Brain, oxytocin, and parenting behavior were measured in primary-caregiving mothers, secondary-caregiving fathers, and primary-caregiving homosexual fathers raising infants without maternal involvement. Parenting integrated functioning of two neural networks: subcortical-paralimbic structures implicated in emotional processing and cortical circuits involved in social understanding. Mothers showed greater activation in the emotional processing network and fathers in the socio-cognitive circuits, which were differentially linked with oxytocin and behavior. Primary-caregiving fathers exhibited high amygdala activation similar to mothers, alongside high superior temporal sulcus (STS) activation comparable to fathers, and functional connectivity between amygdala and STS. Among all fathers, time spent in childcare correlated with amygdala-STS connectivity. Findings describe mechanisms of brain malleability with caregiving experiences in human fathers.

Abstract

Although contemporary socio-cultural changes dramatically increased fathers' involvement in childrearing, little is known about the brain basis of human fatherhood, its comparability with the maternal brain, and its sensitivity to caregiving experiences. We measured parental brain response to infant stimuli using functional MRI, oxytocin, and parenting behavior in three groups of parents (n = 89) raising their firstborn infant: heterosexual primary-caregiving mothers (PC-Mothers), heterosexual secondary-caregiving fathers (SC-Fathers), and primary-caregiving homosexual fathers (PC-Fathers) rearing infants without maternal involvement. Results revealed that parenting implemented a global “parental caregiving” neural network, mainly consistent across parents, which integrated functioning of two systems: the emotional processing network including subcortical and paralimbic structures associated with vigilance, salience, reward, and motivation, and mentalizing network involving frontopolar-medial-prefrontal and temporo-parietal circuits implicated in social understanding and cognitive empathy. These networks work in concert to imbue infant care with emotional salience, attune with the infant state, and plan adequate parenting. PC-Mothers showed greater activation in emotion processing structures, correlated with oxytocin and parent-infant synchrony, whereas SC-Fathers displayed greater activation in cortical circuits, associated with oxytocin and parenting. PC-Fathers exhibited high amygdala activation similar to PC-Mothers, alongside high activation of superior temporal sulcus (STS) comparable to SC-Fathers, and functional connectivity between amygdala and STS. Among all fathers, time spent in direct childcare was linked with the degree of amygdala-STS connectivity. Findings underscore the common neural basis of maternal and paternal care, chart brain–hormone–behavior pathways that support parenthood, and specify mechanisms of brain malleability with caregiving experiences in human fathers.