The relative contribution of proximal 5′ flanking sequence and microsatellite variation on brain vasopressin 1a receptor (Avpr1a) gene expression and behavior
Open accessAbstract
Certain genes exhibit notable diversity in their expression patterns both within and between species. One such gene is the vasopressin receptor 1a gene (Avpr1a), which exhibits striking differences in neural expression patterns that are responsible for mediating differences in vasopressin-mediated social behaviors. The genomic mechanisms that contribute to these remarkable differences in expression are not well understood. Previous work has suggested that both the proximal 5' flanking region and a polymorphic microsatellite element within that region of the vole Avpr1a gene are associated with variation in V1a receptor (V1aR) distribution and behavior, but neither has been causally linked. Using homologous recombination in mice, we reveal the modest contribution of proximal 5' flanking sequences to species differences in V1aR distribution, and confirm that variation in V1aR distribution impacts stress-coping in the forced swim test. We also demonstrate that the vole Avpr1a microsatellite structure contributes to Avpr1a expression in the amygdala, thalamus, and hippocampus, mirroring a subset of the inter- and intra-species differences observed in central V1aR patterns in voles. This is the first direct evidence that polymorphic microsatellite elements near behaviorally relevant genes can contribute to diversity in brain gene expression profiles, providing a mechanism for generating behavioral diversity both at the individual and species level. However, our results suggest that many features of species-specific expression patterns are mediated by elements outside of the immediate 5' flanking region of the gene.
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In prairie voles, a microsatellite in the 5' flanking region of Avpr1a containing cis-regulatory elements has functional influence over species differences and individual variation in Avpr1a expression and is associated with variation in social behavior.
“In prairie voles, a microsatellite in the 5’ flanking region of the vasopressin receptor gene (Avpr1a) containing cis-REs has been shown to have functional influence over species differences and individual variation in Avpr1a expression and is associated with variation in social behavior (47, 48).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [47]
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 [151]
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King, M.-C., & Wilson, A. C. (1975) · Science · doi:10.1126/science.1090005 · Cited by 2,815 · see citing works
Quandt, K., Frech, K., Karas, H., Wingender, E., & Werner, T. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.23.4878 · Cited by 2,587 · see citing works
Gene Regulation for Higher Cells: A Theory
Britten, R. J., & Davidson, E. H. (1969) · Science · doi:10.1126/science.165.3891.349 · Cited by 2,049 · see citing works
MatInspector and beyond: promoter analysis based on transcription factor binding sites
Cartharius, K., Frech, K., Grote, K., Klocke, B., Haltmeier, M., Klingenhoff, A., Frisch, M., Bayerlein, M., & Werner, T. (2005) · Computer applications in the biosciences · doi:10.1093/bioinformatics/bti473 · Cited by 1,962 · see citing works
Oxytocin 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
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
Microsatellites, from molecules to populations and back
Jarne, P., & Lagoda, P. (1996) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(96)10049-5 · Cited by 1,561 · see citing works
Recognition memory: What are the roles of the perirhinal cortex and hippocampus?
Brown, M. W., & Aggleton, J. P. (2001) · Nature reviews. Neuroscience · doi:10.1038/35049064 · Cited by 1,555 · see citing works
The neurobiology of pair bonding.
Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523 · see citing works
Insel, T. R. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.005 · Cited by 1,044 · see citing works
THE LOCUS OF EVOLUTION: EVO DEVO AND THE GENETICS OF ADAPTATION
Hoekstra, H. E., & Coyne, J. A. (2007) · Evolution · doi:10.1111/j.1558-5646.2007.00105.x · Cited by 962 · 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 · see citing works
de Bono, M., & Bargmann, C. I. (1998) · Cell · doi:10.1016/s0092-8674(00)81609-8 · Cited by 819 · see citing works
A genome-wide view of the spectrum of spontaneous mutations in yeast.
Lynch, M., Sung, W., Morris, K., Coffey, N., Landry, C. R., Dopman, E. B., Dickinson, W. J., Okamoto, K., Kulkarni, S., Hartl, D. L., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803466105 · Cited by 708 · see citing works
Lim, M. M., Wang, Z., Olazábal, D. E., Ren, X., Terwilliger, E. F., & Young, L. J. (2004) · Nature · doi:10.1038/nature02539 · Cited by 628 · see citing works
Evolution of a Vertebrate Social Decision-Making Network
O’Connell, L. A., & Hofmann, H. A. (2012) · Science · doi:10.1126/science.1218889 · Cited by 608 · see citing works
Simple sequence repeats as advantageous mutators in evolution
Kashi, Y., & King, D. G. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.03.005 · Cited by 588 · 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
Is Genetic Evolution Predictable?
