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Neural mechanisms of mother–infant bonding and pair bonding: Similarities, differences, and broader implications
Open accessAbstract
This article is part of a Special Issue "Parental Care". Mother-infant bonding is a characteristic of virtually all mammals. The maternal neural system may have provided the scaffold upon which other types of social bonds in mammals have been built. For example, most mammals exhibit a polygamous mating system, but monogamy and pair bonding between mating partners occur in ~5% of mammalian species. In mammals, it is plausible that the neural mechanisms that promote mother-infant bonding have been modified by natural selection to establish the capacity to develop a selective bond with a mate during the evolution of monogamous mating strategies. Here we compare the details of the neural mechanisms that promote mother-infant bonding in rats and other mammals with those that underpin pair bond formation in the monogamous prairie vole. Although details remain to be resolved, remarkable similarities and a few differences between the mechanisms underlying these two types of bond formation are revealed. For example, amygdala and nucleus accumbens-ventral pallidum (NA-VP) circuits are involved in both types of bond formation, and dopamine and oxytocin actions within NA appear to promote the synaptic plasticity that allows either infant or mating partner stimuli to persistently activate NA-VP attraction circuits, leading to an enduring social attraction and bonding. Further, although the medial preoptic area is essential for maternal behavior, its role in pair bonding remains to be determined. Our review concludes by examining the broader implications of this comparative analysis, and evidence is provided that the maternal care system may have also provided the basic neural foundation for other types of strong social relationships, beyond pair bonding, in mammals, including humans.
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In the citing paper
“Oxytocin is also released somatodendritically to act within the SON and PVN to facilitate synchronous firing and pulsatile release during parturition and nursing”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Numan & Young 2016
Experimental — accuracy not yet measuredIn the citing paper
“Animal24 and human studies25 indicate that similar neural systems and behavioral patterns underpin the parent-infant and pair bonds and demonstrate that both forms of human attachment are characterized by behavioral synchrony26–28.”
From Brain-to-Brain Synchrony during Naturalistic Social Interactions (2017) · cites this paper as [24]
In the citing paper
“Work in rats has demonstrated that central OT signalling is crucial for the onset of maternal nurturing behaviour (1,2).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [2]
In the citing paper
“In monogamous prairie voles (Microtus ochrogaster), OT and AVP interact with the dopamine system to facilitate the formation of pair bonds between mates (2,6).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [2]
In the citing paper
“OXTR affects a range of social behaviors in animals including maternal nurturing and bonding (1, 2), social reward and gregariousness (3, 4), social recognition (5), and pair bonding in monogamous species (6–8).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [2]
In the citing paper
“The mother–infant bond is thought to be the evolutionary and neurobiological origin for the capacity to form adult social bonds in species that form bonds between mates, like humans.”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Numan and Young 2016
In the citing paper
“Although it remains unclear whether learning in human infants is the same as the rodent, NE plays a critical role in bond formation in numerous species (Nelson and Panksepp, 1998, Numan and Young, 2016), suggesting it is a phylogenetically conserved system.”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Numan and Young, 2016
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“1 is: (a) MPOA/vBST neurons project to VTA (Numan & Numan, 1997; 1996), and VTA neural activity is necessary for the occurrence of the appetitive aspects of maternal behavior (Numan et al., 2009); (b) DA is released into NAs during maternal behavior (Afonso et al., 2009; Champagne et al., 2004);…”
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Pup odor and ultrasonic vocalizations synergistically stimulate maternal attention in mice.
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Impairments in the Initiation of Maternal Behavior in Oxytocin Receptor Knockout Mice
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Neurobiology of Social Behavior: Toward an Understanding of the Prosocial and Antisocial Brain
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Self-citationOxytocin-induced excitation of neurones in the rat central and medial amygdaloid nuclei
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Understanding the human parental brain: A critical role of the orbitofrontal cortex
Parsons, C. E., Stark, E. A., Young, K. S., Stein, A. L., & Kringelbach, M. L. (2013) · Social Neuroscience · doi:10.1080/17470919.2013.842610 · Cited by 91
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A Neural Signature of Affiliative Emotion in the Human Septohypothalamic Area
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Self-citationExperience-facilitated improvements in pup retrieval; evidence for an epigenetic effect
Stolzenberg, D. S., Stevens, J. S., & Rissman, E. F. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.05.012 · Cited by 86
Numan, M., Bress, J. N., Ranker, L. R., Gary, A. J., DeNicola, A. L., Bettis, J. K., & Knapp, S. E. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.06.006 · Cited by 84
Self-citationThe roles of accumbal dopamine D1 and D2 receptors in maternal memory in rats.
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CD38 in the nucleus accumbens and oxytocin are related to paternal behavior in mice
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Oxytocin, social cognition and psychiatry
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Maternal Behavior: Neural Circuits, Stimulus Valence, and Motivational Processes
Numan, M. (2012) · Parenting · doi:10.1080/15295192.2012.680406 · Cited by 62
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A role for the ventral pallidum in context‐induced and primed reinstatement of alcohol seeking
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Flagged first, then by citations
2 of the 156 references couldn’t be matched to a known paper.
Research works printed but not linked: 2
- Mogenson, 1987, Limbic-motor integration, Prog. Psychobiol. Physiol. Psychol., 12, 117
- Numan, 2006, Maternal behavior, vol. 2, 1921
Cited by
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The oxytocin receptor: from intracellular signaling to behavior
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The Neurobiology of Human Attachments
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Self-citationOxytocin, Neural Plasticity, and Social Behavior
Froemke, R. C., & Young, L. J. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-102320-102847 · Cited by 480
“Oxytocin is also released somatodendritically to act within the SON and PVN to facilitate synchronous firing and pulsatile release during parturition and nursing (Burbach et al. 2006, Leng et al. 2008, Numan & Young 2016, Jurek & Neumann 2018, Valtcheva & Froemke 2019).”
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Metadata
- Authors
- Numan, M., & Young, L. J.
- Affiliations
- Emory University (US)
- Corresponding author
- Numan, Michael
- ORCID
- Young, Larry J.
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 2016-01
- Volume
- 77
- Pages
- 98-112
- ISSN
- 0018-506X (ISSN-L)
- PMC
- PMC4671834
- OpenAlex
- W625443388
- Cited by
- 355
- References
- 156
- Citations by year
- 2026: 16 · 2025: 25 · 2024: 31 · 2023: 28 · 2022: 29 · 2021: 39 · 2020: 50 · 2019: 26 · 2018: 30 · 2017: 38 · 2016: 33
- FWCI
- 5.77
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Hormones and Behavior (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (R01MH096983, 1P50MH100023, OD P51OD11132)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- mother-infant bonding, pair bonding, monogamy, Microtus ochrogaster, rats, amygdala, dopamine, oxytocin, synaptic plasticity, medial preoptic area, maternal behavior
- MeSH terms
- Animals, Dopamine, Female, Mammals, Maternal Behavior, Mothers, Object Attachment, Oxytocin, Pair Bond, Cerebrum
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