Anatomy and neurochemistry of the pair bond

Young, Larry J.; Murphy Young, Anne Z.; Hammock, Elizabeth A.D.

doi:10.1002/cne.20771

Cited by 163Neuroendocrine regulation and behaviorOlfactory and Sensory Function StudiesNeurotransmitter Receptor Influence on Behavior

Anatomy and neurochemistry of the pair bond

Young, Larry J., Murphy Young, Anne Z., Hammock, Elizabeth A.D.·2005·Journal of Comparative Neurology

DOI 10.1002/cne.20771

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Abstract

Studies in monogamous rodents have begun to elucidate the neural circuitry underlying the formation and maintenance of selective pair bonds between mates. This research suggests that at least three distinct, yet interconnected, neural pathways interact in the establishment of the pair bond. These include circuits involved in conveying somatosensory information from the genitalia to the brain during sexual activity, the mesolimbic dopamine circuits of reward and reinforcement, and neuropeptidergic circuits involved specifically in the processing of socially salient cues. Here we present an integrated description of the interaction of these circuits in a model of pair bond formation in rodents with a discussion of the implications of these findings for evolution, individual variation, and human bonding. J. Comp. Neurol. 493:51–57, 2005. © 2005 Wiley‐Liss, Inc.

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OT release induced by vaginocervical and nipple stimulation during human sex acts analogously to labor and nursing to induce bonding between sexual partners.
“This has contributed to the theory that the OT release induced by vaginocervical stimulation and nipple stimulation during human sex, acts analogous to labor and nursing, serves to induce bonding between sexual partners (Young et al 2005); and furthermore, that pair bonding is mediated by neural systems that were elaborated in evolution from circuits originally adapted for maternal behavior (Ross”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Young et al 2005
These studies support the hypothesis that OT release during human romantic activities induces formation of long-term bonds.
“These studies lend support to the hypothesis that OT release during human romantic activities serves to induce the formation of long-term bonds (Young et al 2005; Feldman 2012).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Young et al 2005

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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
Brain basis of early parent–infant interactions: psychology, physiology, and in vivo functional neuroimaging studies
Swain, J. E., Lorberbaum, J. P., Kose, S., & Strathearn, L. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2007.01731.x · Cited by 499 · see citing works
Reward processing in autism
Scott‐Van Zeeland, A. A., Dapretto, M., Ghahremani, D. G., Poldrack, R. A., & Bookheimer, S. Y. (2010) · Autism Research · doi:10.1002/aur.122 · Cited by 458 · see citing works
Pharmacologic rescue of impaired cognitive flexibility, social deficits, increased aggression, and seizure susceptibility in oxytocin receptor null mice: a neurobehavioral model of autism
Sala, M., Braida, D., Lentini, D., Busnelli, M., Bulgheroni, E., Capurro, V., Finardi, A., Donzelli, A., Pattini, L., Rubino, T., et al. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.12.022 · Cited by 375 · see citing works
Sex differences in the neural and behavioral response to intranasal oxytocin and vasopressin during human social interaction
Rilling, J. K., DeMarco, A. C., Hackett, P. D., Chen, X., Gautam, P., Stair, S., Haroon, E., Thompson, R., Ditzen, B., Patel, R., et al. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.09.022 · Cited by 343 · see citing works
“, 2006), along with evidence that AVP is more influential in males compared with females (Young et al., 2005), we did not expect AVP to augment activation in BNST, lateral septum and stria terminalis in women as it did in men.”
