveness. J. Neuroendocrinol. 26, 627–640 (2014).
Shahrokh, D. K., Zhang, T.-Y., Diorio, J., Gratton, A. & Meaney, M. J. Oxytocin-dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology 151, 2276–2286 (2010).
Fang, Y.-Y., Yamaguchi, T., Song, S. C., Tritsch, N. X. & Lin, D. A. Hypothalamic midbrain pathway essential for driving maternal behaviors. Neuron 98, 192–207 (2018).
McHenry, J. A. et al. Hormonal gain control of a medial preoptic area social reward circuit. Nat. Neurosci. 20, 449–458 (2017).
Ferguson, J. N., Aldag, J. M., Insel, T. R. & Young, L. J. Oxytocin in the medial amygdala is essential for social recognition in the mouse. J. Neurosci. 21, 8278–8285 (2001).
Insel, T. R. Postpartum increases in brain oxytocin binding. Neuroendocrinology 44, 515–518 (1986).
Numan, M. et al. Medial preoptic area interactions with the nucleus accumbens-ventral pallidum circuit and maternal behavior in rats. Behav. Brain Res. 158, 53–68 (2005).
Rosenblatt, J. S., Hazelwood, S. & Poole, J. Maternal behavior in male rats: effects of medial preoptic area lesions and presence of maternal aggression. Horm. Behav. 30, 201–215 (1996).
Sturgis, J. D. & Bridges, R. S. N-Methyl-DL-aspartic acid lesions of the medial preoptic area disrupt ongoing parental behavior in male rats. Physiol. Behav. 62, 305–310 (1997).
Lee, A. W. & Brown, R. E. Medial preoptic lesions disrupt parental behavior in both male and female California mice (Peromyscus californicus). Behav. Neurosci. 116, 968–975 (2002).
de Jong, T. R., Chauke, M., Harris, B. N. & Saltzman, W. From here to paternity: Neural correlates of the onset of paternal behavior in California mice (Peromyscus californicus). Horm. Behav. 56, 220–231 (2009).
Lee, A. W. & Brown, R. E. Comparison of medial preoptic, amygdala, and nucleus accumbens lesions on parental behavior in California mice (Peromyscus californicus). Physiol. Behav. 92, 617–628 (2007).
Akther, S., Fakhrul, A. A. K. M. & Higashida, H. Effects of electrical lesions of the medial preoptic area and the ventral pallidum on mate-dependent paternal behavior in mice. Neurosci. Lett. 570, 21–24 (2014).
Kirkpatrick, B., Kim, J. W. & Insel, T. R. Limbic system fos expression associated with paternal behavior. Brain Res. 658, 112–118 (1994).
Almond, R. E. A., Ziegler, T. E. & Snowdon, C. T. Changes in prolactin and glucocorticoid levels in cotton-top tamarin fathers during their mate’s pregnancy: the effect of infants and paternal experience. Am. J. Primatol. 70, 560–565 (2008).
Rafacz, M. L., Margulis, S. U. E. & Santymire, R. M. Hormonal correlates of paternal care differences in the Hylobatidae. Am. J. Primatol. 74, 247–260 (2012).
Fleming, A. S., Corter, C., Stallings, J. & Steiner, M. Testosterone and prolactin are associated with emotional responses to infant cries in new fathers. Horm. Behav. 42, 399–413 (2002).
Wynne-Edwards, K. E. Hormonal changes in mammalian fathers. Horm. Behav. 40, 139–145 (2001).
Nunes, S., Fite, J. E., Patera, K. J. & French, J. A. Interactions among paternal behavior, steroid hormones, and parental experience in male marmosets (Callithrix kuhlii). Horm. Behav. 39, 70–82 (2001).
Schradin, C., Reeder, D. A. M., Mendoza, S. P. & Anzenberger, G. 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 (2003).
Levine, A., Zagoory-Sharon, O., Feldman, R. & Weller, A. Oxytocin during pregnancy and early postpartum: Individual patterns and maternal-fetal attachment. Peptides 28, 1162–1169 (2007).
Tyson, J. E., Hwang, P., Guyda, H. & Friesen, H. G. Studies of prolactin secretion in human pregnancy. Am. J. Obstet. Gynecol. 113, 14–20 (1972).
Wynne-Edwards, K. E. & Timonin, M. E. Paternal care in rodents: weakening support for hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care. Horm. Behav. 52, 114–121 (2007).
Saltzman, W. et al. Paternal care in biparental rodents: intra-and inter-individual variation. Integr. Comp. Biol. 57, 589–602 (2017). This paper reviews environmental and hormonal factors that influence paternal responsiveness and contribute to intra-individual and inter-individual variations in paternal behaviour.
Ziegler, T. E., Prudom, S. L., Schultz-Darken, N. J., Kurian, A. V. & Snowdon, C. T. Pregnancy weight gain: marmoset and tamarin dads show it too. Biol. Lett. 2, 181–183 (2006).
