Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene.
Abstract
The molecular mechanisms underlying the evolution of complex behaviour are poorly understood. The mammalian genus Microtus provides an excellent model for investigating the evolution of social behaviour. Prairie voles (Microtus ochrogaster) exhibit a monogamous social structure in nature, whereas closely related meadow voles (Microtus pennsylvanicus) are solitary and polygamous. In male prairie voles, both vasopressin and dopamine act in the ventral forebrain to regulate selective affiliation between adult mates, known as pair bond formation, as assessed by partner preference in the laboratory. The vasopressin V1a receptor (V1aR) is expressed at higher levels in the ventral forebrain of monogamous than in promiscuous vole species, whereas dopamine receptor distribution is relatively conserved between species. Here we substantially increase partner preference formation in the socially promiscuous meadow vole by using viral vector V1aR gene transfer into the ventral forebrain. We show that a change in the expression of a single gene in the larger context of pre-existing genetic and neural circuits can profoundly alter social behaviour, providing a potential molecular mechanism for the rapid evolution of complex social behaviour.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Only 37% of couples claim to be very happy in their marriage.
“While achieving relationship satisfaction is a primary goal for most individuals, only 37% of couples claim to be very happy in their marriage [24].”
From Could intranasal oxytocin be used to enhance relationships? Research imperatives, clinical policy, and ethical considerations (2013) · cites this paper as [24]
Pair-bonded prairie voles spend more time with their partner than with a stranger, whereas non-monogamous meadow voles spend little time interacting with their partner or stranger.
“Pair-bonded prairie voles spend more time with their partner than with the stranger, whereas non-monogamous meadow voles (Microtus pennsylvanicus) spend little time interacting with their partner or stranger [138].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [138]
Viral-mediated increases in VP AVPR1a expression induce partner preferences and increase affiliative behaviors in sexually naïve male prairie voles and also lead to partner preference formation in non-monogamous meadow voles.
“Conversely, viral-mediated increases in VP AVPR1a expression induce partner preferences and increase affiliative behaviors in male prairie voles that are sexually naïve and, interestingly, also lead to partner preference formation in non-monogamous meadow voles [138,146].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [138]
Over-expressing the gene encoding the prairie vole AVPR1A, Avpr1a, in the ventral pallidum of male meadow voles using viral vector-mediated gene transfer results in the ability of this promiscuous species to display partner preferences.
“Over-expressing the gene encoding the prairie vole AVPR1A, Avpr1a, in the ventral pallidum of male meadow voles using viral vector-mediated gene transfer results in the ability of this promiscuous species to display partner preferences [23].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [23]
Viral-mediated Avpr1a receptor overexpression studies show that species differences in Avpr1a expression mediate species differences in social behavior, and variation in Avpr1a expression in the brain is related to microsatellite diversity in the gene's 5' flanking region.
“Viral-mediated Avpr1a receptor overexpression studies show that species differences in Avpr1a expression mediate species differences in social behavior, and variation in Avpr1a expression in the brain is related to microsatellite diversity in the gene's 5′ flanking region (151-154).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [152]
Cites
Kleiman, D. G. (1977) · The Quarterly Review of Biology · doi:10.1086/409721 · Cited by 1,436 · see citing works
A 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 1× · see citing works
“Central administration of vasopressin facilitates each of these monogamous-typical behaviours in male prairie voles through V1aRs in the brai”
BackgroundBielsky, I. F., Hu, S.-B., Szegda, K. L., Westphal, H., & Young, L. J. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300360 · Cited by 531 · see citing works
Self-citationYoung, L. J., Nilsen, R., Waymire, K. G., MacGregor, G. R., & Insel, T. R. (1999) · Nature · doi:10.1038/23475 · Cited by 488 · see citing works
Insel, T., Wang, Z., & Ferris, C. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-09-05381.1994 · Cited by 454 · see citing works
Self-citationVasopressin and oxytocin receptors in the central nervous system
Tribollet, E., & Barberis, C. (1996) · Critical Reviews™ in Neurobiology · doi:10.1615/critrevneurobiol.v10.i1.60 · Cited by 399 · see citing works
Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster).