Background
Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity in men
Rilling, J. K., DeMarco, A. C., Hackett, P. D., Thompson, R., Ditzen, B., Patel, R., & Pagnoni, G. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.07.013 · Cited by 303 · see citing works
The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction
Burkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307 · see citing works
“This has contributed to the theory that the OT release induced by vaginocervical stimulation and nipple stimulation during human sex, which acts analogously to labor and nursing, serves to induce bonding between sexual partners (Young et al. 2005) and, furthermore, that pair bonding is mediated by neural systems that…”
Self-citation
Environmental Complexity and Social Organization Sculpt the Brain in Lake Tanganyikan Cichlid Fish
Pollen, A. A., Dobberfuhl, A., Scace, J., Igulu, M. M., Renn, S. C. P., Shumway, C. A., & Hofmann, H. A. (2007) · Brain Behavior and Evolution · doi:10.1159/000101067 · Cited by 294 · see citing works
The 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
Self-citation
Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles
Bales, K. L., Perkeybile, A. M., Conley, O. G., Lee, M. H., Guoynes, C. D., Downing, G. M., Yun, C. R., Solomon, M., Jacob, S., & Mendoza, S. P. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.08.025 · Cited by 265 · see citing works
The biology of paternal care in human and nonhuman primates
Fernandez-Duque, E., Valeggia, C. R., & Mendoza, S. P. (2009) · Annual Review of Anthropology · doi:10.1146/annurev-anthro-091908-164334 · Cited by 232 · see citing works
Who, what, where, when (and maybe even why)? How the experience of sexual reward connects sexual desire, preference, and performance
Pfaus, J. G., Kippin, T. E., Coria-Avila, G. A., Gelez, H., Afonso, V. M., Ismail, N., & Parada, M. (2012) · Archives of Sexual Behavior · doi:10.1007/s10508-012-9935-5 · Cited by 215 · see citing works
Anterior hypothalamic neural activation and neurochemical associations with aggression in pair-bonded male prairie voles
Gobrogge, K. L., Liu, Y., Jia, X., & Wang, Z. (2007) · Journal of Comparative Neurology · doi:10.1002/cne.21364 · Cited by 178 · see citing works
Consequences of Early Experiences and Exposure to Oxytocin and Vasopressin Are Sexually Dimorphic
Carter, C. S., Boone, E. M., Pournajafi-Nazarloo, H., & Bales, K. L. (2009) · Developmental Neuroscience · doi:10.1159/000216544 · Cited by 176 · see citing works
Intranasal administration of oxytocin: behavioral and clinical effects, a review
Veening, J. G., & Olivier, B. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.04.012 · Cited by 169 · see citing works
Oxytocin receptor density is associated with male mating tactics and social monogamy
Ophir, A. G., Gessel, A., Zheng, D.-J., & Phelps, S. M. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.007 · Cited by 161 · see citing works
Oxytocin and vasopressin effects on the neural response to social cooperation are modulated by sex in humans
Feng, C., Hackett, P. D., DeMarco, A. C., Chen, X., Stair, S., Haroon, E., Ditzen, B., Pagnoni, G., & Rilling, J. K. (2015) · Brain Imaging and Behavior · doi:10.1007/s11682-014-9333-9 · Cited by 157 · see citing works
The role of oxytocin in male and female reproductive behavior
Veening, J. G., A, T. R. D. J., Waldinger, M. D., Korte, S. M., & Olivier, B. (2014) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.07.045 · Cited by 156 · see citing works
Integrative Approaches Utilizing Oxytocin to Enhance Prosocial Behavior: From Animal and Human Social Behavior to Autistic Social Dysfunction
Yamasue, H., Yee, J. R., Hurlemann, R., Rilling, J. K., Chen, F. S., Meyer-Lindenberg, A., & Tost, H. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3327-12.2012 · Cited by 149 · see citing works
Neural Signatures of Autism Spectrum Disorders: Insights into Brain Network Dynamics
Hernandez, L. M., Rudie, J. D., Green, S. A., Bookheimer, S. Y., & Dapretto, M. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.172 · Cited by 141 · see citing works
Activation of μ-Opioid Receptors in the Dorsal Striatum is Necessary for Adult Social Attachment in Monogamous Prairie Voles
Burkett, J. P., Spiegel, L. L., Inoue, K., Murphy, A. Z., & Young, L. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.117 · Cited by 133 · see citing works
Self-citation
Neural mechanisms underlying the evolvability of behaviour
Katz, P. S. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0336 · Cited by 117 · see citing works
κ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance
Resendez, S. L., Kuhnmuench, M., Krzywosinski, T., & Aragona, B. J. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5779-11.2012 · Cited by 110 · see citing works
“The socially monogamous prairie vole (Microtus ochrogaster) is an excellent model system to study the neurobiology of social attachment (Young and Wang, 2004; Young et al., 2005; Aragona and Wang, 2009).”
