Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults
Open accessAbstract
Oxytocin receptors (OXTR) in the nucleus accumbens (NAcc) promote alloparental behavior and partner preference formation in female prairie voles. Within the NAcc there is significant individual variation in OXTR binding and virgin juvenile and adult females with a high density of OXTR in the NAcc display an elevated propensity to engage in alloparental behavior toward novel pups. Over-expression of OXTR in the NAcc of adult female prairie voles using viral vector gene transfer facilitates partner preference formation, but has no effect on alloparental behavior, even though OXTR antagonists infused into the NAcc blocks both behaviors. We therefore hypothesized that long-term increases in OXTR signaling during development may underlie the relationship between adult OXTR density in the NAcc and alloparental behavior. To test this hypothesis, we used viral vector gene transfer to increase OXTR density in the NAcc of prepubertal, 21day old female prairie voles and tested for both alloparental behavior and partner preference formation as adults. Consistent with a developmental impact of OXTR signaling, adults over-expressing OXTR from weaning display both increased alloparental behavior and partner preference formation. Thus, the relatively acute impact of elevated OXTR signaling in the NAcc on partner preference formation previously reported appears to be dissociable from the effects of longer term, developmentally relevant OXTR signaling necessary for modulating alloparental behavior. These results are consistent with the hypothesis that oxytocin can have both long-term "organizational" effects as well as acute "activational" effects on affiliative behaviors.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Viral knockdown of OXTRs within the NAc of voles disrupts partner preference formation and alloparental behavior; increasing OXTR expression in the NAc facilitates pair bonding and maternal care.
“Additionally, viral knockdown of OXTRs within the NAc of voles disrupts partner preference formation and alloparental behavior; however, pair bonding and maternal care are facilitated when OXTR expression in the NAc is increased, suggesting a direct role of NAc OXTRs in driving affiliative behavior [15,140].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [140]
The Introduction and Discussion report that blocking NAc OXTRs with antagonists disrupts alloparental behavior and partner preference formation, not that viral knockdown does so. The paper's experiment supports the other half of the claim: viral OXTR overexpression in prepubertal female prairie voles increased partner preference formation and alloparental care in adulthood. The care measured was toward pups in females that were not mothers, rather than maternal care by mothers; page numbers were not available in our copy. (LLM, conf=0.90)
Experimental — accuracy not yet measuredPrairie voles are highly nurturing, and virgin females can display spontaneous levels of maternal care depending on density of nucleus accumbens oxytocin receptors.
“Prairie voles are highly nurturing, and virgin females can display spontaneous levels of maternal care depending on density of nucleus accumbens oxytocin receptors”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Keebaugh & Young 2011
Decreasing OXTR density in the nucleus accumbens using RNA interference inhibits partner preference formation.
“Increasing OXTR density in the NAcc using viral-vector mediated gene transfer facilitates partner preference formation, while decreasing OXTR density in the same region using RNA interference inhibits such bonding (37–39).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [37]
Increasing OXTR density in the nucleus accumbens using viral-vector mediated gene transfer facilitates partner preference formation.
“Increasing OXTR density in the NAcc using viral-vector mediated gene transfer facilitates partner preference formation, while decreasing OXTR density in the same region using RNA interference inhibits such bonding (37–39).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [37]
Differences in pair bonding behavior are mediated by OXTR variation.
“and OXTR variation mediates individual differences in pair bonding behaviors (37–39).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [37]
In prairie voles, spontaneous maternal behavior in virgin females is organized by developmental OTR levels in the NAC shell and is prevented by OTR antagonist injected there.
“Additionally, in prairie voles, the expression of spontaneous maternal behavior in virgin females is organized by developmental (and not adult) levels of OTR in the NAC shell, and is prevented by OTR antagonist injected into this region (Olazabal and Young 2006a; Ross et al 2009b; Keebaugh and Young 2011).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Keebaugh and Young 2011
Intra-NAc OT receptor activation facilitates partner preference formation in female, but not male, prairie voles.
“several studies have characterized the role of intra-NAc OR activation in facilitating partner preference formation in female, but not male, prairie voles”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Keebaugh and Young 2011
Viral-mediated small interfering RNA knockdown of OXTR in the nucleus accumbens of prairie voles inhibits partner preference, while overexpressing NAcc OXTR enhances partner preference formation.
“Viral-mediated small interfering RNA knockdown of OXTR in NAcc of prairie voles inhibits partner preference (138), while overexpressing NAcc OXTR enhances partner preference formation (139).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [139]
The density of NAc OXTR correlates with preferences for an individual.
“Furthermore, OXTR signaling in the NAc plays a critical role for the formation of a preference for an individual, and the density of NAc OXTR correlates with such preferences 27–29.”
From Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles (2022) · cites this paper as [29]
OXTR signaling in the nucleus accumbens plays a critical role for the formation of a preference for an individual.
“Furthermore, OXTR signaling in the NAc plays a critical role for the formation of a preference for an individual, and the density of NAc OXTR correlates with such preferences 27–29.”
From Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles (2022) · cites this paper as [29]
Experimentally increasing or decreasing OXTR expression in the prairie vole nucleus accumbens modulated partner preference behavior.