Gordon, I., Zagoory-Sharon, O., Leckman, J. F. & Feldman, R. Oxytocin, cortisol, and triadic family interactions. Physiol. Behav. 101, 679–684 (2010).
Gordon, I., Zagoory-Sharon, O., Leckman, J. F. & Feldman, R. Oxytocin and the development of parenting in humans. Biol. Psychiatry 68, 377–382 (2010).
Ziegler, T. E., Jacoris, S. & Snowdon, C. T. Sexual communication between breeding male and female cotton-top Tamarins (Saguinus oedipus), and its relationship to infant care. Am. J. Primatol. 64, 57–69 (2004).
Perea-Rodriguez, J. P. et al. Effects of reproductive experience on central expression of progesterone, oestrogen α, oxytocin and vasopressin receptor mRNA in male California mice (Peromyscus californicus). J. Neuroendocrinol. 27, 245–252 (2015).
Wang, B., Li, Y., Wu, R., Zhang, S. & Tai, F. Behavioral responses to pups in males with different reproductive experiences are associated with changes in central OT, TH and OTR, D1R, D2R mRNA expression in mandarin voles. Horm. Behav. 67, 73–82 (2015).
Wang, Z. X., Liu, Y., Young, L. J. & Insel, T. R. Hypothalamic vasopressin gene expression increases in both males and females postpartum in a biparental rodent. J. Neuroendocrinol. 12, 111–120 (2000).
Kelly, A. M., Hiura, L. C., Saunders, A. G. & Ophir, A. G. Oxytocin neurons exhibit extensive functional plasticity due to offspring age in mothers and fathers. Integr. Comp. Biol. 57, 603–618 (2017).
Mak, G. K. & Weiss, S. Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat. Neurosci. 13, 753–758 (2010). This study in mice provides evidence that neurogenesis in the paternal brain may be involved in adult offspring recognition.
Kinsley, C. H. & Lambert, K. G. Reproduction-induced neuroplasticity: natural behavioural and neuronal alterations associated with the production and care of offspring. J. Neuroendocrinol. 20, 515–525 (2008).
Hyer, M. M., Hunter, T. J., Katakam, J., Wolz, T. & Glasper, E. R. Neurogenesis and anxiety-like behavior in male California mice during the mate’s postpartum period. Eur. J. Neurosci. 43, 703–709 (2016).
Glasper, E. R. et al. Fatherhood contributes to increased hippocampal spine density and anxiety regulation in California mice. Brain Behav. 6, 1–6 (2016).
Franssen, C. L. et al. Fatherhood alters behavioural and neural responsiveness in a spatial task. J. Neuroendocrinol. 23, 1177–1187 (2011).
Rilling, J. K. & Mascaro, J. S. The neurobiology of fatherhood. Curr. Opin. Psychol. 15, 26–32 (2017).
Mascaro, J. S., Hackett, P. D. & Rilling, J. K. Testicular volume is inversely correlated with nurturing-related brain activity in human fathers. Proc. Natl Acad. Sci. USA 110, 15746–15751 (2013).
Seifritz, E. et al. Differential sex-independent amygdala response to infant crying and laughing in parents versus nonparents. Biol. Psychiatry 54, 1367–1375 (2003).
Fan, Y., Duncan, N. W., de Greck, M. & Northoff, G. Is there a core neural network in empathy? An fMRI based quantitative meta-analysis. Neurosci. Biobehav. Rev. 35, 903–911 (2011).
Craig, A. D. How do you feel - now? The anterior insula and human awareness. Nat. Rev. Neurosci. 10, 59–70 (2009).
Mielke, E. L. et al. Maternal sensitivity and the empathic brain: Influences of early life maltreatment. J. Psychiatr. Res. 77, 59–66 (2016).
Singer, T. et al. Empathy for pain involves the affective but not sensory components of pain. Science 303, 1157–1163 (2004).
Rizzolatti, G. & Craighero, L. The mirror-neuron system. Annu. Rev. Neurosci. 27, 169–192 (2004).
Schaefer, M., Heinze, H. J. & Rotte, M. Close to you: embodied simulation for peripersonal space in primary somatosensory cortex. PLOS ONE 7, e42308 (2012).
Bornstein, M. H. et al. Neurobiology of culturally common maternal responses to infant cry. Proc. Natl Acad. Sci. USA 114, E9465–E9473 (2017).
Lenzi, D. et al. Neural basis of maternal communication and emotional expression processing during infant preverbal stage. Cereb. Cortex 19, 1124–1133 (2009).
Raz, G. et al. Cry for her or cry with her: context-dependent dissociation of two modes of cinematic empathy reflected in network cohesion dynamics. Soc. Cogn. Affect. Neurosci. 9, 30–38 (2014).
Kanat, M., Heinrichs, M. & Domes, G. Oxytocin and the social brain: neural mechanisms and perspectives in human research. Brain Res. 1580, 160–171 (2014).