Stern, D. L., & Courtier‐Orgogozo, V. (2009) · Science · doi:10.1126/science.1158997 · Cited by 524 · see citing works
Young, 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
Walum, 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
Simple sequence repeats as a source of quantitative genetic variation
Kashi, Y., King, D. G., & Soller, M. (1997) · Trends in Genetics · doi:10.1016/s0168-9525(97)01008-1 · Cited by 459 · 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
Engelmann, M., Landgraf, R., & Wotjak, C. T. (2004) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2004.09.001 · Cited by 450 · see citing works
Young (1999) · doi:10.1038/23650 · Cited by 389 · see citing works
Unstable Tandem Repeats in Promoters Confer Transcriptional Evolvability
Vinces, M. D., Legendre, M., Caldara, M., Hagihara, M., & Verstrepen, K. J. (2009) · Science · doi:10.1126/science.1170097 · Cited by 372 · see citing works
Bielsky, 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
The molecular genetic architecture of human personality: beyond self-report questionnaires
Ebstein, R. P. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001814 · Cited by 362 · see citing works
Vasopressin-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
Pitkow, 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-citationKnafo, A., Israel, S., Darvasi, A., Bachner‐Melman, R., Uzefovsky, F., Cohen, L., Feldman, E., Lerer, E., Laiba, E., Raz, Y., et al. (2007) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2007.00341.x · Cited by 294 · see citing works
The contributions of oxytocin and vasopressin pathway genes to human behavior
Ebstein, R. P., Knafo, A., Mankuta, D., Chew, S. H., & Lai, P. S. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.014 · Cited by 283 · see citing works
Engelmann, M., Wotjak, C. T., Neumann, I. D., Ludwig, M., & Landgraf, R. (1996) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00059-3 · Cited by 267 · see citing works
Kim, 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
Eppig, J. T., Blake, J. A., Bult, C. J., Kadin, J. A., Richardson, J. E., & the Mouse Genome Database Group (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr974 · Cited by 243 · see citing works
Young, 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
Yirmiya, N., Rosenberg, C., Levi, S., Salomon, S., Shulman, C., Nemanov, L., Dina, C., & Ebstein, R. P. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001812 · Cited by 232 · see citing works
Thierry, B., Iwaniuk, A. N., & Pellis, S. M. (2000) · Ethology · doi:10.1046/j.1439-0310.2000.00583.x · Cited by 226 · see citing works
Meyer‐Lindenberg, A., Kolachana, B. S., Gold, B., Olsh, A., Nicodemus, K. K., Mattay, V. S., Dean, M. C., & Weinberger, D. R. (2008) · Molecular Psychiatry · doi:10.1038/mp.2008.54 · Cited by 219 · see citing works
Human brain evolution: insights from microarrays
Preuss, T. M., Cáceres, M., Oldham, M. C., & Geschwind, D. H. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1469 · Cited by 215 · see citing works
Examination of AVPR1a as an autism susceptibility gene
Wassink, T. H., Piven, J., Vieland, V. J., Pietila, J., Goedken, R. J., Folstein, S. E., & Sheffield, V. C. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001503 · Cited by 212 · see citing works
Oxytocin 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
Denny, C. A., Burghardt, N. S., Schachter, D., Hen, R., & Drew, M. R. (2011) · Hippocampus · doi:10.1002/hipo.20964 · Cited by 199 · see citing works
Young, 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
The multiple codes of nucleotide sequences
Trifonov, E. N. (1989) · Bulletin of Mathematical Biology · doi:10.1016/s0092-8240(89)80087-4 · Cited by 185 · see citing works
Fish and chips: functional genomics of social plasticity in an African cichlid fish
Renn, S. C. P., Aubin‐Horth, N., & Hofmann, H. A. (2008) · Journal of Experimental Biology · doi:10.1242/jeb.018242 · Cited by 181 · see citing works
Gobrogge, 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
The multiple codes of nucleotide sequences
Trifonov, E. N. (1989) · Bulletin of Mathematical Biology · doi:10.1007/bf02460081 · Cited by 176 · 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
Evolving nonapeptide mechanisms of gregariousness and social diversity in birds
Goodson, J. L., Kelly, A. M., & Kingsbury, M. A. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.005 · Cited by 139 · see citing works
Wang, Z., Young, L. J., Liu, Y., & Insel, T. R. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970224)378:4 · Cited by 135 · 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 · cited 1× · see citing works
“However, a subsequent survey of the Avpr1a locus in several other vole species and, more recently, in Peromyscus species did not support the hypothesis that the presence or absence of the microsatellite element was associated with monogamy [64,69].”
BackgroundDavid, D. J. P., Klemenhagen, K. C., Holick, K. A., Saxe, M., Mendez‐David, I., Santarelli, L., Craig, D. A., Zhong, H., Swanson, C. J., Hegde, L. G., et al. (2007) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.106.109678 · Cited by 131 · see citing works
Greidanus, T. B. V. W., van Ree, J. M., & de Wied, D. (1983) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(83)90036-0 · Cited by 130 · see citing works
Association of vasopressin 1a receptor levels with a regulatory microsatellite and behavior
Hammock, E. A. D., Lim, M. M., Nair, H. P., & Young, L. J. (2005) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2005.00119.x · Cited by 128 · see citing works
Simple sequence repeats: genetic modulators of brain function and behavior
Fondon, J. W., Hammock, E. A. D., Hannan, A. J., & King, D. G. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.03.006 · Cited by 126 · see citing works
Monogamy Evolves through Multiple Mechanisms: Evidence from V1aR in Deer Mice
Turner, L. M., Young, A. R., Römpler, H., Schöneberg, T., Phelps, S. M., & Hoekstra, H. E. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq013 · Cited by 122 · 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
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
Oxytocin and Vasopressin: Genetics and Behavioral Implications
Caldwell, H. K., & Young, W. S. (2006) · Springer eBooks · doi:10.1007/0-387-30395-2_25 · Cited by 113 · see citing works
Promoter architecture and the evolvability of gene expression
Tirosh, I., Barkai, N., & Verstrepen, K. J. (2009) · Journal of Biology · doi:10.1186/jbiol204 · Cited by 108 · see citing works
Ebner, K., Wotjak, C. T., Landgraf, R., & Engelmann, M. (2002) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01869.x · Cited by 104 · see citing works
Venkatesh, B., Si-Hoe, S. L., Murphy, D., & Brenner, S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.23.12462 · Cited by 103 · see citing works
Barrett, 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
Patterns and Trends in Primate Pair Bonds
Fuentes, A. (2002) · International Journal of Primatology · doi:10.1023/a:1019647514080 · Cited by 92 · see citing works
Curley, J. P., Jensen, C. L., Franks, B., & Champagne, F. A. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.013 · Cited by 90 · 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
Thibonnier, M., Graves, M. K., Wagner, M., Chatelain, N., Soubrier, F., Corvol, P. L., Willard, H. F., & Jeunemaı̂tre, X. (2000) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2000.1108 · Cited by 73 · see citing works
Beating the boojum: Comparative approaches to the neurobiology of social behavior
Phelps, S. M., Polly Campbell, A., Zheng, D., & Ophir, A. G. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.06.043 · Cited by 72 · see citing works
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
Donaldson, Z. R., Kondrashov, F. A., Putnam, A. S., Bai, Y., Stoinski, T., Hammock, E. A. D., & Young, L. J. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-180 · Cited by 61 · 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-citationCell‐Specific Expression of the Rat Oxytocin Gene in Transgenic Mice
Young, W. S., Reynolds, K., Shepard, E. A., Gainer, H., & Castel, M. (1990) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1990.tb00660.x · Cited by 58 · see citing works
Vasopressin induction of long‐lasting potentiation of synaptic transmission in the dentate gyrus
Chen, C., Brinton, R. D., Shors, T. J., & Thompson, R. F. (1993) · Hippocampus · doi:10.1002/hipo.450030211 · Cited by 54 · see citing works
Bachner‐Melman, R., Zohar, A. H., Bacon-Shnoor, N., Elizur, Y., Nemanov, L., Gritsenko, I., & Ebstein, R. P. (2005) · Journal of Individual Differences · doi:10.1027/1614-0001.26.1.2 · Cited by 52 · see citing works
Feder, M. E. (2007) · Journal of Experimental Biology · doi:10.1242/jeb.02725 · Cited by 38 · see citing works
Mating system and avpr1a promoter variation in primates
Rosso, L., Keller, L., Kaessmann, H., & Hammond, R. L. (2008) · Biology Letters · doi:10.1098/rsbl.2008.0122 · Cited by 36 · see citing works
Allen Brain Atlas maps 21 000 genes of the mouse brain
McCarthy, M. (2006) · The Lancet Neurology · doi:10.1016/s1474-4422(06)70594-4 · Cited by 30 · see citing works
Effects of arginine-vasopressin (AVP) on long-term potentiation in intact anesthetized rats