Wang, Z., Ferris, C. F., & De Vries, G. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.1.400 · Cited by 381 · see citing works
Self-citationA critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles
Aragona, B. J., Liu, Y., Curtis, J. T., Stephan, F. K., & Wang, Z. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03483.2003 · Cited by 351 · see citing works
Self-citationGingrich, B., Liu, Y., Cascio, C., Wang, Z., & Insel, T. R. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.1.173 · Cited by 339 · see citing works
Self-citationVasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole
Lim, M. M., & Young, L. J. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.12.008 · Cited by 322 · see citing works
Self-citationPitkow, L. J., Sharer, C. A., Ren, X., Insel, T. R., Terwilliger, E. F., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07392.2001 · Cited by 295 · see citing works
Self-citationBester‐Meredith, J. K., Young, L. J., & Marler, C. A. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1522 · Cited by 285 · see citing works
Self-citationKim, S.-J., Young, L. J., Gonen, D., Veenstra-VanderWeele, J., Courchesne, R., Courchesne, E., Lord, C., Leventhal, B. L., Cook Jr, E. H., & Insel, T. R. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001125 · Cited by 265 · see citing works
Self-citationYoung, L. J., Winslow, J., Nilsen, R., & Insel, T. R. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.3.599 · Cited by 235 · see citing works
Self-citationOxytocin and Vasopressin Receptors and Species-Typical Social Behaviors
Young, L. J. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1548 · Cited by 211 · see citing works
Self-citationWang, Z., Yu, G., Cascio, C., Liu, Y., Gingrich, B., & Insel, T. R. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.3.602 · Cited by 205 · see citing works
Self-citationYoung, L. J., Winslow, J. T., Nilsen, R., & Insel, T. R. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.3.599 · Cited by 196 · see citing works
Self-citationComparison of the Mating System and Paternal Behavior in Microtus ochrogaster and M. pennsylvanicus
Gruder-Adams, S., & Getz, L. L. (1985) · Journal of Mammalogy · doi:10.2307/1380976 · Cited by 167 · see citing works
Landgraf, R., Frank, E., Aldag, J. M., Neumann, I. D., Sharer, C. A., Ren, X., Terwilliger, E. F., Niwa, M., Wigger, A., & Young, L. J. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02750.x · Cited by 164 · see citing works
Self-citationLim, M. M., Murphy, A. Z., & Young, L. J. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.10973 · Cited by 163 · see citing works
Self-citationCooperative breeding and monogamy in prairie voles: influence of the sire and geographical variation
Roberts, R. L., WILLIAMS, J. R., Wang, A. S., & Carter, C. S. (1998) · Animal Behaviour · doi:10.1006/anbe.1997.0659 · Cited by 152 · see citing works
Localization of Vasopressin (V<sub>1a</sub>) Receptor Binding and mRNA in the Rhesus Monkey Brain
Young, Toloczko, & Insel (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00332.x · Cited by 139 · see citing works
Functional Microsatellite Polymorphism Associated with Divergent Social Structure in Vole Species
Hammock, E. A. D. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh104 · Cited by 121 · see citing works
Phelps, S. M., & Young, L. J. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10902 · Cited by 116 · see citing works
Self-citationSocial behavior and comparative genomics: new genes or new gene regulation?
Robinson, G. E., & Ben‐Shahar, Y. (2002) · Genes Brain & Behavior · doi:10.1034/j.1601-183x.2002.10401.x · Cited by 101 · see citing works
Hammock, E. A. D., & Young, L. J. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02083.x · Cited by 95 · see citing works
Self-citationWang, Z., Toloczko, D., Young, L. J., Moody, K., Newman, J. D., & Insel, T. R. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00636-7 · Cited by 75 · see citing works
Self-citationBehavioral Consequences of Trauma
Gensemer, I. B., McMurry, F. G., WALKER, J. C., Monasky, M., & BROTMAN, S. J. (1988) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/00005373-198801000-00006 · Cited by 64 · see citing works
Parker, K. J., Phillips, K. M., & Lee, T. M. (2001) · Animal Behaviour · doi:10.1006/anbe.2000.1707 · Cited by 41 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Oxytocin, vasopressin, and the neurogenetics of sociality
Donaldson, Z. R., & Young, L. J. (2008) · Science · doi:10.1126/science.1158668 · Cited by 1,645 · see citing works
Self-citationThe neurobiology of pair bonding.
Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523 · see citing works
Behavioural phenotyping assays for mouse models of autism
Silverman, J. L., Yang, M., Lord, C., & Crawley, J. N. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2851 · Cited by 1,462 · see citing works
Neural reuse: A fundamental organizational principle of the brain
Anderson, M. L. (2010) · Behavioral and Brain Sciences · doi:10.1017/s0140525x10000853 · Cited by 1,212 · see citing works
Fonagy, P., & Luyten, P. (2009) · Development and Psychopathology · doi:10.1017/s0954579409990198 · Cited by 1,146 · see citing works
“pecially in males (Caldwell, Lee, Macbeth, & Young, 2008; Lim et al., 2004).”
