The DOI matches its Crossref record; 154 of the 156 references it cites were found in a registry or an index.
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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Citations
Cites
The Physiology of Reproduction
Legendre, M., & Jalabert, B. (1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-109-2-176_1 · Cited by 7,876
How do you feel — now? The anterior insula and human awareness
(Bud) Craig, A. D. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2555 · Cited by 6,657 · cited 2×
“As an example, the anterior insular cortex (AI) is a prominent part of the neural circuitry underlying empathic feeling states in humans (Craig, 2009; Engen and Singer, 2013), and AI has direct and indirect neural connections with the amygdala, PFC, NA, and hypothalamus.”
BackgroundMothers and others: the evolutionary origins of mutual understanding
(2010) · Choice Reviews Online · doi:10.5860/choice.47-3250 · Cited by 1,735
The neurobiology of pair bonding.
Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523 · cited 7×
“While the roles of OT, vasopressin, and DA in the NAs and VP in regulating pair bonding have been well documented (Young et al., 2011; Young and Wang, 2004), the precise neural mechanisms by which these molecules lead to the formation of a selective social preference for the partner has yet to be determined, and is th…”
BackgroundResultInfluentialSelf-citationKleiman, D. G. (1977) · The Quarterly Review of Biology · doi:10.1086/409721 · Cited by 1,436
The neurobiology of attachment
Insel, T. R., & Young, L. J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35053579 · Cited by 1,173
Self-citationSocial reward requires coordinated activity of nucleus accumbens oxytocin and serotonin
Dölen, G., Darvishzadeh, A., Huang, K. W., & Malenka, R. C. (2013) · Nature · doi:10.1038/nature12518 · Cited by 1,161
Evoked axonal oxytocin release in the central amygdala attenuates fear response
Knobloch, H. S., Charlet, A., Hoffmann, L. C., Eliava, M., Khrulev, S., Cetin, A. H., Osten, P., Schwarz, M. K., Seeburg, P. H., Stoop, R., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.030 · Cited by 1,049
Oxytocin in the Medial Amygdala is Essential for Social Recognition in the Mouse
Ferguson, J. N., Aldag, J. M., Insel, T. R., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-20-08278.2001 · Cited by 1,043
Self-citationA role for central vasopressin in pair bonding in monogamous prairie voles
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. (1993) · Nature · doi:10.1038/365545a0 · Cited by 948 · cited 5×
“Early research in male prairie voles suggested that arginine vasopressin (AVP, which is structurally similar to OT), but not OT, regulated the development of partner preferences following mating (Winslow et al., 1993).”
BackgroundResultInfluential
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
Sorted by citations
The oxytocin receptor: from intracellular signaling to behavior
Jurek, B., & Neumann, I. D. (2018) · Physiological Reviews · doi:10.1152/physrev.00031.2017 · Cited by 999
The Neurobiology of Human Attachments
Feldman, R. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.11.007 · Cited by 839
Oxytocin-dependent consolation behavior in rodents
Burkett, J. P., Andari, E., Johnson, Z. V., Curry, D. C., de Waal, F. B. M., & Young, L. J. (2016) · Science · doi:10.1126/science.aac4785 · Cited by 692
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).”
BackgroundSelf-citationBrain-to-Brain Synchrony during Naturalistic Social Interactions
Kinreich, S., Djalovski, A., Kraus, L., Louzoun, Y., & Feldman, R. (2017) · Scientific Reports · doi:10.1038/s41598-017-17339-5 · Cited by 402
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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