Isik, L., Koldewyn, K., Beeler, D. & Kanwisher, N. Perceiving social interactions in the posterior superior temporal sulcus. Proc. Natl Acad. Sci. USA 114, E9145–E9152 (2017).
Menon, V. Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn. Sci. 15, 483–506 (2011).
Hipwell, A. E., Guo, C., Phillips, M. L., Swain, J. E. & Moses-Kolko, E. L. Right frontoinsular cortex and subcortical activity to infant cry is associated with maternal mental state talk. J. Neurosci. 35, 12725–12732 (2015).
Abraham, E., Hendler, T., Zagoory-Sharon, O. & Feldman, R. Network integrity of the parental brain in infancy supports the development of children’s social competencies. Soc. Cogn. Affect. Neurosci. 11, 1707–1718 (2016).
Kuo, P. X., Carp, J., Light, K. C. & Grewen, K. M. Neural responses to infants linked with behavioral interactions and testosterone in fathers. Biol. Psychol. 91, 302–306 (2012).
Abraham, E., Raz, G., Zagoory-Sharon, O. & Feldman, R. Empathy networks in the parental brain and their long-term effects on children’s stress reactivity and behavior adaptation. Neuropsychologia 116, 75–85 (2017).
Nishitani, S. et al. Genetic variants in oxytocin receptor and arginine-vasopressin receptor 1 A are associated with the neural correlates of maternal and paternal affection towards their child. Horm. Behav. 87, 47–56 (2017).
Gettler, L. T., McDade, T. W., Feranil, A. B. & Kuzawa, C. W. From the cover: longitudinal evidence that fatherhood decreases testosterone in human males. Proc. Natl Acad. Sci. USA 108, 16194–16199 (2011).
Wittfoth-Schardt, D. et al. Oxytocin modulates neural reactivity to children’s faces as a function of social salience. Neuropsychopharmacology 37, 1799–1807 (2012).
Li, T., Chen, X., Mascaro, J., Haroon, E. & Rilling, J. K. Intranasal oxytocin, but not vasopressin, augments neural responses to toddlers in human fathers. Horm. Behav. 93, 193–202 (2017).
Weisman, O., Zagoory-Sharon, O. & Feldman, R. Oxytocin administration, salivary testosterone, and father–infant social behavior. Prog. Neuropsychopharmacol. Biol. Psychiatry 49, 47–52 (2014).
Weisman, O. et al. Oxytocin shapes parental motion during father–infant interaction. Biol. Lett. 9, 20130828 (2013).
Weisman, O., Feldman, R. & Goldstein, A. Parental and romantic attachment shape brain processing of infant cues. Biol. Psychol. 89, 533–538 (2012).
Weisman, O., Zagoory-Sharon, O. & Feldman, R. Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement. Biol. Psychiatry 72, 982–989 (2012).
Naber, F., van Ijzendoorn, M. H., Deschamps, P., van Engeland, H. & Bakermans-Kranenburg, M. J. Intranasal oxytocin increases fathers’ observed responsiveness during play with their children: a double-blind within-subject experiment. Psychoneuroendocrinology 35, 1583–1586 (2010).
Leng, G. & Ludwig, M. Intranasal oxytocin: myths and delusions. Biol. Psychiatry 79, 243–250 (2016).
Maccari, S., Krugers, H. J., Morley-Fletcher, S., Szyf, M. & Brunton, P. J. The consequences of early-life adversity: Neurobiological, behavioural and epigenetic adaptations. J. Neuroendocrinol. 26, 707–723 (2014).
Weinstock, M. The long-term behavioural consequences of prenatal stress. Neurosci. Biobehav. Rev. 32, 1073–1086 (2008).
Meaney, M. J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 24, 1161–1192 (2001).
McGraw, L. A. & Young, L. J. The prairie vole: an emerging model organism for understanding the social brain. Trends Neurosci. 33, 103–109 (2010).
Birnie, A. K., Taylor, J. H., Cavanaugh, J. & French, J. A. Quality of maternal and paternal care predicts later stress reactivity in the cooperatively-breeding marmoset (Callithrix geoffroyi). Psychoneuroendocrinology 38, 3003–3014 (2013).
Bester-Meredith, J. K. & Marler, C. A. Vasopressin and the transmission of paternal behavior across generations in mated, cross-fostered Peromyscus mice. Behav. Neurosci. 117, 455–463 (2003).
Frazier, C. R. M., Trainor, B. C., Cravens, C. J., Whitney, T. K. & Marler, C. A. Paternal behavior influences development of aggression and vasopressin expression in male California mouse offspring. Horm. Behav. 50, 699–707 (2006).
Wang, J., Tai, F., Yan, X. & Yu, P. Paternal deprivation alters play-fighting, serum corticosterone and the expression of hypothalamic vasopressin and oxytocin in juvenile male mandarin voles. J. Comp. Physiol. A 198, 787–796 (2012).
Yu, P. et al. 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 (2012).