Dubrovsky, B. O., Tatarinov, A. L., Gijsbers, K., Harris, J., & Tsiodras, A. (2003) · Brain Research Bulletin · doi:10.1016/s0361-9230(02)00961-9 · Cited by 25 · see citing works
Bovine Oxytocin Transgenes in Mice
Ho, M.-Y., Carter, D., Ang, H., & Murphy, D. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.45.27199 · Cited by 20 · see citing works
Wang, Z., LIU, Y., Young, L. J., & Insel, T. R. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51954.x · Cited by 19 · see citing works
Belenky, M. A., Castel, M., Young, W. S., Gainer, H., & Cohen, S. (1992) · Brain Research · doi:10.1016/s0006-8993(10)80034-4 · Cited by 19 · see citing works
Yang, J., Pan, Y.-J., Yin, Z., Hai, G.-F., Lu, L., Zhao, Y. Y., Wang, D., Wang, H., & Wang, G. (2012) · Neuropeptides · doi:10.1016/j.npep.2012.03.003 · Cited by 16 · see citing works
Ho, M.-Y., & Murphy, D. (1997) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(97)00208-6 · Cited by 11 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [82]Bielsky IF, Hu S-B, Ren X, Terwilliger EF, Young LJ (2005) The V1a Vasopressin Receptor Is Necessary and Sufficient for Normal Social Recognition: A Gene Replacement Study. Neuron 47: 503– 513. 16102534
Cited by
Sorted by citations
King, L. B., Walum, H., Inoue, K., Eyrich, N. W., & Young, L. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.12.008 · Cited by 191 · see citing works
“In prairie voles, a microsatellite in the 50 flanking region of the vasopressin receptor gene (Avpr1a) containing cis-REs has been shown to have functional influence over species differences and individual variation in Avpr1a expression and is associated with variation in social behavior (46,47).”
Albers, H. E. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.07.001 · Cited by 200 · see citing works
Oxytocin, 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
Functional Mechanisms of Microsatellite DNA in Eukaryotic Genomes
Bagshaw, A. (2017) · Genome Biology and Evolution · doi:10.1093/gbe/evx164 · Cited by 151 · see citing works
Park, S. G., Hannenhalli, S. S., & Choi, S. S. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-526 · Cited by 82 · see citing works
Genetic Influences on Receptive Joint Attention in Chimpanzees (Pan troglodytes)
Hopkins, W. D., Keebaugh, A. C., Reamer, L. A., Schaeffer, J. A., Schapiro, S. J., & Young, L. J. (2014) · Scientific Reports · doi:10.1038/srep03774 · Cited by 69 · see citing works
Modulation of social behavior by distinct vasopressin sources
Rigney, N., Vries, G. J. D., & Petrulis, A. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1127792 · Cited by 61 · see citing works
Staes, N., Stevens, J. M. G., Helsen, P., Hillyer, M. J., Korody, M. L., & Eens, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113364 · Cited by 60 · see citing works
Coevolution of Genome Architecture and Social Behavior
Rubenstein, D. R., Ågren, J. A., Carbone, L., Elde, N. C., Hoekstra, H. E., Kapheim, K. M., Keller, L., Moreau, C. S., Toth, A. L., Yeaman, S., et al. (2019) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2019.04.011 · Cited by 55 · see citing works
Staes, N., Koski, S. E., Helsen, P., Fransén, E., Eens, M., & Stevens, J. M. G. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.08.006 · Cited by 52 · 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
Reconciling the deep homology of neuromodulation with the evolution of behavior
Katz, P. S., & Lillvis, J. L. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.05.002 · Cited by 50 · see citing works
Balancing selection maintains polymorphisms at neurogenetic loci in field experiments
Lönn, E., Koskela, E., Mappes, T., Mökkönen, M., Sims, A. M., & Watts, P. C. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1621228114 · Cited by 39 · see citing works
SVA retrotransposons as potential modulators of neuropeptide gene expression
Gianfrancesco, O., Bubb, V. J., & Quinn, J. P. (2016) · Neuropeptides · doi:10.1016/j.npep.2016.09.006 · Cited by 33 · see citing works
Mahovetz, L. M., Young, L. J., & Hopkins, W. D. (2016) · Genes Brain & Behavior · doi:10.1111/gbb.12291 · Cited by 32 · see citing works
Johnson, K. V. ‐., & Burnet, P. W. J. (2020) · BMC Neuroscience · doi:10.1186/s12868-020-00583-3 · Cited by 31 · see citing works
Sadino, J. M., & Donaldson, Z. R. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.7b00475 · Cited by 28 · see citing works
Schaschl, H., Huber, S., Schæfer, K., Windhager, S., Wallner, B., & Fieder, M. (2015) · BMC Evolutionary Biology · doi:10.1186/s12862-015-0372-7 · Cited by 27 · see citing works