Background
Oxytocin and appetite
LENG, G., ONAKA, T., CAQUINEAU, C., SABATIER, N., TOBIN, V, & TAKAYANAGI, Y. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00413-5 · Cited by 112 · see citing works
Neuroscientific approaches and applications within anthropology
Rilling, J. K. (2008) · American Journal of Physical Anthropology · doi:10.1002/ajpa.20947 · Cited by 112 · see citing works
Neural correlates of pair-bonding in a monogamous primate
Bales, K. L., Mason, W. A., Catana, C., Cherry, S. R., & Mendoza, S. P. (2007) · Brain Research · doi:10.1016/j.brainres.2007.09.087 · Cited by 112 · see citing works
Neurobiology of social attachments
Coria‐Ávila, G. A., Manzo, J. G., García, L. I., Carrillo, P., Miquel, M., & Pfaus, J. G. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.04.004 · Cited by 106 · see citing works
Intranasal oxytocin, but not vasopressin, augments neural responses to toddlers in human fathers
Li, T., Chen, X., Mascaro, J., Haroon, E., & Rilling, J. K. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.01.006 · Cited by 105 · see citing works
Why the Legend of the Killer Ape Never Dies
Sussman, R. W. (2013) · doi:10.1093/acprof:oso/9780199858996.003.0006 · Cited by 104 · see citing works
The onset of puberty: effects on the psychophysiology of defensive and appetitive motivation
Quevedo, K. M., Benning, S. D., Gunnar, M. R., & Dahl, R. E. (2009) · Development and Psychopathology · doi:10.1017/s0954579409000030 · Cited by 100 · see citing works
μ-Opioid receptors within subregions of the striatum mediate pair bond formation through parallel yet distinct reward mechanisms
Resendez, S. L., Dome, M., Gormley, G., Franco, D., Nevárez, N., Hamid, A. A., & Aragona, B. J. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4123-12.2013 · Cited by 93 · see citing works
A common oxytocin receptor gene (<scp>OXTR</scp>) polymorphism modulates intranasal oxytocin effects on the neural response to social cooperation in humans
Feng, C., Lori, A., Waldman, I. D., Binder, E. B., Haroon, E., & Rilling, J. K. (2015) · Genes, Brain and Behavior · doi:10.1111/gbb.12234 · Cited by 94 · see citing works
Estrogen receptors in the medial amygdala inhibit the expression of male prosocial behavior
Cushing, B. S., Perry, A., Musatov, S., Ogawa, S., & Papademetriou, E. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1928-08.2008 · Cited by 95 · see citing works
Telencephalic binding sites for oxytocin and social organization: A comparative study of eusocial naked mole‐rats and solitary cape mole‐rats
Kalamatianos, T., Faulkes, C. G., Oosthuizen, M. K., Poorun, R., Bennett, N. C., & Coen, C. W. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22302 · Cited by 92 · see citing works
Salubrious effects of oxytocin on social stress-induced deficits
Smith, A. S., & Wang, Z. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.11.010 · Cited by 88 · see citing works
Thy1‐hAPPLond/Swe+ mouse model of Alzheimer's disease displays broad behavioral deficits in sensorimotor, cognitive and social function
Faizi, M., Bader, P. L., Saw, N. L., Nguyen, T. V., Beraki, S., Wyss‐Coray, T., Longo, F. M., & Shamloo, M. (2012) · Brain and Behavior · doi:10.1002/brb3.41 · Cited by 86 · see citing works
Neuroendocrinology of social behavior
Adkins-Regan, E. (2009) · ILAR Journal · doi:10.1093/ilar.50.1.5 · Cited by 81 · see citing works
Neuroendocrinology and sexual differentiation in eusocial mammals
