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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Oxytocin is also released somatodendritically to act within the SON and PVN to facilitate synchronous firing and pulsatile release during parturition and nursing.
“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
The ‘Oxytocin, Nucleus Accumbens, and the Mesolimbic Reward System’ section says oxytocin is released in the brain during parturition and nursing. The ‘Brain Circuits Regulating Maternal Motivation in Rats’ section links PVN oxytocin neurons to stimulation associated with birth and suckling. Neither passage establishes somatodendritic release within the SON and PVN or its proposed role in synchronous firing and pulsatile release; no page numbers were provided in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measuredAnimal and human studies indicate that similar neural systems and behavioral patterns underpin the parent-infant and pair bonds.
“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]
Central oxytocin signalling is crucial for the onset of maternal nurturing behaviour in rats.
“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 monogamous prairie voles, oxytocin and vasopressin interact with the dopamine system to facilitate pair bond formation between mates.
“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]
Oxytocin receptor signaling influences several social behaviors in animals, including maternal care and bonding, social reward and gregariousness, social recognition, and pair bonding in monogamous species.
“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]
The mother-infant bond is the evolutionary and neurobiological origin for the capacity to form adult social bonds in species that form bonds between mates, like humans.
“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
NE plays a critical role in bond formation in numerous species, suggesting it is a phylogenetically conserved system.
“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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Self-citationExperience with pups sustains maternal responding in postpartum rats
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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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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
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The roles of accumbal dopamine D1 and D2 receptors in maternal memory in rats.
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A developmental and component analysis of active sleep
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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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Self-citationMaternal Behavior: Neural Circuits, Stimulus Valence, and Motivational Processes
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Self-citationReproductive experience and activation of maternal memory.
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A role for the ventral pallidum in context‐induced and primed reinstatement of alcohol seeking
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Arginine vasopressin V1a receptor antagonist impairs maternal memory in rats
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- Numan M Fleming AS Levy F 2006 Maternal behavior Neill JD Physiology of Reproduction 2 Academic Press San Diego 1921 1993
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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 · see citing works
The Neurobiology of Human Attachments
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Oxytocin-dependent consolation behavior in rodents
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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 487 · see citing works
“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 · see citing works
The neural mechanisms and circuitry of the pair bond
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Self-citationWhat is resilience: an affiliative neuroscience approach
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“Work in rats has demonstrated that central OT signalling is crucial for the onset of maternal nurturing behaviour (1,2).”
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Oxytocin and early parent-infant interactions: A systematic review
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“The 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).”
Self-citationJohnson, Z. V., Walum, H., Jamal, Y. A., Xiao, Y., Keebaugh, A. C., Inoue, K., & Young, L. J. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.11.011 · Cited by 190 · see citing works
Self-citationDopamine in the medial amygdala network mediates human bonding
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The Use of Oxytocin to Improve Feeding and Social Skills in Infants With Prader–Willi Syndrome
Tauber, M., Boulanouar, K., Diene, G., Çabal-Berthoumieu, S., Ehlinger, V., Fichaux-Bourin, P., Molinas, C., Faye, S., Valette, M., Pourrinet, J., et al. (2017) · PEDIATRICS · doi:10.1542/peds.2016-2976 · Cited by 179 · see citing works
The neural mechanisms and consequences of paternal caregiving
Feldman, R., Braun, K., & Champagne, F. A. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0124-6 · Cited by 168 · see citing works
Walter, M. H., Abele, H., & Plappert, C. F. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.742236 · Cited by 186 · see citing works
Oxytocin and Social Relationships: From Attachment to Bond Disruption
Bosch, O. J., & Young, L. J. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_10 · Cited by 162 · see citing works
Self-citationPet Face: Mechanisms Underlying Human-Animal Relationships
Borgi, M., & Cirulli, F. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.00298 · Cited by 161 · see citing works
Lonstein, J. S., Lévy, F., & Fleming, A. S. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.06.011 · Cited by 151 · see citing works
The neurobiology of parenting: A neural circuit perspective
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Perry, R. E., Blair, C., & Sullivan, R. M. (2017) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2017.04.022 · Cited by 127 · see citing works
Overview of human oxytocin research
Kendrick, K. M., Guastella, A. J., & Becker, B. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_19 · Cited by 121 · see citing works
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Hormonal contraceptives suppress oxytocin-induced brain reward responses to the partner’s face
Scheele, D., Plota, J., Stoffel-Wagner, B., Maier, W., & Hurlemann, R. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv157 · Cited by 116 · see citing works
“Thus, our observation that OXT contributes to pair-bonding behavior in both men and women lends support to the notion that human pair-bonding behavior may have evolved from the evolutionarily older mother-infant bonding (Numan and Young, 2015).”