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Tickerhoof, M. C., & Smith, A. S. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00265 · Cited by 25 · see citing works
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Mulholland, M. M., Navabpour, S., Mareno, M. C., Schapiro, S. J., Young, L. J., & Hopkins, W. D. (2020) · Genes Brain & Behavior · doi:10.1111/gbb.12631 · Cited by 22 · see citing works
Charles, R., Sakurai, T., Takahashi, N., Elder, G. A., Sosa, M. A. G., Young, L. J., & Buxbaum, J. D. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.017053 · Cited by 23 · see citing works
Watts, P. C., Kallio, E. R. K., Koskela, E., Lönn, E., Mappes, T., & Mökkönen, M. (2017) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.1896 · Cited by 22 · see citing works
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Závodná, M., Bagshaw, A., Bräuning, R., & Gemmell, N. J. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1253 · Cited by 20 · see citing works
Nishitani, S., Ikematsu, K., Takamura, T., Honda, S., Yoshiura, K.-I., & Shinohara, K. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.09.010 · Cited by 19 · see citing works
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Kuo, D., De‐Miguel, F. F., Heath-Heckman, E., Szczupak, L., Todd, K., Weisblat, D. A., & Winchell, C. J. (2020) · Evolution & Development · doi:10.1111/ede.12358 · Cited by 14 · see citing works
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YOUNG, L. J., & ZHANG, Q. (2021) · Japanese Journal of Animal Psychology · doi:10.2502/janip.71.1.4 · Cited by 13 · see citing works
Bagshaw, A., Horwood, L. J., Fergusson, D. M., Gemmell, N. J., & Kennedy, M. A. (2017) · BMC Medical Genetics · doi:10.1186/s12881-017-0374-y · Cited by 12 · see citing works
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Zhang, L., Liu, J., Cheng, P., & Lv, F. (2019) · Bioscience Reports · doi:10.1042/bsr20182232 · Cited by 12 · see citing works
Polymorphic variation as a driver of differential neuropeptide gene expression
Quinn, J. P., Warburton, A., Myers, P., Pfaff, A. L., & Bubb, V. J. (2013) · Neuropeptides · doi:10.1016/j.npep.2013.10.003 · Cited by 11 · see citing works
Keane, B., Parsons, S., Smucker, B. J., & Solomon, N. G. (2014) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-014-1801-0 · Cited by 11 · see citing works
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Konner, M. J. (2021) · Human Nature · doi:10.1007/s12110-021-09414-8 · Cited by 10 · see citing works
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Beery, A. K., Kamal, Y., Sobrero, R., & Hayes, L. D. (2016) · Wiley eBooks · doi:10.1002/9781118846506.ch3 · Cited by 9 · see citing works
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Tanaka, H., Nishina, K., Shou, Q., Takahashi, H., Sakagami, M., Matsuda, T., Inoue‐Murayama, M., & Takagishi, H. (2023) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2023.0378 · Cited by 7 · see citing works
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Carmel-Gross, I., Levy, E., Armon, L., Yaron, O., Ben‐Asher, H. W., & Urbach, A. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.10.002 · Cited by 8 · see citing works
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Ávila‐González, D., Young, L. J., Camacho, F., Paredes, R. G., Díaz, N. F., & Portillo, W. (2020) · Journal of Visualized Experiments · doi:10.3791/61402 · Cited by 7 · see citing works
Tandon, D., Enikö Kubinyi, B., Sándor, S., Faughnan, H., Miklósi, Á., & vonHoldt, B. M. (2024) · BMC Genomics · doi:10.1186/s12864-024-10614-6 · Cited by 6 · see citing works
Stay social, stay young: a bioanthropological outlook on the processes linking sociality and ageing
Iannuzzi, V., Narboux‐Nême, N., Lehoczki, A., Levi, G., & Giuliani, C. (2024) · GeroScience · doi:10.1007/s11357-024-01416-5 · Cited by 6 · see citing works
Vasopressin: Roles in Modulating Social Behaviors
Williams, S. K., & Cymerblit‐Sabba, A. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00057-2 · Cited by 5 · see citing works
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King, L. B., & Young, L. J. (2016) · Wiley eBooks · doi:10.1002/9781118760369.ch19 · Cited by 5 · see citing works
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Mökkönen, M., Koskela, E., Procyshyn, T. L., & Crespi, B. J. (2018) · The American Naturalist · doi:10.1086/698216 · Cited by 4 · see citing works
Is Infidelity Biologically Determined?