Holmes, M. M., Goldman, B. D., Goldman, S. L., Seney, M. L., & Forger, N. G. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.04.010 · Cited by 79 · see citing works
Social bonding: regulation by neuropeptides
Lieberwirth, C., & Wang, Z. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00171 · Cited by 80 · see citing works
Social attachment in juvenile monkeys with neonatal lesion of the hippocampus, amygdala and orbital frontal cortex
Goursaud, A. P., & Bachevalier, J. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.09.020 · Cited by 78 · see citing works
The neurobiology of pair bond formation, bond disruption, and social buffering
Lieberwirth, C., & Wang, Z. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.05.006 · Cited by 72 · see citing works
Female Sexual Behavior
Pfaus, J. G., Jones, S. L., Flanagan‐Cato, L. M., & Blaustein, J. D. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00050-8 · Cited by 71 · see citing works
Field tests of cis-regulatory variation at the prairie vole avpr1a locus: association with V1aR abundance but not sexual or social fidelity
OPHIR, A., CAMPBELL, P., HANNA, K., & PHELPS, S. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.07.009 · Cited by 66 · see citing works
Navigating Monogamy: Nonapeptide Sensitivity in a Memory Neural Circuit May Shape Social Behavior and Mating Decisions
Ophir, A. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00397 · Cited by 62 · see citing works
Aversive motivation and the maintenance of monogamous pair bonding
Resendez, S. L., & Aragona, B. J. (2013) · Reviews in the Neurosciences · doi:10.1515/revneuro-2012-0068 · Cited by 57 · see citing works
Neurochemical basis of conditioned partner preference in the female rat: I. Disruption by naloxone.
Coria‐Ávila, G. A., Solomon, C. E., Vargas, E. B., Lemme, I., Ryan, R., Ménard, S., Gavrila, A. M., & Pfaus, J. G. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.2.385 · Cited by 56 · see citing works
Neuronal activation by stimuli that predict sexual reward in female rats
Coria‐Ávila, G. A., & Pfaus, J. G. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.05.052 · Cited by 55 · see citing works
Poison frogs as a model system for studying the neurobiology of parental care
Roland, A. B., & O’Connell, L. A. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.10.002 · Cited by 54 · see citing works
Oxytocin‐ and arginine vasopressin‐containing fibers in the cortex of humans, chimpanzees, and rhesus macaques
Flattery, C. N. R., Ross, A. P., Sahu, S. P., Siegel, E. R., Dooyema, J. M., Cree, M. A., Stopa, E. G., Young, L. J., Rilling, J. K., Albers, H. E., et al. (2018) · American Journal of Primatology · doi:10.1002/ajp.22875 · Cited by 50 · see citing works
Self-citation
The Contribution of Oxytocin and Vasopressin to Mammalian Social Behavior: Potential Role in Autism Spectrum Disorder
Harony, H., & Wagner, S. (2010) · Neurosignals · doi:10.1159/000321035 · Cited by 62 · see citing works
The AVPR1A Gene and Substance Use Disorders: Association, Replication, and Functional Evidence
Maher, B. S., Vladimirov, V. I., Latendresse, S. J., Thiselton, D. L., McNamee, R. L., Kang, M., Bigdeli, T. B., Chen, X., Riley, B. P., Hettema, J. M., et al. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.02.023 · Cited by 49 · see citing works
Dynamic regulation of brain aromatase and isotocin receptor gene expression depends on parenting status
DeAngelis, R., Dodd, L., Snyder, A., & Rhodes, J. S. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.06.006 · Cited by 45 · see citing works