“experimentally increasing9 or decreasing10 OXTR expression in the prairie vole nucleus accumbens modulated partner preference behavior”
From Oxytocin pathway gene networks in the human brain (2019) · cites this paper as [9]
Animal models demonstrate that OXTR expression levels directly modulate social behavior.
“animal models demonstrating that OXTR expression levels directly modulate social behavior9,10”
From Oxytocin pathway gene networks in the human brain (2019) · cites this paper as [9]
Increased OXTR gene expression is associated with increased oxytocin binding.
“and that increased OXTR gene expression is associated with increased oxytocin binding”
From Oxytocin pathway gene networks in the human brain (2019) · cites this paper as [9]
Injecting an adeno-associated viral vector overexpressing the oxytocin receptor into the nucleus accumbens shell of female prairie voles at postnatal day 21 facilitates alloparental care, as measured by reductions in approach times and increases in time spent licking and grooming pups compared to controls.
“By injecting an adeno-associated viral vector into the nucleus accumbens (NAcc) shell of female prairie voles at PND21 they were able to facilitate alloparental care, as measured by reductions in approach times and increases in time spent licking and grooming pups compared to controls (57).”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [57]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Oxytocin increases trust in humans
Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., & Fehr, E. (2005) · Nature · doi:10.1038/nature03701 · Cited by 3,690 · see citing works
PHOENIX, C. H., GOY, R. W., GERALL, A. A., & YOUNG, W. C. (1959) · Endocrinology · doi:10.1210/endo-65-3-369 · Cited by 1,934 · see citing works
The neurobiology of pair bonding.
Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523 · cited 1× · see citing works
“In contrast to traditional laboratory models like mouse and rat, prairie voles (Microtus ochrogaster) are genetically diverse microtine rodents that possess a rich repertoire of social behaviors, including pair bonding between mates and biparental care (Carter et al., 1995; Young and Wang, 2004).”
ResultOxytocin improves “mind-reading” in humans
Domes, G., Heinrichs, M., Michel, A., Berger, C., & Herpertz, S. C. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.07.015 · Cited by 1,298 · see citing works
Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders.
Guastella, A. J., Einfeld, S. L., Gray, K. M., Rinehart, N. J., Tonge, B. J., Lambert, T. J., & Hickie, I. B. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.09.020 · Cited by 962 · see citing works
Promoting social behavior with oxytocin in high-functioning autism spectrum disorders.
Andari, E., Duhamel, J.-R., Zalla, T., Herbrecht, E., Leboyer, M., & Sirigu, A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910249107 · Cited by 941 · see citing works
Pedersen, C. A., & Prange, A. J. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.12.6661 · Cited by 841 · see citing works
Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles
Insel, T. R., & Shapiro, L. E. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.13.5981 · Cited by 833 · see citing works
Oxytocin increases gaze to the eye region of human faces
Guastella, A. J., Mitchell, P. B., & Dadds, M. R. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.06.026 · Cited by 798 · see citing works
Ditzen, B., Schaer, M., Gabriel, B., Bodenmann, G., Ehlert, U., & Heinrichs, M. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.10.011 · Cited by 784 · cited 1× · see citing works
“In humans, OT has been shown to modulate social behavior, including interpersonal trust, eye gaze, facial memory, and emotion perception (Ditzen et al., 2009; Domes et al., 2007; Guastella et al., 2008; Kosfeld et al., 2005).”
BackgroundOxytocin Increases Retention of Social Cognition in Autism
Hollander, E., Bartz, J., Chaplin, W., Phillips, A., Sumner, J., Soorya, L., Anagnostou, E., & Wasserman, S. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.05.030 · Cited by 693 · see citing works
Physiological substrates of mammalian monogamy: The prairie vole model
Sue Carter, C., Courtney Devries, A., & Getz, L. L. (1995) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(94)00070-h · Cited by 615 · see citing works
Back to the future: The organizational-activational hypothesis adapted to puberty and adolescence
Schulz, K. M., Molenda-Figueira, H. A., & Sisk, C. L. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.03.010 · Cited by 587 · see citing works
Genomic and epigenetic evidence for oxytocin receptor deficiency in autism
Gregory, S. G., Connelly, J. J., Towers, A. J., Johnson, J., Biscocho, D., Markunas, C. A., Lintas, C., Abramson, R. K., Wright, H. H., Ellis, P., et al. (2009) · BMC Medicine · doi:10.1186/1741-7015-7-62 · Cited by 576 · see citing works
Cellular Mechanisms of Social Attachment
Young, L. J., Lim, M. M., Gingrich, B., & Insel, T. R. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1691 · Cited by 523 · see citing works
Self-citationWilliams, J. R., Insel, T. R., Harbaugh, C. R., & Carter, C. S. (1994) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1994.tb00579.x · Cited by 483 · see citing works
Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep
Kendrick, K. M., Keverne, E. B., & Baldwin, B. A. (2008) · Neuroendocrinology · doi:10.1159/000124796 · Cited by 373 · see citing works
Developmental consequences of oxytocin
Carter, C. S. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00151-3 · