Father’s brain is sensitive to childcare experiences Eyal Abrahama, Talma Hendlerb,c, Irit Shapira-Lichterb,d, Yaniv Kanat-Maymone, Orna Zagoory-Sharona, and Ruth Feldmana,1 aDepartment of Psychology and the Gonda Brain Research Center, Bar-Ilan University, Ramat-Gan 52900, Israel; bFunctional Brain Center, Wohl Institute of Advanced Imaging, and dFunctional Neurosurgery Unit, Tel-Aviv Sourasky Center, Tel Aviv 64239, Israel; cSchool of Psychological Sciences, Faculty of Medicine and Sagol School of Neuroscience, Tel Aviv University, Tel Aviv 69978, Israel; and eSchool of Psychology, Interdisciplinary Center, Herzlia 46346, Israel Edited by Michael I. Posner, University of Oregon, Eugene, OR, and approved May 1, 2014 (received for review February 11, 2014) Although contemporary socio-cultural changes dramatically in- that maximize survival (2, 9). Animal studies have demonstrated creased fathers’ involvement in childrearing, little is known about that mammalian mothering is supported by evolutionarily an- the brain basis of human fatherhood, its comparability with the cient structures implicated in emotional processing, vigilance, maternal brain, and its sensitivity to caregiving experiences. We motivation, and reward, which are rich in oxytocin receptors, measured parental brain response to infant stimuli using func- including the amygdala, hypothalamus, nucleus accumbens, and tional MRI, oxytocin, and parenting behavior in three groups of ventral tegmental area (VTA), and that these regions are sen- parents (n = 89) raising their firstborn infant: heterosexual primary- sitive to caregiving behavior (9, 10). Imaging studies of human caregiving mothers (PC-Mothers), heterosexual secondary-caregiving mothers found activation in similar areas, combined with para- fathers (SC-Fathers), and primary-caregiving homosexual fathers limbic insula-cingulate structures that imbue infants with affec- tive salience, ground experience in the present moment and (PC-Fathers) rearing infants without maternal involvement. Results – revealed that parenting implemented a global “parental caregiving” enable maternal simulation of infant states (11 13). These neural network, mainly consistent across parents, which integrated structures implicate a phylogenetically ancient network of emo- tional processing that rapidly detects motivationally salient and functioning of two systems: the emotional processing network survival-related cues (14) and enables parents to automatically including subcortical and paralimbic structures associated with vig- identify and immediately respond to infant distress, thereby ilance, salience, reward, and motivation, and mentalizing network maximizing survival. In humans, this emotional processing involving frontopolar-medial-prefrontal and temporo-parietal cir- network is complemented by a cortical mentalizing network of cuits implicated in social understanding and cognitive empathy. frontopolar-medial-prefrontal-temporo-parietal structures in- These networks work in concert to imbue infant care with emo- volved in social understanding, theory of mind, and cognitive tional salience, attune with the infant state, and plan adequate empathy, including the medial prefrontal cortex (mPFC), parenting. PC-Mothers showed greater activation in emotion pro- frontopolar cortex, superior temporal sulcus (STS), and tem- cessing structures, correlated with oxytocin and parent-infant poral poles (15). The mentalizing network plays an important synchrony, whereas SC-Fathers displayed greater activation in role in individuals’ ability to infer mental states from behavior, cortical circuits, associated with oxytocin and parenting. PC-Fathers is already activated during the parents’ first weeks of parenting, exhibited high amygdala activation similar to PC-Mothers, alongside and enables parents to cognitively represent infant states, high activation of superior temporal sulcus (STS) comparable to predict infant needs, and plan future caregiving (11–13). SC-Fathers, and functional connectivity between amygdala and The few studies examining the human father’s brain showed STS. Among all fathers, time spent in direct childcare was linked activation in similar areas, including the STS, lateral and medial with the degree of amygdala-STS connectivity. Findings under- score the common neural basis of maternal and paternal care, Significance chart brain–hormone–behavior pathways that support parent- hood, and specify mechanisms of brain malleability with care- Brain, oxytocin, and parenting behavior were measured in giving experiences in human fathers. primary-caregiving mothers, secondary-caregiving fathers, and primary-caregiving homosexual fathers raising infants without mothering | parent–infant interaction | alloparental care | maternal involvement. Parenting integrated functioning of transition to parenthood | social brain two neural networks: subcortical-paralimbic structures impli- cated in emotional processing and cortical circuits involved in hroughout human history and across cultures, women have social understanding. Mothers showed greater activation in Ttypically assumed primary caregiving responsibility for in- the emotional processing network and fathers in the socio- fants (1, 2). Although humans are among the few mammalian cognitive circuits, which were differentially linked with oxy- species where some male parental caregiving is relatively common, tocin and behavior. Primary-caregiving fathers exhibited high father involvement varies considerably within and across cul- amygdala activation similar to mothers, alongside high supe- tures, adapting to ecological conditions (1, 3). Involved fathering rior temporal sulcus (STS) activation comparable to fathers, and has been linked with children’s long-term physiological and so- functional connectivity between amygdala and STS. Among all cial development and with increases in mothers’ caregiving- fathers, time spent in childcare correlated with amygdala-STS related hormones such as oxytocin and prolactin (3–6). In ad- connectivity. Findings describe mechanisms of brain mallea- dition, animal studies demonstrated structural brain alterations bility with caregiving experiences in human fathers. in caregiving fathers (7, 8). It has been suggested that, although maternal caregiving is triggered by neurobiological processes related Author contributions: E.A., T.H., and R.F. designed research; E.A. and O.Z.-S. performed to pregnancy and labor, the human father’s brain, similar to other research; T.H. and R.F. contributed new reagents/analytic tools; E.A., I.S.-L., Y.K.-M., O.Z.-S., biparental mammals, adapts to the parental role through active in- and R.F. analyzed data; and E.A. and R.F. wrote the paper. volvement in childcare (1–3). Despite growing childcare involvement The authors declare no conflict of interest. of fathers (3, 5, 6), mechanisms for human fathers’ brain adaptation This article is a PNAS Direct Submission. to caregiving experiences remain largely unknown, and no study to Freely available online through the PNAS open access option. our knowledge has examined the brain basis of human fatherhood See Commentary on page 9671. when fathers assume primary responsibility for infant care. 1To whom correspondence should be addressed. E-mail: [email protected]. For social species with lengthy periods of dependence, pa- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. rental caregiving is key to survival and relies on brain structures 1073/pnas.1402569111/-/DCSupplemental. 9792–9797 | PNAS | July 8, 2014 | vol. 111 | no. 27 www.pnas.org/cgi/doi/10.1073/pnas.1402569111 Downloaded by guest on September 26, 2021 frontal regions, VTA, inferior frontal gyrus (IFG), and orbitofrontal brain response as mediated by actual caregiving experiences. cortex (OFC) (16, 17). Only one study compared maternal and Such variability would be particularly noted among the primary- SEE COMMENTARY paternal brain response to infant cues, reporting mothers’ greater caregiving fathers raising infants without mothers and may amygdala activation, fathers’ greater superior-temporal and medial- involve functional integration of the subcortical and cortical frontal activation, and maternal and paternal oxytocin’s different networks subserving parenting. Finally, we expected that the path- associations with amygdala vs. cortical activation (18). Oxytocin, ways leading from the parent’s primary caregiving role to greater a nine-amino acid neuropeptide that underpins the formation of parent–infant synchrony would be mediated by parental brain ac- affiliative bonds (19), supports the development of human parental tivation and oxytocin levels. caregiving (20). Research has shown that maternal and paternal oxytocin levels are associated with parent–infant synchrony, which Results is the parent’s careful adaptation of caregiving behavior to infant’s Coinciding with ethological perspectives, we first examined dif- social signals (21). However, although oxytocin levels are similar ferences in parenting behavior. The parent–infant synchrony in mothers and fathers, oxytocin is differentially linked with the construct includes eight scales assessing parents’ provision of the parent-specific repertoire, for instance, with affectionate contact in human parental repertoire (i.e., vocalizations and affective mothers and stimulatory play in fathers (5, 20). touch) and its coordination with infant signals (Materials and Ethological perspectives emphasize the importance of study-