Alcohol Intake in Prairie Voles is Influenced by the Drinking Level of a Peer
Anacker, A. M. J., Loftis, J. M., & Ryabinin, A. E. (2011) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2011.01533.x · Cited by 48 · see citing works
Female alternative mating tactics, reproductive success and nonapeptide receptor expression in the social decision-making network
Zheng, D., Larsson, B., Phelps, S. M., & Ophir, A. G. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.02.024 · Cited by 48 · see citing works
Training Reduces Stress in Human-Socialised Wolves to the Same Degree as in Dogs
Vasconcellos, A. D. S., Virányi, Z., Range, F., Ades, C., Scheidegger, J. K., Möstl, E., & Kotrschal, K. M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0162389 · Cited by 48 · see citing works
Plastic changes induced by neonatal handling in the hypothalamus of female rats
Duarte, E. C. W., Todeschin, A. S., Fernandes, M. D. C., Bittencourt, L. C., Pereira, G. A. M., Samios, V. N., Schuh, A. F. S., Achaval, M., Xavier, L. L., Sanvitto, G. L., et al. (2007) · Brain Research · doi:10.1016/j.brainres.2007.07.030 · Cited by 47 · see citing works
Neuropeptide Regulation of Social Attachment: The Prairie Vole Model
Tabbaa, M., Paedae, B., Liu, Y., & Wang, Z. (2016) · Comprehensive physiology · doi:10.1002/cphy.c150055 · Cited by 53 · see citing works
Challenges to the Pair Bond: Neural and Hormonal Effects of Separation and Reunion in a Monogamous Primate
Hinde, K., Muth, C., Maninger, N., Ragen, B., Larke, R. H., Jarcho, M. R., Mendoza, S. P., Mason, W. A., Ferrer, E. E., Cherry, S. R., et al. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00221 · Cited by 46 · see citing works
Social investigation in a memory task relates to natural variation in septal expression of oxytocin receptor and vasopressin receptor 1a in prairie voles (Microtus ochrogaster).
Ophir, A. G., Zheng, D.-J., Eans, S. O., & Phelps, S. M. (2009) · Behavioral Neuroscience · doi:10.1037/a0016663 · Cited by 45 · see citing works
Dysfunctional play and dopamine physiology in the Fischer 344 rat
Siviy, S. M., Crawford, C. A., Akopian, G. K., & Walsh, J. P. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.02.009 · Cited by 44 · see citing works
Blockade of arginine vasotocin signaling reduces aggressive behavior and c-Fos expression in the preoptic area and periventricular nucleus of the posterior tuberculum in male Amphiprion ocellaris
Yaeger, C. E., Ros, A. M., Cross, V., DeAngelis, R., Stobaugh, D. J., & Rhodes, J. S. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.02.045 · Cited by 44 · see citing works
Prosociality and a Sociosexual Hypothesis for the Evolution of Same-Sex Attraction in Humans
Barron, A. B., & Hare, B. A. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.02955 · Cited by 43 · see citing works
Intranasal oxytocin modulates neural functional connectivity during human social interaction
Rilling, J. K., Chen, X., Chen, X., & Haroon, E. (2018) · American Journal of Primatology · doi:10.1002/ajp.22740 · Cited by 40 · see citing works
OXTR methylation modulates exogenous oxytocin effects on human brain activity during social interaction
Chen, X., Nishitani, S., Haroon, E., Smith, A. K., & Rilling, J. K. (2019) · Genes Brain & Behavior · doi:10.1111/gbb.12555 · Cited by 38 · see citing works
The neurochemistry of social reward during development: What have we learned from rodent models?
