The neurobiology of pair bonding.
Abstract
A neurobiological model for pair-bond formation has emerged from studies in monogamous rodents. The neuropeptides oxytocin and vasopressin contribute to the processing of social cues necessary for individual recognition. Mesolimbic dopamine is involved in reinforcement and reward learning. Concurrent activation of neuropeptide and dopamine receptors in the reward centers of the brain during mating results in a conditioned partner preference, observed as a pair bond. Differential regulation of neuropeptide receptor expression may explain species differences in the ability to form pair bonds. These and other studies discussed here have intriguing implications for the neurobiology of social attachment in our own species.
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Meta-analyses and systematic reviews indicate that a range of common therapies can be effective in relieving couple distress in many situations.
“Meta-analyses and systematic reviews indicate that a range of common therapies can indeed be effective in relieving couple distress in many situations [26, 27].”
From Could intranasal oxytocin be used to enhance relationships? Research imperatives, clinical policy, and ethical considerations (2013) · cites this paper as [26]
Oxytocin (OXT) is a key modulator of pair-bonding in men.
“The hypothalamic peptide oxytocin (OXT) has been identified as a key modulator of pair-bonding in men, but its effects in women are still elusive.”
From Hormonal contraceptives suppress oxytocin-induced brain reward responses to the partner’s face (2016) · cites this paper as Young and Wang, 2004
A study injecting 3H-leucine into the SON found multiple extrahypothalamic projections, including olfactory bulb, amygdala, cingulum, and locus coeruleus.
“A study injecting 3H-leucine into the SON found multiple extrahypothalamic projections, including olfactory bulb, amygdala, cingulum, and locus coeruleus [140].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [140]
Species-specific differences in neural oxytocin receptor distributions can reflect the social organisation of the species.
“which suggests that species-specific differences in neural distributions of OXTR can reflect the social organisation of the species (20,21).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [20]
OXTR signaling in the nucleus accumbens is required for mating-induced partner preference formation in prairie voles.
“OXTR signaling in the NAcc is required for mating-induced partner preference formation, a laboratory proxy of pair bonding (6).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [6]
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 [6]
In prairie voles, OXTR is enriched in mesolimbic reward regions including the nucleus accumbens and prefrontal cortex, which are part of a neural network for pair bonding.
“In a socially monogamous rodent, the prairie vole (Microtus ochrogaster), OXTR is enriched in important MLR regions such as the nucleus accumbens (NAcc) and prefrontal cortex (PFC) that constitute part of a neural network for pair bonding (6, 8, 34).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [6]
OXTR density is much higher in the nucleus accumbens of prairie voles than in promiscuous vole species.
“OXTR density is much higher in the NAcc of prairie voles than promiscuous vole species”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [6]
The interface between oxytocin and the dopaminergic reward system may contribute to the success of mother-infant and pair-bonding processes.
“It is thought that the interface between oxytocin and the dopaminergic reward system may contribute to the success of mother-infant and pair-bonding processes [18,[75][76][77].”
From Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees (2014) · cites this paper as [76]
Arginine vasopressin (AVP) and oxytocin (OT) are key neuropeptides that facilitate social communication, affiliative behaviors and social cognition across mammals.
“Our first studies of the role of the AVPR1a gene in social cognition exemplified by a simple laboratory paradigm converges with a wide range of both animal and human experimentation showing that arginine vasopressin (AVP) and the closely related oxytocin (OT) are key neuropeptides that facilitate social communication, affiliative behaviors and social cognition across mammals [6], [7] .”
From The oxytocin receptor (OXTR) contributes to prosocial fund allocations in the dictator game and the social value orientations task (2009) · cites this paper as [7]
Meadow voles and montane voles do not readily form social bonds.
“By contrast, other related vole species such as the meadow vole (M. pennsylvanicus) and the montane vole (M. montanus) are relatively asocial and do not readily form social bonds, providing a useful point of comparison for identifying neurobiological and genetic systems leading to diversity in social behaviors [2].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [2]
Meadow voles and montane voles are relatively asocial.
