The neural mechanisms and consequences of paternal caregiving

Abstract

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.

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Fig. 1: The paternal brain.
Fig. 2: The paternally deprived offspring brain.
Fig. 3: Paternal transmission via germ cells.

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Acknowledgements

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.

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Nature Reviews Neuroscience thanks J. Rilling and T. Ziegler, and other anonymous reviewer(s), for their contribution to the peer review of this work.

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Glossary

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.

Allomothers

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.

Oxytocin

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.

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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

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