Manduca, A., Carbone, E., Schiavi, S., Cacchione, C., Buzzelli, V., Campolongo, P., & Trezza, V. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15321 · Cited by 34 · see citing works
Newly paired zebra finches have higher dopamine levels and immediate early gene Fos expression in dopaminergic neurons
Banerjee, S. B., Dias, B. G., Crews, D. P., & Adkins–Regan, E. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12378 · Cited by 35 · see citing works
Large household reduces dementia mortality: A cross-sectional data analysis of 183 populations
You, W., & Henneberg, M. (2022) · PLoS ONE · doi:10.1371/journal.pone.0263309 · Cited by 33 · see citing works
Greater family size is associated with less cancer risk: an ecological analysis of 178 countries
You, W., Rühli, F. J., Henneberg, R. J., & Henneberg, M. (2018) · BMC Cancer · doi:10.1186/s12885-018-4837-0 · Cited by 32 · see citing works
The Neurobiology of Cooperation and Altruism
Rilling, J. K. (2011) · Springer eBooks · doi:10.1007/978-1-4419-9520-9_17 · Cited by 32 · see citing works
Social recognition in paired, but not single, male prairie voles
Blocker, T. D., & Ophir, A. G. (2015) · Animal Behaviour · doi:10.1016/j.anbehav.2015.07.003 · Cited by 31 · see citing works
Hormones and Human Partnering
van Anders, S. M., & Gray, P. B. (2007) · Annual Review of Sex Research · doi:10.1080/10532528.2007.10559847 · Cited by 31 · see citing works
The role of orgasm in the development and shaping of partner preferences
Coria‐Ávila, G. A., Herrera‐Covarrubias, D., Ismail, N., & Pfaus, J. G. (2016) · Socioaffective Neuroscience & Psychology · doi:10.3402/snp.v6.31815 · Cited by 30 · see citing works
Mating and social exposure induces an opioid-dependent conditioned place preference in male but not in female prairie voles (Microtus ochrogaster)
Ulloa, M., Portillo, W., Díaz, N. F., Young, L. J., Camacho, F. J., Rodríguez, V. M., & Paredes, R. G. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.10.015 · Cited by 31 · see citing works
Self-citation
Prairie Voles as a Model for Understanding the Genetic and Epigenetic Regulation of Attachment Behaviors
Sadino, J. M., & Donaldson, Z. R. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.7b00475 · Cited by 28 · see citing works
Somatic genital reflexes in rats with a nod to humans: Anatomy, physiology, and the role of the social neuropeptides
Normandin, J. J., & Murphy, A. Z. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.02.006 · Cited by 30 · see citing works
Neural Circuits Underlying Rodent Sociality: A Comparative Approach
Lee, N. S., & Beery, A. K. (2019) · Current topics in behavioral neurosciences · doi:10.1007/7854_2018_77 · Cited by 31 · see citing works
AVPR1A Sequence Variation in Monogamous Owl Monkeys (Aotus azarai) and Its Implications for the Evolution of Platyrrhine Social Behavior
Babb, P. L., Fernández‐Duque, E., & Schurr, T. G. (2010) · Journal of Molecular Evolution · doi:10.1007/s00239-010-9383-6 · Cited by 29 · see citing works
Reciprocal processes of sensory perception and social bonding: an integrated social‐sensory framework of social behavior
Prior, N. H., Bentz, E. J., & Ophir, A. G. (2021) · Genes Brain & Behavior · doi:10.1111/gbb.12781 · Cited by 27 · see citing works
Animal Models for the Study of Female Sexual Dysfunction
Marson, L., Giamberardino, M. A., Costantini, R., Czakanski, P. P., & Wesselmann, U. (2013) · Sexual Medicine Reviews · doi:10.1002/smrj.14 · Cited by 28 · see citing works
Insect Reward Systems
Søvik, E., Perry, C. J., & Barron, A. B. (2015) · Advances in insect physiology · doi:10.1016/bs.aiip.2014.12.006 · Cited by 27 · see citing works
The Influence of Predation on Primate and Early Human Evolution: Impetus for Cooperation
Hart, D., & Sussman, R. W. (2011) · Springer eBooks · doi:10.1007/978-1-4419-9520-9_3 · Cited by 28 · see citing works
Low fertility may be a significant determinant of ovarian cancer worldwide: an ecological analysis of cross- sectional data from 182 countries