Bambico, F. R., Lacoste, B., Hattan, P. R. & Gobbi, G. Father absence in the monogamous California mouse impairs social behavior and modifies dopamine and glutamate synapses in the medial prefrontal cortex. Cereb. Cortex 25, 1163–1175 (2013).
Cao, Y. et al. Neonatal paternal deprivation impairs social recognition and alters levels of oxytocin and estrogen receptor α mRNA expression in the MeA and NAcc, and serum oxytocin in mandarin voles. Horm. Behav. 65, 57–65 (2014).
Braun, K. & Poeggel, G. Recognition of mother’s voice evokes metabolic activation in the medial prefrontal cortex and lateral thalamus of Octodon degus pups. Neuroscience 103, 861–864 (2001). This functional imaging study in degus demonstrates specific activation of prefrontal and thalamic regions in pups while recognizing their mother’s voice.
Poeggel, G. & Braun, K. Early auditory filial learning in degus (Octodon degus): behavioral and autoradiographic studies. Brain Res. 743, 162–170 (1996).
Greenough, W. T., Black, J. E. & Wallace, C. S. Experience and brain development. Child Dev. 58, 539–559 (1987).
Turrigiano, G. Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb. Perspect. Biol. 4, a005736 (2012). This paper is an overview of homeostatic plasticity mechanisms contributing to the stabilization of neuronal synaptic and circuit functions.
Helmeke, C. et al. Paternal deprivation during infancy results in dendrite-and time-specific changes of dendritic development and spine formation in the orbitofrontal cortex of the biparental rodent Octodon degus. Neuroscience 163, 790–798 (2009).
Braun, K., Seidel, K., Weigel, S., Roski, C. & Poeggel, G. Paternal deprivation alters region- and age-specific interneuron expression patterns in the biparental rodent, Octodon degus. Cereb. Cortex 21, 1532–1546 (2011).
Hyman, S. E., Malenka, R. C. & Nestler, E. J. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu. Rev. Neurosci. 29, 565–598 (2006).
Bredy, T. W., Brown, R. E. & Meaney, M. J. Effect of resource availability on biparental care, and offspring neural and behavioral development in the California mouse (Peromyscus californicus). Eur. J. Neurosci. 25, 567–575 (2007).
Pinkernelle, J., Abraham, A., Seidel, K. & Braun, K. Paternal deprivation induces dendritic and synaptic changes and hemispheric asymmetry of pyramidal neurons in the somatosensory cortex. Dev. Neurobiol. 69, 663–673 (2009).
Wu, R. et al. Early paternal deprivation alters levels of hippocampal brain-derived neurotrophic factor and glucocorticoid receptor and serum corticosterone and adrenocorticotropin in a sex-specific way in socially monogamous mandarin voles. Neuroendocrinology 100, 119–128 (2014).
Tabbaa, M., Lei, K., Liu, Y. & Wang, Z. Paternal deprivation affects social behaviors and neurochemical systems in the offspring of socially monogamous prairie voles. Neuroscience 343, 284–297 (2017).
Bramham, C. R. & Messaoudi, E. BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog. Neurobiol. 76, 99–125 (2005).
Braun, K., Seidel, K., Holetschka, R., Groeger, N. & Poeggel, G. Paternal deprivation alters the development of catecholaminergic innervation in the prefrontal cortex and related limbic brain regions. Brain Struct. Funct. 218, 859–872 (2013). This study in degus demonstrates the critical impact of paternal care during the development of catecholaminergic afferents into prefrontal and limbic brain areas.
Barker, J. M., Taylor, J. R. & Chandler, L. J. A unifying model of the role of the infralimbic cortex in extinction and habits. Learn. Mem. 21, 441–448 (2014).
Ragozzino, M. E., Adams, S. & Kesner, R. P. Differential involvement of the dorsal anterior cingulate and prelimbic-infralimbic areas of the rodent prefrontal cortex in spatial working memory. Behav. Neurosci. 112, 293–303 (1998).
Floresco, S. B. The nucleus accumbens: an interface between cognition, emotion, and action. Annu. Rev. Psychol. 66, 25–52 (2015).
Ch’ng, S., Fu, J., Brown, R. M., McDougall, S. J. & Lawrence, A. J. The intersection of stress and reward: BNST modulation of aversive and appetitive states. Prog. Neuropsychopharmacol. Biol. Psychiatry 87, 108–125 (2018).
Lebow, M. A. & Chen, A. Overshadowed by the amygdala: the bed nucleus of the stria terminalis emerges as key to psychiatric disorders. Mol. Psychiatry 21, 450–463 (2016).
Seidel, K., Poeggel, G., Holetschka, R., Helmeke, C. & Braun, K. Paternal deprivation affects the development of corticotrophin-releasing factor-expressing neurones in prefrontal cortex, amygdala and hippocampus of the biparental Octodon degus. J. Neuroendocrinol. 23, 1166–1176 (2011).
Gos, T. et al. Paternal deprivation affects the functional maturation of corticotropin-releasing hormone (CRH)- and calbindin-D28k-expressing neurons in the bed nucleus of the stria terminalis (BNST) of the biparental Octodon degus. Brain Struct. Funct. 219, 1983–1990 (2014).
Chen, Y., Andres, A. L., Frotscher, M. & Baram, T. Z. Tuning synaptic transmission in the hippocampus by stress: the CRH system. Front. Cell. Neurosci. 6, 13 (2012).
Jia, R., Tai, F., An, S. & Zhang, X. 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 (2011).
Wang, L. et al. Neuroendocrine responses to social isolation and paternal deprivation at different postnatal ages in mandarin voles. Dev. Psychobiol. 56, 1214–1228 (2014).
Mascaro, J. S., Rentscher, K. E., Hackett, P. D., Mehl, M. R. & Rilling, J. K. Child gender influences paternal behavior, language, and brain function. Behav. Neurosci. 131, 262–273 (2017). This study in humans provides evidence that gender differences in paternal behaviour are related to differential paternal brain responses towards male and female children.
Champagne, F. A. Epigenetic mechanisms and the transgenerational effects of maternal care. Front. Neuroendocrinol. 29, 386–397 (2008).
Wang, P. et al. Oxytocin-secreting system: a major part of the neuroendocrine center regulating immunologic activity. J. Neuroimmunol. 289, 152–161 (2015).
Gleason, E. D. & Marler, C. A. Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse. Proc. R. Soc. B 280, 20130824 (2013).
Gromov, V. S. Interactions of partners in family pairs, care of the offspring, and the role of tactile stimulation in formation of parental behavior of the Mongolian gerbil (Meriones unguiculatus) under laboratory conditions. Biol. Bull. 36, 479–488 (2009).
McGhee, K. E. & Bell, A. M. Paternal care in a fish: epigenetics and fitness enhancing effects on offspring anxiety. Proc. R. Soc. B 281, 20141146 (2014).
Ledig, M. et al. Paternal alcohol exposure: Developmental and behavioral effects on the offspring of rats. Neuropharmacology 37, 57–66 (1998).
Ceccanti, M. et al. Paternal alcohol exposure in mice alters brain NGF and BDNF and increases ethanol-elicited preference in male offspring. Addict. Biol. 21, 776–787 (2016).
Liang, F. et al. Paternal ethanol exposure and behavioral abnormities in offspring: Associated alterations in imprinted gene methylation. Neuropharmacology 81, 126–133 (2014).
Franklin, T. B. et al. Epigenetic transmission of the impact of early stress across generations. Biol. Psychiatry 68, 408–415 (2010).
Morgan, C. P. & Bale, T. L. Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. J. Neurosci. 31, 11748–11755 (2011).
Mychasiuk, R., Harker, A., Ilnytskyy, S. & Gibb, R. Paternal stress prior to conception alters DNA methylation and behaviour of developing rat offspring. Neuroscience 241, 100–105 (2013). This study in rats demonstrates that paternal stress prior to conception influences behavioural development and DNA methylation patterns in offspring in a sex-specific manner.
Rodgers, A. B., Morgan, C. P., Bronson, S. L., Revello, S. & Bale, T. L. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J. Neurosci. 33, 9003–9012 (2013). This study in mice reveals that paternal experience during puberty or adulthood induces epigenetic reprogramming in paternal germ cells and alters paternal sperm microRNA as well as hypothalamic–pituitary–adrenal stress axis regulation in the offspring.
Cordero, M. I., Just, N., Poirier, G. L. & Sandi, C. Effects of paternal and peripubertal stress on aggression, anxiety, and metabolic alterations in the lateral septum. Eur. Neuropsychopharmacol. 26, 357–367 (2016).
Harker, A., Raza, S., Williamson, K., Kolb, B. & Gibb, R. Preconception paternal stress in rats alters dendritic morphology and connectivity in the brain of developing male and female offspring. Neuroscience 303, 200–210 (2015).
Park, H.-S. & Kim, T.-W. Paternal physical exercise improves spatial learning ability by enhancing hippocampal neuroplasticity in male pups born from obese maternal rats. J. Exerc. Rehabil. 13, 266–272 (2017).
Luo, G., Wei, R., Wang, S., Luo, G. & Wei, R. Paternal bisphenol a diet changes prefrontal cortex proteome and provokes behavioral dysfunction in male offspring. Chemosphere 184, 720–729 (2017).
Fan, Y. et al. Does preconception paternal exposure to a physiologically relevant level of bisphenol A alter spatial memory in an adult rat? Horm. Behav. 64, 598–604 (2013).
Hultman, C. M., Sandin, S., Levine, S. Z., Lichtenstein, P. & Reichenberg, A. Advancing paternal age and risk of autism: new evidence from a population-based study and a meta-analysis of epidemiological studies. Mol. Psychiatry 16, 1203–1212 (2011).