Balon, R. (2016) · Current Sexual Health Reports · doi:10.1007/s11930-016-0084-z · Cited by 3 · see citing works
Linked OXTR Variants Are Associated With Social Behavior Differences in Bonobos ( Pan paniscus )Preprint
Skiba, S. A., McCall, R., Byers, A., Waldron, S., Epping, A. J., & Taglialatela, J. P. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.22.573122 · Cited by 2 · see citing works
Abuelanin, M., Kaya, G., Lake, J. A., Lambert, C. C., Wu, M. V., Berendzen, K. M., Wood, J., Krasheninnikova, K., Solomon, N. G., Donaldson, Z. R., et al. (2026) · Cell Genomics · doi:10.1016/j.xgen.2026.101336 · Cited by 1 · see citing works
Oxytocin, Vasopressin, and Sex Differences in Social Behavior. It’s Complicated!
Veney, S. L., & Caldwell, H. K. (2024) · Masterclass in neuroendocrinology · doi:10.1007/978-3-031-51112-7_5 · Cited by 1 · see citing works
Is Infidelity Biologically Determined?
Balon, R. (2015) · European Psychiatry · doi:10.1016/s0924-9338(15)30061-4 · Cited by 1 · see citing works
Lönn, E. (2017) · Jyväskylä University Digital Archive (University of Jyväskylä)
Kean, C. E., Radchenko, E. A., Lindenbaum, N. M., Materne, G., & Mirkin, S. M. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.09.687482
Oxytocin, vasopressin, and their crosstalk in sexually-dimorphic psychiatric conditions
Yamasue, H. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106641
Kean, C. E., Radchenko, E. A., Lindenbaum, N. M., Materne, G., & Mirkin, S. M. (2026) · NAR Molecular Medicine · doi:10.1093/narmme/ugag032
- Authors
- Donaldson, Z. R., & Young, L. J.
- Affiliations
- Emory University (US)
- Corresponding author
- Donaldson, Zoe R.
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-08-29
- Volume
- 9
- Issue
- 8
- Pages
- e1003729
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3757045
- OpenAlex
- W2027725231
- Cited by
- 52
- References
- 84
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 3 · 2023: 3 · 2022: 1 · 2021: 3 · 2020: 6 · 2019: 2 · 2018: 2 · 2017: 7 · 2016: 8 · 2015: 4 · 2014: 8 · 2013: 1
- FWCI
- 10.48
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Columbia Academic Commons (Columbia University)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (P51RR165, P51OD011132)
- Yerkes National Primate Research Center, Emory University (P51OD11132, /OD P51OD11132)
- National Institute of Mental Health (K02MH064692, MH064692, R29MH056897, MH056897, R01MH056897, T32MH015144)
- National Center for Research Resources (OD P51OD11132, P51RR165, P51-OD11132)
- Office of Research Infrastructure Programs, National Institutes of Health (ODP51OD11132, P51RR165, P51OD11132)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- vasopressin 1a receptor, AVPR1A, 5'-flanking region, microsatellite polymorphism, brain gene expression, voles, social behavior, stress coping, forced swim test, amygdala, thalamus, hippocampus, homologous recombination, behavioral diversity
- MeSH terms
- Animals, Behavior, Animal, Brain, Arvicolinae, Humans, Polymorphism, Genetic, Species Specificity, Gene Expression, Receptors, Vasopressin, Microsatellite Repeats, Gene Expression Profiling, 5' Flanking Region, Mice, Homologous Recombination
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