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Father's brain is sensitive to childcare experiences

Eyal Abraham, Talma Hendler, Irit Shapira-Lichter, Yaniv Kanat-Maymon, Orna Zagoory-Sharon, and Ruth Feldman
PNAS published ahead of print May 27, 2014 https://doi.org/10.1073/pnas.1402569111
Eyal Abraham
aDepartment of Psychology and the Gonda Brain Research Center, Bar-Ilan University, Ramat-Gan 52900, Israel;
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Talma Hendler
bFunctional Brain Center, Wohl Institute of Advanced Imaging, andcSchool of Psychological Sciences, Faculty of Medicine and Sagol School of Neuroscience, Tel Aviv University, Tel Aviv 69978, Israel; and
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Irit Shapira-Lichter
bFunctional Brain Center, Wohl Institute of Advanced Imaging, anddFunctional Neurosurgery Unit, Tel-Aviv Sourasky Center, Tel Aviv 64239, Israel;
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Yaniv Kanat-Maymon
eSchool of Psychology, Interdisciplinary Center, Herzlia 46346, Israel
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Orna Zagoory-Sharon
aDepartment of Psychology and the Gonda Brain Research Center, Bar-Ilan University, Ramat-Gan 52900, Israel;
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Ruth Feldman
aDepartment of Psychology and the Gonda Brain Research Center, Bar-Ilan University, Ramat-Gan 52900, Israel;
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  • For correspondence: feldman@mail.biu.ac.il
  1. Edited by Michael I. Posner, University of Oregon, Eugene, OR, and approved May 1, 2014 (received for review February 11, 2014)

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Significance

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.

  • mothering
  • parent–infant interaction
  • alloparental care
  • transition to parenthood
  • social brain

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: feldman{at}mail.biu.ac.il.
  • Author contributions: E.A., T.H., and R.F. designed research; E.A. and O.Z.-S. performed research; T.H. and R.F. contributed new reagents/analytic tools; E.A., I.S.-L., Y.K.-M., O.Z.-S., and R.F. analyzed data; and E.A. and R.F. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1402569111/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Brain basis of human fatherhood
Eyal Abraham, Talma Hendler, Irit Shapira-Lichter, Yaniv Kanat-Maymon, Orna Zagoory-Sharon, Ruth Feldman
Proceedings of the National Academy of Sciences May 2014, 201402569; DOI: 10.1073/pnas.1402569111

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Brain basis of human fatherhood
Eyal Abraham, Talma Hendler, Irit Shapira-Lichter, Yaniv Kanat-Maymon, Orna Zagoory-Sharon, Ruth Feldman
Proceedings of the National Academy of Sciences May 2014, 201402569; DOI: 10.1073/pnas.1402569111
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