BackgroundInsel, T. R. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.005 · Cited by 1,044 · see citing works
Dendritic peptide release and peptide-dependent behaviours
Ludwig, M., & Leng, G. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1845 · Cited by 945 · see citing works
Reward, Motivation, and Emotion Systems Associated With Early-Stage Intense Romantic Love
Aron, A., Fisher, H., Mashek, D. J., Strong, G., Li, H., & Brown, L. L. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00838.2004 · Cited by 963 · see citing works
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
The social role of touch in humans and primates: Behavioural function and neurobiological mechanisms
Dunbar, R. I. M. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.07.001 · Cited by 798 · see citing works
The vertebrate social behavior network: Evolutionary themes and variations
Goodson, J. L. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.02.003 · Cited by 771 · see citing works
Neuropeptidergic 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
Self-citationFries, 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
Microsatellite instability generates diversity in brain and sociobehavioral traits
Hammock, E. A. D., & Young, L. J. (2005) · Science · doi:10.1126/science.1111427 · Cited by 545 · see citing works
Self-citationVentral pallidum roles in reward and motivation
Smith, K. S., Tindell, A. J., Aldridge, J. W., & Berridge, K. C. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.09.038 · Cited by 548 · see citing works
Dumais, K. M., & Veenema, A. H. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.04.003 · Cited by 520 · see citing works
“Male prairie voles additionally show more VP-immunoreactive fibers in the ventral pallidum compared to females (Lim et al., 2004a).”
BackgroundResultInfluentialVasopressin: 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
Aragona, 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
Self-citationWalum, H., Westberg, L., Henningsson, S., Neiderhiser, J. M., Reiss, D., Igl, W., Ganiban, J. M., Spotts, E. L., Pedersen, N. L., Eriksson, E., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803081105 · Cited by 460 · see citing works
Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders?
CARTER, C. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.025 · Cited by 432 · see citing works
The 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
Self-citationVitamin D hormone regulates serotonin synthesis. Part 1: Relevance for autism
Patrick, R. P., & Ames, B. N. (2014) · The FASEB Journal · doi:10.1096/fj.13-246546 · Cited by 414 · see citing works
Romantic love: an fMRI study of a neural mechanism for mate choice.
Fisher, H., Aron, A., & Brown, L. L. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20772 · Cited by 396 · see citing works
The neural mechanisms and circuitry of the pair bond
Walum, H., & Young, L. J. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0072-6 · Cited by 353 · see citing works
Self-citationNuman, M., & Young, L. J. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.015 · Cited by 355 · see citing works
Self-citationBielsky, I. F., Hu, S.-B., Ren, X., Terwilliger, E. F., & Young, L. J. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.031 · Cited by 367 · see citing works
Self-citationCentral vasopressin and oxytocin release: regulation of complex social behaviours
VEENEMA, A., & NEUMANN, I. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00422-6 · Cited by 338 · see citing works
Ross, 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
Self-citationReward, Addiction, and Emotion Regulation Systems Associated With Rejection in Love
Fisher, H. E., Brown, L. L., Aron, A., Strong, G., & Mashek, D. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00784.2009 · Cited by 328 · 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
Burkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307 · see citing works
“When these receptors are upregulated in the VP of meadow voles to the “prairie vole-like” phenotype, these animals become capable of forming a partner preference toward a female mate (Lim et al. 2004).”