“By contrast, other related vole species such as the meadow vole (M. pennsylvanicus) and the montane vole (M. montanus) are relatively asocial and do not readily form social bonds, providing a useful point of comparison for identifying neurobiological and genetic systems leading to diversity in social behaviors [2].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [2]
Socially monogamous male prairie voles have high densities of AVPR1A binding in the ventral pallidum, while non-monogamous vole species do not.
“For example, socially monogamous male prairie voles have high densities of AVPR1A binding in the ventral pallidum, a major output of the NAcc, while non-mongamous vole species do not [2].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [2]
The prairie vole is a socially monogamous mammal that has provided remarkable insights into the neural and neurogenetic mechanisms of social attachments.
“One of these socially monogamous mammals that has provided remarkable insights into the neural and neurogenetic mechanisms of social attachments is the prairie vole (Microtus ochrogaster)”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Young and Wang 2004
V1aR signaling in the ventral pallidum and lateral septum promote partner preferences, while pair bond-induced aggression is mediated by V1aR in the lateral hypothalamus.
“V1aR signaling in the ventral pallidum and LS promote partner preferences (149), while pair bond-induced aggression is mediated by V1aR in the lateral hypothalamus (43,150).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [149]
Animal research has documented that oxytocin is primarily a social bonding hormone that activates socio-emotional neural pathways in the brain.
“Because animal research has documented that OT is primarily a social bonding hormone that activates socio-emotional neural pathways in the brain 22,23 , we would also expect the effect of OT in humans to be limited to social situations where initiating or establishing partnership is important to realize synergy.”
From A registered replication study on oxytocin and trust (2020) · cites this paper as [23]
OT has a crucial function as a female hormone in labor, bonding and parenting in human and non-human mammals.
“this finding fits with the crucial function of OT as a female hormone in labor, bonding and parenting both in human- [54], [4] and non-human mammals [55]”
From A direct examination of the effect of intranasal administration of oxytocin on approach-avoidance motor responses to emotional stimuli (2013) · cites this paper as [55]
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“The neuropeptide oxytocin (OT) has received considerable attention in preclinical and human research for its role in mediating social affiliation, mother–child attachment, social support and trust (Young and Wang, 2004; Kosfeld et al., 2005).”
BackgroundOxytocin and vasopressin in the human brain: social neuropeptides for translational medicine
Meyer-Lindenberg, A., Domes, G., Kirsch, P., & Heinrichs, M. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3044 · Cited by 1,688 · see citing works
“— which is in line with animal studies indicating that central OXT facilitates pair bonding behaviou”
ResultOxytocin, vasopressin, and the neurogenetics of sociality
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Natural neural projection dynamics underlying social behavior
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“In rodents, most studies on social behavior have focused on socio-sexual behaviors, such as pair bonding and behaviors related to sexual competition (Aragona et al., 2006; Curtis and Wang, 2005; Gingrich et al., 2000; Leypold et al., 2002; Liu and Wang, 2003; Young et al., 2001; Young and Wang, 2004).”
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Oxytocin improves “mind-reading” in humans
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“Evidence for the key role of oxytocin in prosocial behavior and affiliation has come primarily from studies in animals (Bartz and Hollander, in press; Carter 1998; Ferguson et al 2000; Young and Wang 2004).”
Oxytocin shapes the neural circuitry of trust and trust adaptation in humans
Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U., & Fehr, E. (2008) · Neuron · doi:10.1016/j.neuron.2008.04.009 · Cited by 1,258 · see citing works
Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin
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Lending a Hand: Social Regulation of the Neural Response to Threat
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The oxytocin receptor: from intracellular signaling to behavior
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The Vertebrate mesolimbic reward system and social behavior network: A comparative synthesis
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“During pairbond formation in monogamous female voles (Microtus ochrogaster), a process involving the mesolimbic reward system (Young and Wang, 2004), neuronal activity as measured by c-fos induction increases in the BNST (Curtis and Wang, 2003).”
BackgroundInfluentialDendritic peptide release and peptide-dependent behaviours
Ludwig, M., & Leng, G. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1845 · Cited by 945 · see citing works
“These effects seem to be consistent with observations that indicate general effects of oxytocin on social behaviour”
ResultThe Social Salience Hypothesis of Oxytocin
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Social Bonds and Posttraumatic Stress Disorder
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“More recently, OT and AVP have been identified as essential chemical mediators of social bonding in animals (Insel 2003, Keverne & Curley 2004, Young & Wang 2004).”