BackgroundOxytocin receptors modulate a social salience neural network in male prairie voles
Johnson, Z. V., Walum, H., Xiao, Y., Riefkohl, P. C., & Young, L. J. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.10.009 · Cited by 113 · see citing works
Self-citationHormone-mediated neural remodeling orchestrates parenting onset during pregnancy
Ammari, R., Monaca, F., Cao, M., Nassar, E., Wai, P. T., Grosso, N. A. D., Lee, M., Borak, N., Schneider-Luftman, D., & Kohl, J. (2023) · Science · doi:10.1126/science.adi0576 · Cited by 114 · see citing works
Perception of social synchrony induces mother–child gamma coupling in the social brain
Levy, J., Goldstein, A., & Feldman, R. (2017) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsx032 · Cited by 109 · see citing works
Song, Z., Borland, J. M., Larkin, T. E., O’Malley, M., & Albers, H. E. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.09.001 · Cited by 101 · see citing works
Hrdy, S. B. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.10.016 · Cited by 101 · see citing works
Proximate and Ultimate Perspectives on Romantic Love
Bode, A., & Kushnick, G. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.573123 · Cited by 106 · see citing works
Role of oxytocin in the control of stress and food intake
Onaka, T., & Takayanagi, Y. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12700 · Cited by 98 · see citing works
Oxytocin and Parental Behaviors
Yoshihara, C., Numan, M., & Kuroda, K. O. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_11 · Cited by 102 · see citing works
Self-citationOpendak, M., Gould, E., & Sullivan, R. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2017.02.002 · Cited by 94 · see citing works
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How the brain codes intimacy: The neurobiological substrates of romantic touch
Kreuder, A.-K., Scheele, D., Wassermann, L., Wollseifer, M., Stoffel-Wagner, B., Lee, M. R., Hennig, J., Maier, W., & Hurlemann, R. (2017) · Human Brain Mapping · doi:10.1002/hbm.23679 · Cited by 89 · see citing works
Do Pregnancy-Induced Brain Changes Reverse? The Brain of a Mother Six Years after Parturition
Martínez‐Garcia, M., Paternina-Die, M., Barba‐Müller, E., de Blas, D. M., Beumala, L., Cortizo, R., Pozzobon, C., Vidal, L. M., Fernández‐Pena, A., Picado, M., et al. (2021) · Brain Sciences · doi:10.3390/brainsci11020168 · Cited by 86 · see citing works
Synchronous caregiving from birth to adulthood tunes humans’ social brain
Ulmer-Yaniv, A., Salomon, R., Waidergoren, S., Shimon-Raz, O., Djalovski, A., & Feldman, R. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2012900118 · Cited by 81 · see citing works
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Self-citationSpecific maternal brain responses to their own child’s face: An fMRI meta-analysis
Rigo, P., Kim, P., Esposito, G., Putnick, D. L., Venuti, P., & Bornstein, M. H. (2018) · Developmental Review · doi:10.1016/j.dr.2018.12.001 · Cited by 76 · see citing works
Testosterone, oxytocin, and the development of human parental care
Gordon, I., Pratt, M., Bergunde, K., Zagoory‐Sharon, O., & Feldman, R. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.05.016 · Cited by 75 · see citing works
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Thalamic integration of social stimuli regulating parental behavior and the oxytocin system
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“The BLA has been proposed as a key brain region regulating pair bonding as well (Numan and Young, 2016; Walum and Young, 2018).”
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- 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 · 2015: 10
- 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
- Social Sciences › Psychology › Social Psychology › 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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