Self-citationMother–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
Brain vasopressin is an important regulator of maternal behavior independent of dams’ trait anxiety
Bosch, O. J., & Neumann, I. D. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807412105 · Cited by 280 · 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-citationThe genetic basis of parental care evolution in monogamous mice
Bendesky, A., Kwon, Y.-M., Lassance, J.-M., Lewarch, C. L., Yao, S., Peterson, B. K., He, M. X., Dulac, C., & Hoekstra, H. E. (2017) · Nature · doi:10.1038/nature22074 · Cited by 268 · see citing works
Veenema, A. H., Bredewold, R., & Neumann, I. D. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.02.008 · Cited by 263 · see citing works
Johnson, Z. V., & Young, L. J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.034 · Cited by 242 · see citing works
Self-citationAhern, T. H. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.017.2009 · Cited by 239 · 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
Nonapeptides and the evolutionary patterning of sociality
GOODSON, J. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00401-9 · Cited by 228 · see citing works
Smeltzer, M. D., Curtis, J. T., Aragona, B. J., & Wang, Z. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2005.10.019 · Cited by 222 · see citing works
Self-citationShultz, S. R., MacFabe, D. F., Ossenkopp, K.-P., Scratch, S., Whelan, J., Taylor, R., & Cain, D. P. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.01.013 · Cited by 217 · see citing works
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
Oxytocin and vasopressin: powerful regulators of social behavior
Caldwell, H. K. (2017) · The Neuroscientist · doi:10.1177/1073858417708284 · Cited by 216 · see citing works
Genes, brains and mammalian social bonds
Curley, J. P., & Keverne, E. B. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.05.018 · Cited by 214 · see citing works
Deconstructing sociality, social evolution and relevant nonapeptide functions
Goodson, J. L. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.12.005 · Cited by 206 · see citing works
Albers, H. E. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.07.001 · Cited by 200 · see citing works
Freeman, S. M., Inoue, K., Smith, A. L., Goodman, M. M., & Young, L. J. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.03.023 · Cited by 185 · see citing works
“…vector gene manipulations, and transgenic mouse technology have led to the elucidation of the neural mechanisms underlying the effects of these neuropeptides and their receptors on these complex social behaviors (Dölen et al., 2013; Ferguson et al., 2001; Lim et al., 2004b; Owen et al., 2013).”
BackgroundMethodOxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities
Rigney, N., de Vries, G. J., Petrulis, A., & Young, L. J. (2022) · Endocrinology · doi:10.1210/endocr/bqac111 · Cited by 191 · see citing works
Self-citationConservation of core gene expression in vertebrate tissues
Chan, E. T., Quon, G. T., Chua, G., Babak, T., Trochesset, M., Zirngibl, R. A., Aubin, J., Ratcliffe, M. J., Wilde, A., Brudno, M., et al. (2009) · Journal of Biology · doi:10.1186/jbiol130 · Cited by 190 · see citing works
Johnson, 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-citationVeenema, A. H., Beiderbeck, D. I., Lukas, M., & Neumann, I. D. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.006 · Cited by 180 · see citing works
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
Self-citationGobrogge, K. L., Liu, Y., Young, L. J., & Wang, Z. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908620106 · Cited by 178 · see citing works
Self-citationHormonal mechanisms of cooperative behaviour
Soares, M. C., Bshary, R., Fusani, L., Goymann, W., Hau, M., Hirschenhauser, K., & Oliveira, R. F. (2010) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2010.0151 · Cited by 173 · see citing works
Young, K. A., Liu, Y., & Wang, Z. (2008) · Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology · doi:10.1016/j.cbpc.2008.02.004 · Cited by 163 · see citing works
Self-citationAnatomy and neurochemistry of the pair bond
Young, L. J., Murphy Young, A. Z., & Hammock, E. A. D. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20771 · Cited by 163 · see citing works
Self-citationOxytocin 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-citationFreeman, S. M., Walum, H., Inoue, K., Smith, A. L., Goodman, M. M., Bales, K. L., & Young, L. J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.04.055 · Cited by 153 · see citing works
Self-citation2006 Curt P. Richter award winner