BackgroundHuman fronto–mesolimbic networks guide decisions about charitable donation
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Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior
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“We hypothesize that pair bond formation is the result of an association between the rewarding mating experience and the olfactory signature of the partner [55].”
BackgroundThe Neurobiology of Human Attachments
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“Neural models for parental care in rats are indicated by broken black lines and for pair bonding formation in prairie voles by dotted black lines [10,19,80].”
Oxytocin, vasopressin, and human social behavior
Heinrichs, M., von Dawans, B., & Domes, G. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.005 · Cited by 799 · see citing works
“005 E D P R O O F studies have previously shown an association between the AVPR1a receptor gene and autism [90,143,156], as well as partner preference in the male prairie vole [165].”
BackgroundThe adaptive value of sociality in mammalian groups
Silk, J. B. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1994 · Cited by 797 · see citing works
“…to form and maintain social bonds plays an integral role in functional interpretations of many aspects of behaviour, such as reconciliation in monkeys (Aureli & de Waal 2000), coalitions in cetaceans (Connor et al. 1998; Connor 2007) and pair bonding in microtine rodents (Young & Wang 2004).”
BackgroundOxytocin attenuates amygdala responses to emotional faces regardless of valence
Domes, G., Heinrichs, M., Gläscher, J., Büchel, C., Braus, D. F., & Herpertz, S. C. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.03.025 · Cited by 774 · see citing works
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Oxytocin-gaze positive loop and the coevolution of human-dog bonds
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Brain oxytocin: A key regulator of emotional and social behaviours in both females and males
Neumann, I. D. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01726.x · Cited by 743 · see citing works
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“For instance, there is some evidence that AVP plays particular roles in prosocial behavior in males, and it has also been shown to mediate aggressive behaviors and territoriality in many species (Caldwell et al., 2008; Donaldson & Young, 2008; Young & Wang, 2004).”
BackgroundOxytocin-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 · see citing works
“In prairie voles, this is sufficient time for a pair bond to form (41).”
BackgroundPfaus, J. G. (2009) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2009.01309.x · Cited by 678 · see citing works
CD38 is critical for social behaviour by regulating oxytocin secretion
Jin, D., Liu, H.-X., Hirai, H., Torashima, T., Nagai, T., Lopatina, O., Shnayder, N. A., Yamada, K., Noda, M., Seike, T., et al. (2007) · Nature · doi:10.1038/nature05526 · Cited by 665 · see citing works
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Gating of social reward by oxytocin in the ventral tegmental area
Hung, L. W., Neuner, S., Polepalli, J. S., Beier, K. T., Wright, M., Walsh, J. J., Lewis, E. M., Luo, L., Deisseroth, K., Dölen, G., et al. (2017) · Science · doi:10.1126/science.aan4994 · Cited by 578 · see citing works
Social buffering: relief from stress and anxiety
Kikusui, T., Winslow, J. T., & Mori, Y. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1941 · Cited by 635 · see citing works
“These stimulations increase oxytocin release in mesocorticolimbic pathways; blocking the oxytocin neurotransmission abolished social attachment, indicating that an oxytocin pathway is indispensable for attachment (Insel et al. 1997; Kendrick 2004; Wang & Aragona 2004; Young & Wang 2004).”
BackgroundNeuropeptidergic regulation of affiliative behavior and social bonding in animals
Lim, M. M., & Young, L. J. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.028 · Cited by 624 · see citing works
“…vole animal model of social attachment is complemented by the natural comparison of two other vole species, the non-monogamous montane and meadow voles (Microtus montanus and Microtus pennsylvanicus), in addition to the monogamous pine vole (Microtus pinetorum) (reviewed in Young and Wang, 2004).”