Smith, R. G. et al. Advancing paternal age is associated with deficits in social and exploratory behaviors in the offspring: a mouse model. PLOS ONE 4, e8456 (2009).
Anway, M. D., Leathers, C. & Skinner, M. K. Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 147, 5515–5523 (2006).
Saavedra-Rodríguez, L. & Feig, L. A. Chronic social instability induces anxiety and defective social interactions across generations. Biol. Psychiatry 73, 44–53 (2013).
Dias, B. G. & Ressler, K. J. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat. Neurosci. 17, 89–96 (2014). This paper integrates multiple molecular, neural and behavioural techniques combined with in vitro fertilization to illustrate the likely role of the sperm-mediated transfer of paternal effects across generations.
Aarabi, M. et al. High-dose folic acid supplementation alters the human sperm methylome and is influenced by the MTHFR C677T polymorphism. Hum. Mol. Genet. 24, 6301–6313 (2015).
Hinkelmann, K. et al. Association between childhood trauma and low hair cortisol in depressed patients and healthy control subjects. Biol. Psychiatry 74, e15–e17 (2013).
Gapp, K. et al. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat. Neurosci. 17, 667–669 (2014). This paper illustrates the critical role of sperm RNAs in the propagation of paternal stress effects to offspring.
Rodgers, A. B., Morgan, C. P., Leu, N. A. & Bale, T. L. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc. Natl Acad. Sci. USA 112, 13699–13704 (2015).
Weismann, A. The Germ-Plasm: A Theory Of Heredity (Scribner’s, 1893).
Wilkins, J. F. & Haig, D. What good is genomic imprinting: the function of parent-specific gene expression. Nat. Rev. Genet. 4, 359–368 (2003).
Cameron, N. M. et al. The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci. Biobehav. Rev. 29, 843–865 (2005).
Zeybel, M. et al. Multigenerational epigenetic adaptation of the hepatic wound-healing response. Nat. Med. 18, 1369–1377 (2012). This paper illustrates the potential adaptiveness of multigenerational effects through the illustration of enhanced wound healing in descendants of male rats exposed to liver damage.
Vassoler, F. M. et al. Transgenerational attenuation of opioid self-administration as a consequence of adolescent morphine exposure. Neuropharmacology 113, 271–280 (2017).
Vassoler, F. M., White, S. L., Schmidt, H. D., Sadri-Vakili, G. & Pierce, R. C. Epigenetic inheritance of a cocaine-resistance phenotype. Nat. Neurosci. 16, 42–47 (2013).
Gilbert, L., Williamson, K., Hazon, N. & Graves, J. Maternal effects due to male attractiveness affect offspring development in the zebra finch. Proc. R. Soc. B 273, 1765–1771 (2006).
Harris, W. E. & Uller, T. Reproductive investment when mate quality varies: differential allocation versus reproductive compensation. Phil. Trans. R. Soc. B 364, 1039–1048 (2009).
Mashoodh, R., Habrylo, I. B., Gudsnuk, K. M., Pelle, G. & Champagne, F. A. Maternal modulation of paternal effects on offspring development. Proc. R. Soc. B 285, 20180118 (2018). This paper presents a study in mice demonstrating paternal influence on prenatal and postnatal maternal investment in offspring and using embryo transfer to illustrate paternal effects of paternal food restriction on offspring.
Mashoodh, R., Franks, B., Curley, J. P. & Champagne, F. A. Paternal social enrichment effects on maternal behavior and offspring growth. Proc. Natl Acad. Sci. USA 109, 17232–17238 (2012).
Yehuda, R. et al. Influences of maternal and paternal PTSD on epigenetic regulation of the glucocorticoid receptor gene in Holocaust survivor offspring. Am. J. Psychiatry 171, 872–880 (2014).
Kinnally, E. L. & Capitanio, J. P. Paternal early experiences influence infant development through non-social mechanisms in Rhesus Macaques. Front. Zool. 12, S14 (2015).
Whiting, B. B., Edwards, C. P., Edwards, C. P. & Ember, C. R. Children of Different Worlds: The Formation of Social Behavior (Harvard Univ. Press, 1992).
Tamis-LeMonda, C. S., Shannon, J. D., Cabrera, N. J. & Lamb, M. E. Fathers and mothers at play with their 2- and 3-year-olds: contributions to language and cognitive development. Child Dev. 75, 1806–1820 (2004).
Feldman, R. Infant–mother and infant–father synchrony: the coregulation of positive arousal. Infant Ment. Health J. 24, 1–23 (2003).
Feldman, R., Bamberger, E. & Kanat-Maymon, Y. Parent-specific reciprocity from infancy to adolescence shapes children’s social competence and dialogical skills. Attach. Hum. Dev. 15, 407–423 (2013). This longitudinal study of the father–child relationship from infancy to adolescence, in comparison with mother–child relationships, shows the effects of sensitive fathering on child aggression modulation and conflict management.