DeVries, A. C., Craft, T. K. S., Glasper, E. R., Neigh, G. N., & Alexander, J. K. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.04.007 · Cited by 153 · see citing works
Autoantibodies against neuropeptides are associated with psychological traits in eating disorders
Fetissov, S. O., Harro, J., Jaanisk, M., Järv, A., Podar, I., Allik, J., Nilsson, I., Sakthivel, P., Lefvert, A. K., & Hökfelt, T. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507204102 · Cited by 152 · see citing works
Smith, C. J. W., Poehlmann, M. L., Li, S., Ratnaseelan, A. M., Bredewold, R., & Veenema, A. H. (2017) · Brain Structure and Function · doi:10.1007/s00429-016-1260-7 · Cited by 143 · see citing works
Urinary oxytocin as a noninvasive biomarker of positive emotion in dogs
Mitsui, S., Yamamoto, M., Nagasawa, M., Mogi, K., Kikusui, T., Ohtani, N., & Ohta, M. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.05.012 · Cited by 147 · see citing works
Genetics of aggressive behavior: An overview
Veroude, K., Zhang‐James, Y., Fernàndez‐Castillo, N., Bakker, M. J., Cormand, B., & Faraone, S. V. (2016) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32364 · Cited by 147 · see citing works
Beery, A. K., Lacey, E. A., & Francis, D. D. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21638 · Cited by 144 · see citing works
Vasopressin innervation of the mouse ( <i>Mus musculus</i> ) brain and spinal cord
Rood, B. D., & De Vries, G. J. (2011) · Journal of Comparative Neurology · doi:10.1002/cne.22635 · Cited by 134 · see citing works
Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships
Hurlemann, R., & Scheele, D. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.05.013 · Cited by 136 · see citing works
Mammalian monogamy is not controlled by a single gene
Fink, S., Excoffier, L., & Heckel, G. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602380103 · Cited by 133 · see citing works
Oxytocin, vasopressin, and the motivational forces that drive social behaviors
Caldwell, H. K., & Albers, H. E. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2015_390 · Cited by 129 · see citing works
Neuropeptides and the social brain: potential rodent models of autism
Lim, M. M., Bielsky, I. F., & Young, L. J. (2005) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.05.006 · Cited by 129 · see citing works
Self-citationLove is more than just a kiss: a neurobiological perspective on love and affection
de Boer, A., van Buel, E. M., & Ter Horst, G. J. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.017 · Cited by 123 · see citing works
Autism and Oxytocin: New Developments in Translational Approaches to Therapeutics
Green, J. J., & Hollander, E. (2010) · Neurotherapeutics · doi:10.1016/j.nurt.2010.05.006 · Cited by 124 · see citing works
Dopamine regulation of social choice in a monogamous rodent species
Aragona, B. J. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.015.2009 · Cited by 119 · see citing works
Dynamic corticostriatal activity biases social bonding in monogamous female prairie voles
Amadei, E. A., Johnson, Z. V., Jun Kwon, Y., Shpiner, A. C., Saravanan, V., Mays, W. D., Ryan, S. J., Walum, H., Rainnie, D. G., Young, L. J., et al. (2017) · Nature · doi:10.1038/nature22381 · Cited by 115 · see citing works
Self-citationLENG, 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
Oxytocin and vasopressin: genetics and behavioral implications
Caldwell, H. K., & Young, W. S. (2006) · Handbook of Neurochemistry and Molecular Neurobiology · doi:10.1007/978-0-387-30381-9_25 · Cited by 113 · see citing works
Neuroenhancement of love and marriage: the chemicals between us.
Savulescu, J., & Sandberg, A. (2008) · Neuroethics · doi:10.1007/s12152-007-9002-4 · Cited by 111 · see citing works
Genetic contributions to behavioural diversity at the gene-environment interface
Bendesky, A., & Bargmann, C. I. (2011) · Nature Reviews Genetics · doi:10.1038/nrg3065 · Cited by 103 · see citing works
Oxytocin and same-sex social behavior in female meadow voles
Beery, A. K., & Zucker, I. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.05.023 · Cited by 108 · see citing works
Liu, Y., Aragona, B. J., Young, K. A., Dietz, D. M., Kabbaj, M., Mazei-Robison, M., Nestler, E. J., & Wang, Z. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911998107 · Cited by 101 · see citing works
Self-citationBarrett, C. E., Keebaugh, A. C., Ahern, T. H., Bass, C. E., Terwilliger, E. F., & Young, L. J. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.01.005 · Cited by 100 · see citing works
Self-citationCRF receptors in the nucleus accumbens modulate partner preference in prairie voles
Lim, M. M., Liu, Y., Ryabinin, A. E., Bai, Y., Wang, Z., & Young, L. J. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.01.006 · Cited by 99 · see citing works