BackgroundInfluentialFries, A. B. W., Ziegler, T. E., Kurian, J. R., Jacoris, S., & Pollak, S. D. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504767102 · Cited by 570 · see citing works
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“Furthermore, the strong impact of OT on female social behavior (3), and the disproportionately high risk of men for social disorders (80), suggest sexdependent genotype effects at the neural systems level, particularly as emotional deficits have been previously associated with male, but not female, rs53576A carriers (…”
BackgroundClinical and Investigative Medicine
Silverman, M. P., Siminovitch, K. A., McGugan, S., Bergeron, M. G., Cook, D. J., Eaves, A. C., Grover, S. A., Stanbrook, M. B., & Finnigan, A. (2006) · Cited by 570 · see citing works
Sexual differentiation of the vertebrate nervous system
Morris, J. A., Jordan, C. L., & Breedlove, S. M. (2004) · Nature Neuroscience · doi:10.1038/nn1325 · Cited by 627 · see citing works
“Sexual differentiation of the brain in adulthood Arginine vasopressin fibers innervate the septal region in rats and contribute to pair bonding and parental behavior in a variety of rodents (see accompanying revie”
BackgroundEffects of intranasal oxytocin on emotional face processing in women
Domes, G., Lischke, A., Berger, C., Grossmann, A., Hauenstein, K., Heinrichs, M., & Herpertz, S. C. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.06.016 · Cited by 521 · see citing works
“OXT is especially involved in mating, pair bonding, and mother—offspring attachment in mammals (Insel and Young, 2001; Young and Wang, 2004).”
BackgroundDitzen, B., Neumann, I. D., Bodenmann, G., von Dawans, B., Turner, R. A., Ehlert, U., & Heinrichs, M. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.03.011 · Cited by 525 · see citing works
“, 2000a) and promotes social behavior, including pair bonding, maternal behavior, sexual behavior, and social attachment in animals (Carter, 1998; Uvnas-Moberg, 1998a; Insel and Young, 2001; Pedersen and Boccia, 2003; Young and Wang, 2004).”
BackgroundLower CSF oxytocin concentrations in women with a history of childhood abuse
Heim, C., Young, L. J., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2009) · Molecular Psychiatry · doi:10.1038/mp.2008.112 · Cited by 518 · see citing works
“3 The neuropeptide oxytocin (OT), found in the hypothalamus and limbic brain regions, has received considerable attention in preclinical and human research for its role in mediating social affiliation, attachment, social support, maternal behavior and trust”
BackgroundVasopressin: Behavioral roles of an “original” neuropeptide
Caldwell, H. K., Lee, H.-J., Macbeth, A. H., & Young, W. S. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.10.007 · Cited by 504 · see citing works
“For a more in depth review on pair bonding and its genetic regulation, see (Insel, 2003; Aragona and Wang, 2004; Young and Wang, 2004; Lim et al., 2004a; Young et al., 2005; Hammock and Young, 2006; Lim and Young, 2006; Nair and Young, 2006).”
BackgroundAragona, B. J., Liu, Y., Yu, Y. J., Curtis, J. T., Detwiler, J. M., Insel, T. R., & Wang, Z. (2006) · Nature Neuroscience · doi:10.1038/nn1613 · Cited by 473 · see citing works
“has proven to be an excellent model for neurobiological investigations of pair bondin”
BackgroundSelf-citationNeuropeptides and social behaviour: effects of oxytocin and vasopressin in humans
HEINRICHS, M., & DOMES, G. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00428-7 · Cited by 479 · see citing works
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“…in other forms of reward processing (e.g., food, drugs, etc.), underlie social processes such as pair-bonding [Young, Murphy Young, & Hammock, 2005; Young & Wang, 2004] and mother–offspring bonding [Levy, Kendrick, Goode, Guevara-Guzman, & Keverne, 1995] in small rodents [Febo, Numan, & Ferris,…”
Oxytocin and the development of parenting in humans
Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.02.005 · Cited by 469 · see citing works
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“, montane voles (Microtus montanus), meadow voles (Microtus pennsylvanicus), and prairie voles (Microtus ochrogaster) (2).”