You, W., Symonds, I., & Henneberg, M. (2018) · Journal of Ovarian Research · doi:10.1186/s13048-018-0441-9 · Cited by 26 · see citing works
Female-Directed Aggression Predicts Paternal Behavior, but Female Prairie Voles Prefer Affiliative Males to Paternal Males
Ophir, A. G., Crino, O. L., Wilkerson-Vidal, Q. C., Wolff, J. O., & Phelps, S. M. (2007) · Brain Behavior and Evolution · doi:10.1159/000108609 · Cited by 26 · see citing works
Neural mechanisms of reproduction in females as a predisposing factor for drug addiction
Hedges, V. L., Staffend, N. A., & Meisel, R. L. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.02.003 · Cited by 26 · see citing works
The Effects of Romantic Love on Mentalizing Abilities
Wlodarski, R., & Dunbar, R. (2014) · Review of General Psychology · doi:10.1037/gpr0000020 · Cited by 22 · see citing works
Towards meeting Tinbergen's challenge
Ophir, A. G. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.03.012 · Cited by 19 · see citing works
Beyond human intentions and emotions
Juan, E., Frum, C., Bianchi‐Demicheli, F., Wang, Y., Lewis, J. W., & Cacioppo, S. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00099 · Cited by 18 · see citing works
Predicting functional neuroanatomical maps from fusing brain networks with genetic information
Ganglberger, F., Kaczanowska, J., Penninger, J. M., Heß, A., Bühler, K., & Haubensak, W. E. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.08.070 · Cited by 19 · see citing works
A neuromodulatory role for oxytocin within the supramammillary nucleus.
Cumbers, M., Chung, S., & Wakerley, J. (2007) · Neuropeptides · doi:10.1016/j.npep.2007.04.004 · Cited by 17 · see citing works
Neuroanatomical Projections of the Species-Specific Tyrosine Hydroxylase-Immunoreactive Cells of the Male Prairie Vole Bed Nucleus of the Stria Terminalis and Medial Amygdala
Northcutt, K. V., & Lonstein, J. S. (2011) · Brain Behavior and Evolution · doi:10.1159/000326618 · Cited by 18 · see citing works
Reproduction: A New Venue for Studying Function of Adult Neurogenesis?
Lau, B. W.-M., Yau, S., & So, K. (2010) · Cell Transplantation · doi:10.3727/096368910x532765 · Cited by 17 · see citing works
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The neurobiology of pair bonding: Insights from a socially monogamous rodent
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Authors: Young, L. J., Murphy Young, A. Z., & Hammock, E. A. D.
Affiliations: Emory University (US)
Corresponding author: Young, Larry J.
ORCID: Young, Larry J.
Hammock, Elizabeth A.D.
Venue: Journal of Comparative Neurology
Publisher: Wiley
Published: 2005-10-27
Volume: 493
Issue: 1
Pages: 51-57
ISSN: 0021-9967 (ISSN-L)
1096-9861
DOI: 10.1002/cne.20771
OpenAlex: W1975226557
Cited by: 163
References: 83
Citations by year: 2026: 1 · 2025: 6 · 2024: 6 · 2023: 4 · 2022: 3 · 2021: 5 · 2020: 4 · 2019: 4 · 2018: 8 · 2017: 7 · 2016: 8 · 2015: 7 · 2014: 14 · 2013: 11 · 2012: 10
FWCI: 0.99
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Comparative Neurology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5f31mh067397-02)
National Institute of Mental Health (MH-64692, K02MH064692, MH 56897, MH67397, MH 56538, R01MH056538)
National Center for Research Resources (RR-00 165, P51RR000165)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: pair bond, monogamy, neural circuits, mesolimbic dopamine system, reward and reinforcement, neuropeptides, somatosensory processing, genitalia, social bonding, interindividual variability, human connection, rodents
MeSH terms: Animals, Arginine Vasopressin, Brain, Arvicolinae, Female, Humans, Male, Neural Pathways, Oxytocin, Pair Bond, Reward, Sexual Behavior, Animal, Somatosensory Cortex, Receptors, Neuropeptide

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Anatomy and neurochemistry of the pair bond

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