Self-citationOxytocin and vasopressin systems in genetic syndromes and neurodevelopmental disorders
Francis, S. M., Sagar, A., Levin-Decanini, T., Liu, W., Carter, C. S., & Jacob, S. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.021 · Cited by 101 · see citing works
Lim, M. M., Nair, H. P., & Young, L. J. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20532 · Cited by 95 · see citing works
Self-citationDopamine and opioid systems interact within the nucleus accumbens to maintain monogamous pair bonds
Resendez, S. L., Keyes, P. C., Day, J. J., Hambro, C., Austin, C. J., Maina, F. K., Eidson, L. N., Porter-Stransky, K. A., Nevárez, N., McLean, J. W., et al. (2016) · eLife · doi:10.7554/elife.15325 · Cited by 88 · see citing works
Fuxe, K., Borroto-Escuela, D. O., Romero-Fernandez, W., Ciruela, F., Manger, P., Leo, G., Díaz-Cabiale, Z., & Agnati, L. F. (2012) · Brain Research · doi:10.1016/j.brainres.2012.01.062 · Cited by 81 · see citing works
Hopkins, W. D., Donaldson, Z. R., & Young, L. J. (2012) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2012.00799.x · Cited by 78 · see citing works
Self-citationHo, J. M., Murray, J. H., Demas, G. E., & Goodson, J. L. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.021 · Cited by 76 · see citing works
Curtis, J. T., Liu, Y., Aragona, B. J., & Wang, Z. (2006) · Brain Research · doi:10.1016/j.brainres.2006.07.126 · Cited by 74 · see citing works
Self-citationSteroidal/neuropeptide interactions in hypothalamus and amygdala related to social anxiety
CHOLERIS, E., DEVIDZE, N., KAVALIERS, M., & PFAFF, D. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00424-x · Cited by 75 · see citing works
Donaldson, Z. R., Spiegel, L., & Young, L. J. (2010) · Behavioral Neuroscience · doi:10.1037/a0018094 · Cited by 71 · see citing works
Self-citationOxytocin and vasopressin: signalling, behavioural modulation and potential therapeutic effects
Rae, M., Lemos Duarte, M., Gomes, I., Camarini, R., & Devi, L. A. (2022) · British Journal of Pharmacology · doi:10.1111/bph.15481 · Cited by 72 · see citing works
Vasopressin and pair-bond formation: genes to brain to behavior.
Nair, H. P., & Young, L. J. (2006) · Physiology · doi:10.1152/physiol.00049.2005 · Cited by 68 · see citing works
Self-citationCaldwell, H. K. (2012) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4614-1704-0_12 · Cited by 58 · see citing works
The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives
Blumenthal, S. A., & Young, L. J. (2023) · Biology · doi:10.3390/biology12060844 · Cited by 59 · see citing works
Self-citationSeltzer, L. J., & Ziegler, T. E. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.12.012 · Cited by 58 · see citing works
On switches and knobs, microsatellites and monogamy
Young, L. J., & Hammock, E. A. D. (2007) · Trends in Genetics · doi:10.1016/j.tig.2007.02.010 · Cited by 58 · see citing works
Self-citationα‐Melanocyte‐Stimulating Hormone and Oxytocin: A Peptide Signalling Cascade in the Hypothalamus
Sabatier, N. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01464.x · Cited by 54 · see citing works
A Neuroscientist’s Guide to the Vole
Kenkel, W. M., Gustison, M. L., & Beery, A. K. (2021) · Current Protocols · doi:10.1002/cpz1.175 · Cited by 52 · see citing works
Wudarczyk, O. A., Earp, B. D., Guastella, A., & Savulescu, J. (2013) · Current Opinion in Psychiatry · doi:10.1097/yco.0b013e3283642e10 · Cited by 52 · see citing works
- Authors
- Lim, M. M., Wang, Z., Olazábal, D. E., Ren, X., Terwilliger, E. F., & Young, L. J.
- Affiliations
- Emory University (US)
- Florida State University (US)
- Beth Israel Deaconess Medical Center (US)
- Corresponding author
- Young, Larry J.
- Venue
- Nature
- Published
- 2004-06
- Volume
- 429
- Issue
- 6993
- Pages
- 754-757
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2022927508
- Cited by
- 628
- References
- 29
- Citations by year
- 2026: 19 · 2025: 20 · 2024: 17 · 2023: 17 · 2022: 42 · 2021: 18 · 2020: 18 · 2019: 15 · 2018: 24 · 2017: 27 · 2016: 28 · 2015: 24 · 2014: 32 · 2013: 29 · 2012: 33
- FWCI
- 58.76
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Science Foundation
- 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
- mate preferences, pair bonding, vasopressin V1a receptor, Microtus pennsylvanicus, Microtus ochrogaster, Microtus, evolution of social behavior, ventral forebrain, dopamine, viral gene delivery, monogamy, polygamy, promiscuity
- MeSH terms
- Animals, Choice Behavior, Arvicolinae, Female, Male, Pair Bond, Receptors, Dopamine, Sexual Behavior, Animal, Prosencephalon, Receptors, Vasopressin
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review