BackgroundSmall Bioactive Peptides for Biomaterials Design and Therapeutics
Hamley, I. W. (2017) · Chemical Reviews · doi:10.1021/acs.chemrev.7b00522 · Cited by 461 · see citing works
Neural correlates of long-term intense romantic love
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“OT and AVP have been shown to play a critical role in the regulation of social behaviors (Insel et al., 1994) and monogamous pair-bonding in rodent mammals (Young et al., 2001; Lim and Young, 2004; Young and Wang, 2004).”
BackgroundSbarra, D. A., & Hazan, C. (2008) · Personality and Social Psychology Review · doi:10.1177/1088868308315702 · Cited by 427 · see citing works
“In the remainder of this section, we describe this attachment formation process and the resulting physiological coregulation in detail.”
InfluentialThe neurobiology of pair bonding: Insights from a socially monogamous rodent
Young, K. A., Gobrogge, K. L., Liu, Y., & Wang, Z. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.07.006 · Cited by 389 · see citing works
“DAergic cells in the ventral tegmental area (VTA) project to the NAcc and prefrontal cortex (PFC), as well as other forebrain regions.”
InfluentialThe microbiota-gut-brain axis: neurobehavioral correlates, health and sociality
Montiel-Castro, A. J., González-Cervantes, R. M., Bravo-Ruiseco, G., & Pacheco-López, G. (2013) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2013.00070 · Cited by 413 · see citing works
“…stimulate the production of oxytocin, vasopressin or endorphines: neuropeptide mechanisms underlying social-bonding processes in different species (Young and Wang, 2004; Dunbar, 2010); last but not least, (3) during ventroventral contact, mouth-to-mouth kissing can act as a means for the…”
BackgroundBosch, O. J., & Neumann, I. D. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.11.002 · Cited by 400 · see citing works
The human sexual response cycle: Brain imaging evidence linking sex to other pleasures
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“Animal studies have convincingly demonstrated an interaction between sexual activity, the release of the anterior pituitary neuropeptides oxytocin and vasopressin, and pair bond formation (Young and Wang, 2004).”
BackgroundSocial brain, social dysfunction and social withdrawal
Porcelli, S., van der Wee, N. J. A., van der Werff, S. J., Aghajani, M., Glennon, J. C., van Heukelum, S., Mogavero, F., Lobo, A., Olivera, F. J. N., Lobo, E., et al. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.012 · Cited by 397 · see citing works
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The neural mechanisms and circuitry of the pair bond
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“In non-human mammals, research shows that central administration of OT agonists enhances social recognition, memory for peers, the development of partner preference, and partner bonding (for a review see (Young and Wang, 2004)).”
BackgroundGuastella, A. J., Howard, A. L., Dadds, M. R., Mitchell, P., & Carson, D. S. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.01.005 · Cited by 366 · see citing works
Oxytocin, motivation and the role of dopamine
Love, T. M. (2014) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.06.011 · Cited by 369 · see citing works
“Multiple lines of evidence indicate oxytocin is also key neurobiological substrate underlying the development of partner preferences (see review Young and Wang, 2004).”
Oxytocin–dopamine interactions mediate variations in maternal behavior in the rat
Shahrokh, D. K., Zhang, T.-Y., Diorio, J., Gratton, A., & Meaney, M. J. (2010) · Endocrinology · doi:10.1210/en.2009-1271 · Cited by 366 · see citing works
Numan, M., & Young, L. J. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.015 · Cited by 355 · see citing works
“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-citationFrye, C., Bo, E., Calamandrei, G., Calzà, L., Dessì‐Fulgheri, F., Fernández, M., Fusani, L., Kah, O., Kajta, M., Le Page, Y., et al. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02229.x · Cited by 431 · see citing works
“OT is involved in social recognition and maternal behavior (116, 117).”
Stress, social behavior, and resilience: Insights from rodents
Beery, A. K., & Kaufer, D. (2014) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.10.004 · Cited by 373 · see citing works
“Vasopressin activity has been associated with aggression, anxiety, and social behavior (reviewed in Kelly and Goodson, 2014), as well partner preference formation in male prairie voles (Cho et al., 1999; Young and Wang, 2004).”
BackgroundReexamining Human Origins in Light of Ardipithecus ramidus
Lovejoy, C. O. (2009) · Science · doi:10.1126/science.1175834 · Cited by 356 · see citing works
Lerer, E., Levi, S., Salomon, S., Darvasi, A., Yirmiya, N., & Ebstein, R. P. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002087 · Cited by 349 · see citing works
Oxytocin enhances the encoding of positive social memories in humans.