Nelson, C. & Valliant, P. M. Personality dynamics of adolescent boys where the father was absent. Percept. Mot. Skills 76, 435–443 (1993).
Sigle-Rushton, W. & McLanahan, S. Father Absence and Child Wellbeing: A Critical Review (Russell Sage Foundation New York, 2004).
Vakrat, A., Apter-Levy, Y. & Feldman, R. Fathering moderates the effects of maternal depression on the family process. Dev. Psychopathol. 30, 1–12 (2017).
Feldman, R. Sensitive periods in human social development: New insights from research on oxytocin, synchrony, and high-risk parenting. Dev. Psychopathol. 27, 369–395 (2015).
Feldman, R., Gordon, I., Influs, M., Gutbir, T. & Ebstein, R. P. Parental oxytocin and early caregiving jointly shape children’s oxytocin response and social reciprocity. Neuropsychopharmacology 38, 1154–1162 (2013).
Raz, G. et al. Portraying emotions at their unfolding: a multilayered approach for probing dynamics of neural networks. Neuroimage 60, 1448–1461 (2012).
Kim, P. et al. A prospective longitudinal study of perceived infant outcomes at 18–24 months: neural and psychological correlates of parental thoughts and actions assessed during the first month postpartum. Front. Psychol. 6, 1772 (2015).
Conger, R. D., Belsky, J. & Capaldi, D. M. The intergenerational transmission of parenting: closing comments for the special section. Dev. Psychol. 45, 1276–1283 (2009).
Saito, A., Izumi, A. & Nakamura, K. Food transfer in common marmosets: parents change their tolerance depending on the age of offspring. Am. J. Primatol. 70, 999–1002 (2008).
Finkenwirth, C., Martins, E., Deschner, T. & Burkart, J. M. Oxytocin is associated with infant-care behavior and motivation in cooperatively breeding marmoset monkeys. Horm. Behav. 80, 10–18 (2016).
Spence-Aizenberg, A., Di Fiore, A. & Fernandez-Duque, E. Social monogamy, male-female relationships, and biparental care in wild titi monkeys (Callicebus discolor). Primates 57, 103–112 (2016).
Woodroffe, R. & Vincent, A. Mother’s little helpers: patterns of male care in mammals. Trends Ecol. Evol. 9, 294–297 (1994).
Ziegler, T. E., Sosa, M. E. & Colman, R. J. Fathering style influences health outcome in common marmoset (Callithrix jacchus) offspring. PLOS ONE 12, e0185695 (2017).
Williams, E. & Radin, N. Effects of father participation in child rearing: twenty-year follow-up. Am. J. Orthopsychiatry 69, 328–336 (1999).
Pruett, K. Partnership Parenting: How Men and Women Parent Differently — Why It Helps Your Kids and Can Strengthen Your Marriage (ReadHowYouWant.com, 2010).
Feldman, R. Parents’ convergence on sharing and marital satisfaction, father involvement, and parent-child relationship at the transition to parenthood. Infant Ment. Health J. 21, 176–191 (2000).
Feldman, R., Gordon, I., Schneiderman, I., Weisman, O. & Zagoory-Sharon, O. Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 35, 1133–1141 (2010).
Stgeorge, J. & Freeman, E. Measurments of father-child rough-and-tumble play and its relations to childbehavior. Infant Ment. Health J. 38, 709–725 (2017).
Flanders, J. L., Leo, V., Paquette, D., Pihl, R. O. & Séguin, J. R. Rough-and-tumble play and the regulation of aggression: an observational study of father–child play dyads. Aggress. Behav. 35, 285–295 (2009).
StGeorge, J. M., Wroe, J. K. & Cashin, M. E. The concept and measurement of fathers’ stimulating play: a review. Attach. Hum. Dev. 20, 634–658 (2018).
Gordon, I., Zagoory-Sharon, O., Leckman, J. F. & Feldman, R. Prolactin, oxytocin, and the development of paternal behavior across the first six months of fatherhood. Horm. Behav. 58, 513–518 (2010).
Apter-Levi, Y., Zagoory-Sharon, O. & Feldman, R. Oxytocin and vasopressin support distinct configurations of social synchrony. Brain Res. 1580, 124–132 (2014).
Feldman, R. & Klein, P. S. Toddlers’ self-regulated compliance to mothers, caregivers, and fathers: implications for theories of socialization. Dev. Psychol. 39, 680–692 (2003).
Feldman, R. & Masalha, S. Parent-child and triadic antecedents of children’s social competence: cultural specificity, shared process. Dev. Psychol. 46, 455–467 (2010).
Rogoff, B. et al. Guided participation in cultural activity by toddlers and caregivers. Monogr. Soc. Res. Child Dev. 58, 1–179 (1993).
Abraham, E. et al. The human coparental bond implicates distinct corticostriatal pathways; longitudinal impact on family formation and child well-being. Neuropsychopharmacology 42, 2301–2313 (2017).
Pinker, S. The Better Angels of Our Nature: Why Violence Has Declined (Penguin, 2011).