Guastella, A. J., Mitchell, P. B., & Mathews, F. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.02.008 · Cited by 352 · see citing works
The developmental neurobiology of autism spectrum disorder
DiCicco-Bloom, E., Lord, C., Zwaigenbaum, L., Courchesne, E., Dager, S. R., Schmitz, C., Schultz, R. T., Crawley, J., & Young, L. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1712-06.2006 · Cited by 434 · see citing works
“The monogamous prairie vole is highly social, craves social contact, and forms enduring social bonds with its mate (Carter et al., 1995; Young and Wang, 2004).”
InfluentialDe Vries, G. J., & Panzica, G. C. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.050 · Cited by 346 · see citing works
“These functions include, for example, learning and memory (de Wied et al., 1993), reproductive and other social behaviors (Goodson and Bass, 2001; Panzica et al., 2002; Rose and Moore, 2002; Young and Wang, 2004).”
BackgroundConley, T. D., Moors, A. C., Matsick, J. L., & Ziegler, A. (2012) · Analyses of Social Issues and Public Policy · doi:10.1111/j.1530-2415.2012.01286.x · Cited by 344 · see citing works
“Further, words such as “infidelity” and “adultery” are frequently used to describe CNM relationships; these terms, of course, discount the possibility that extradyadic relationships may have been agreed upon by both members of a couple (Finch, 2009; Young & Wang, 2004).”
BackgroundDopaminergic-neuropeptide interactions in the social brain
Skuse, D. H., & Gallagher, L. (2009) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2008.09.007 · Cited by 340 · see citing works
An integrative theoretical framework for understanding sexual motivation, arousal, and behavior
Toates, F. (2009) · Journal of Sex Research · doi:10.1080/00224490902747768 · Cited by 339 · see citing works
“For example, the links between attachment and sexual motivations have been recognized (Diamond, 2003), and animal models of this have been proposed (Young & Wang, 2004).”
BackgroundRoss, H. E., Freeman, S. M., Spiegel, L. L., Ren, X., Terwilliger, E. F., & Young, L. J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5039-08.2009 · Cited by 322 · see citing works
“Species differences in OTR density in the NAcc have been associated with species differences in mating strategy (social monogamy vs polygamy) and alloparental behavior, suggesting that variation in OTR receptor expression may underlie species differences in social organization and behavior (Insel et al., 1991; Young a…”
BackgroundCharacterization of the oxytocin system regulating affiliative behavior in female prairie voles
Ross, H. E., Cole, C. D., Smith, Y., Neumann, I. D., Landgraf, R., Murphy, A. Z., & Young, L. J. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.05.055 · Cited by 309 · see citing works
The role of the striatum in social behavior
Báez-Mendoza, R., & Schultz, W. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00233 · Cited by 312 · see citing works
“As noted by Wang and Young (Lim et al., 2004b; Young and Wang, 2004), the cellular mechanism might be the co-activation of D2-expressing accumbal neurons by vasopressin and/or oxytocin.”
BackgroundA. Bartz, J., & Hollander, E. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.018 · Cited by 311 · see citing works
“For example, studies show that prairie voles have high levels of oxytocin and vasopressin receptors in the prelimbic cortex, nucleus accumbens and ventral pallidum–regions involved in the mesolimbic dopamine reward system–and some researchers theorize that pair-bonding may be a specialized form of conditioned reward l…”
BackgroundBurkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307 · see citing works
“Figure adapted from Young and Wang ( 2004 ) lower than in prairie voles ( Insel et al .”
Psychobiology of social support: The social dimension of stress buffering
Ditzen, B., & Heinrichs, M. (2014) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-139008 · Cited by 298 · see citing works
“…animal studies showing an involvement of the neuropeptides oxytocin and vasopressin in social behavior, anxiety, and stress regulation (Insel, 2010; Young & Wang, 2004), there is growing literature suggesting that these very same mechanisms are involved in the regulation of human sociality…”
Biased Oxytocinergic Modulation of Midbrain Dopamine Systems
Xiao, L., Priest, M. F., Nasenbeny, J., Lu, T., & Kozorovitskiy, Y. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.003 · Cited by 292 · see citing works
“A key example is Oxt release into the vStr, which promotes affiliative social behavior (Liu and Wang, 2003; Shahrokh et al., 2010; Young and Wang, 2004).”
Bethlehem, R. A. I., van Honk, J., Auyeung, B., & Baron-Cohen, S. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.10.011 · Cited by 285 · see citing works
“…Bale et al., 1995 The most obvious link between the dopamine (DA) and OT system stems from the fact that, at least in humans, social affiliative behaviour (which is modulated by OT) is accompanied by modulation of dopaminergic reward pathways (Skuse and Gallagher, 2009; Young and Wang, 2004).”
BackgroundOxytocin, vasopressin and pair bonding: implications for autism
Hammock, E. A. D., & Young, L. J. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1939 · Cited by 289 · see citing works
“…the brain circuits involved in motivation and reward, it has been hypothesized that both oxytocin and vasopressin may be facilitating affiliation and social attachment in monogamous species by modulating these reward pathways (Insel & Young 2001; Young et al. 2001; Insel 2003; Young & Wang 2004).”
BackgroundAlbers, H. E. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.10.007 · Cited by 288 · see citing works
“For example, non-monogomous male Montane voles have few V1a receptors in the ventral pallidum (VP) compared to monogamous Prairie voles, and induction of V1a receptors in the VP of Montane voles by viral vector gene transfer results in pair bonding similar to that seen in Prairie voles (Young and Wang, 2004).”
ResultMother–infant bonding and the evolution of mammalian social relationships
Broad, K. D., Curley, J. P., & Keverne, E. B. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1940 · Cited by 283 · see citing works
“Both pregnancy and oestrus provide the endocrine context for the synthesis of OT and the OT receptors (Thomas et al. 1996; Bale & Dorsa 1997; Young et al. 1997).”
BackgroundNeural mechanisms of social homeostasis
Matthews, G. A., & Tye, K. M. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14016 · Cited by 273 · see citing works
Oxytocin enhances the experience of attachment security
Buchheim, A., Heinrichs, M., George, C., Pokorny, D., Koops, E., Henningsen, P., O’Connor, M.-F., & Gündel, H. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.04.002 · Cited by 277 · see citing works
“…mammals, receptors for the neuropeptide oxytocin are distributed in various brain regions that are associated with the ability to form normal social attachments and affiliation, including parental care, pair bonding, and social memory (Carter, 1998; Uvnas-Moberg, 1998; Young and Wang, 2004).”
Dabrowska, J., Hazra, R., Ahern, T. H., Guo, J.-D., McDonald, A. J., Mascagni, F., Muller, J. F., Young, L. J., & Rainnie, D. G. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.03.003 · Cited by 274 · see citing works
“Hence, OT is known to facilitate partner preference formation (Insel and Hulihan, 1995), and microinjection of CRF into the NAc accelerates partner preference formation in male prairie voles, an effect mediated by CRFR2 (Young and Wang, 2004; Lim and Young, 2006).”
Self-citationIsrael, S., Lerer, E., Shalev, I., Uzefovsky, F., Riebold, M., Laiba, E., Bachner-Melman, R., Maril, A., Bornstein, G., Knafo, A., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005535 · Cited by 278 · see citing works
“Our first studies of the role of the AVPR1a gene in social cognition exemplified by a simple laboratory paradigm converges with a wide range of both animal and human experimentation showing that arginine vasopressin (AVP) and the closely related oxytocin (OT) are key neuropeptides that facilitate social communication,…”
ResultThe prairie vole: An emerging model organism for understanding the social brain
McGraw, L. A., & Young, L. J. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2009.11.006 · Cited by 276 · see citing works
The Placebo Effect in Pain Therapies
Colloca, L. (2018) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010818-021542 · Cited by 290 · see citing works
The animal and human neuroendocrinology of social cognition, motivation and behavior
McCall, C., & Singer, T. (2012) · Nature Neuroscience · doi:10.1038/nn.3084 · Cited by 273 · see citing works
de Oliveira‐Souza, R., Hare, R. D., Bramati, I. E., Garrido, G. J., Ignácio, F. A., Tovar-Moll, F. F., & Moll, J. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2007.12.054 · Cited by 269 · see citing works
“This hypothesis gains further support from the high receptor concentrations in this region for neuropeptides such as oxytocin (Freedman et al., 2000; Young and Wang, 2004), which are known to enhance trust and cooperation among humans (Zak et al.”