Harkness, K. L., Stewart, J. G. & Wynne-Edwards, K. E. Cortisol reactivity to social stress in adolescents: role of depression severity and child maltreatment. Psychoneuroendocrinology 36, 173–181 (2011).
Kim, S., Fonagy, P., Koos, O., Dorsett, K. & Strathearn, L. Maternal oxytocin response predicts mother-to-infant gaze. Brain Res. 1580, 133–142 (2014).
Parker, K. J., Kinney, L. F., Phillips, K. M. & Lee, T. M. Paternal behavior is associated with central neurohormone receptor binding patterns in meadow voles (Microtus pennsylvanicus). Behav. Neurosci. 115, 1341–1348 (2001).
Li, T. et al. Explaining individual variation in paternal brain responses to infant cries. Physiol. Behav. 193, 43–54 (2018).
Mascaro, J. S., Hackett, P. D. & Rilling, J. K. Differential neural responses to child and sexual stimuli in human fathers and non-fathers and their hormonal correlates. Psychoneuroendocrinology 46, 153–163 (2014).
Ko, J. Neuroanatomical substrates of rodent social behavior: the medial prefrontal cortex and its projection patterns. Front. Neural Circuits 11, 41 (2017).
O’Connell, L. A. & Hofmann, H. A. The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J. Comp. Neurol. 519, 3599–3639 (2011).
Kohl, J. & Dulac, C. Neural control of parental behaviors. Curr. Opin. Neurobiol. 49, 116–122 (2018).
Ovtscharoff, Jr, W., Helmeke, C. & Braun, K. Lack of paternal care affects synaptic development in the anterior cingulate cortex. Brain Res. 1116, 58–63 (2006).
He, Z. et al. Pre-weaning paternal deprivation impairs social recognition and alters hippocampal neurogenesis and spine density in adult mandarin voles. Neurobiol. Learn. Mem. 155, 452–462 (2018).
The authors thank K. Yirmiya for her editorial assistance and M. Harel for the graphic art. The authors are supported by funding from the German–Israel Foundation (GIF) to R.F. and K.B. (#1114-101.4/2010), the Simms/Mann Chair to R.F., a Harris Foundation Grant to R.F., the Bundesministerium für Forschung und Technik (BMBF) Konsortium ‘TRANSGEN’ (#01KR1304B) to K.B. and the US National Institute of Mental Health (#1P50MH090964-01A1) to F.A.C.
Nature Reviews Neuroscience thanks J. Rilling and T. Ziegler, and other anonymous reviewer(s), for their contribution to the peer review of this work.
The authors declare no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
- Biparental species
Species in which biological fathers participate in direct caregiving (such as carrying or grooming) and indirect caregiving (such as guarding or provisioning) of their offspring. Biparental care is observed in only 3–5% of mammalian species, and these species are typically socially monogamous.
- Optogenetic targeting
The selective activation of neurons that have been genetically altered to express light-sensitive opsins.
- Phenotypic plasticity
The capacity to dynamically alter the phenotypic characteristics (including their patterns of behaviour) of an individual in response to environmental cues.
Adults (including juveniles and fathers), other than the biological mothers, that care for infants. Allomothering is widespread among primates, including humans, and is critical for infants to survive and thrive.
- Reward value
The degree to which a stimulus, object or activity will result in approach responses.
- Genome-wide association study
A study in which a genome-wide set of genetic variants in different individuals is associated with a trait.
- Pair bonding
The formation of strong social affiliation between two individuals following mating, which typically results in a socially monogamous relationship.
A peptide hormone and neuropeptide that is produced by the hypothalamus and has a role in social bonding and affiliation.
- Global human caregiving network
A network of subcortical and cortical regions that underpins human parental behaviour.
- Stress-hyporesponsive phase
A period during postnatal development during which the physiological and behavioural response to stress is blunted.
- Homeostatic synaptic plasticity
The feedback mechanism used by neurons to balance excessive excitation or inhibition by adjusting the strength and/or the number of synaptic connections. This capacity is essential for restraining network activity and maintaining a healthy level of synaptic plasticity needed for adaptations to the environment.
- Epigenetic transmission
The transmission across generations of epigenetic variation that results in the transmission of associated traits.
About this article
Cite this article
Feldman, R., Braun, K. & Champagne, F.A. The neural mechanisms and consequences of paternal caregiving. Nat Rev Neurosci 20, 205–224 (2019). https://doi.org/10.1038/s41583-019-0124-6
What Guides Us to Neurally and Behaviorally Align With Anyone Specific? A Neurobiological Model Based on fNIRS Hyperscanning Studies
The Neuroscientist (2020)
Frontiers in Cellular Neuroscience (2020)
Cumulative Risk on Oxytocin-Pathway Genes Impairs Default Mode Network Connectivity in Trauma-Exposed Youth
Frontiers in Endocrinology (2020)
World Psychiatry (2020)