Veenema, A. H., Bredewold, R., & Neumann, I. D. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.02.008 · Cited by 263 · see citing works
“In support, across species, it has been found that the AVP system may predominantly regulate male social behaviors, while the OXT system is primarily required for female social behaviors (de Vries and Miller, 1998; Gimpl and Fahrenholz, 2001; Keverne and Curley, 2004; Lim et al., 2004; Young and Wang, 2004; Bielsky et…”
BackgroundJohnson, Z. V., & Young, L. J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.034 · Cited by 242 · see citing works
“…however, it is important to note that variation n region-specific OT- and AVP-like receptor expression has been inked to individual and/or species diversity in social behaviors in ultiple vertebrate lineages (Goodson et al., 2009; Okhovat et al., 015; Ophir et al., 2012; Young and Wang, 2004).”
Singer, T., Snozzi, R., Bird, G., Petrovic, P., Silani, G., Heinrichs, M., & Dolan, R. J. (2008) · Emotion · doi:10.1037/a0014195 · Cited by 248 · see citing works
“More specific, research has shown that it is associated with the ability to form social attachments and with affiliation, including parental care, pair bonding, sexual behavior, and social memory (Carter, 1998; Insel & Young, 2001; Lim & Young, 2006; Young & Wang, 2004 ).”
BackgroundMinagawa-Kawai, Y., Matsuoka, S., Dan, I., Naoi, N., Nakamura, K., & Kojima, S. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn081 · Cited by 273 · see citing works
“…responses around the aOFC area, which has also been shown to be the neural correlate of attachment in other animal studies of rhesus monkeys, rats, and voles (Young and Wang 2004; Moriceau and Sullivan 2005; Goursaud and Bachevalier 2006), supports the aforementioned interpretation in this study.”
Emotional endophenotypes in evolutionary psychiatry
Panksepp, J. (2006) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2006.01.004 · Cited by 246 · see citing works
“Still, animal studies affirm that remarkably complex social tendencies can be strongly influenced by single genes in creatures as diverse as flies (Demir and Dickson, 2005) and rodents (Young and Wang, 2004).”
BackgroundSocial reward among juvenile mice
Panksepp, J. B., & Lahvis, G. P. (2007) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2006.00295.x · Cited by 248 · see citing works
“…reward processes have nevertheless been shown in social contexts that include mating (Agmo & Gomez 1993; Drewett 1973), monogamous pair-bonding (Young & Wang 2004), aggression (Fish et al. 2005), maternal–infant attachment (Insel 2003; Lee et al. 1999) and rough-and-tumble play among…”
Background
- Authors
- Young, L. J., & Wang, Z.
- Affiliations
- Emory University (US)
- Florida State University (US)
- Corresponding author
- Young, Larry J
- Venue
- Nature Neuroscience
- Published
- 2004-09-26
- Volume
- 7
- Issue
- 10
- Pages
- 1048-1054
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2055445652
- Cited by
- 1,523
- References
- 76
- Citations by year
- 2026: 42 · 2025: 63 · 2024: 54 · 2023: 64 · 2022: 62 · 2021: 65 · 2020: 73 · 2019: 60 · 2018: 83 · 2017: 85 · 2016: 99 · 2015: 96 · 2014: 86 · 2013: 106 · 2012: 85
- FWCI
- 6.10
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- pair bonding, monogamy, oxytocin, vasopressin, mesolimbic dopamine system, reward learning, social attachment, individual recognition, social behavior
- MeSH terms
- Animals, Brain, Dopamine, Humans, Neural Pathways, Neuropeptides, Pair Bond, Reward, Receptors, Neuropeptide, Models, Animal
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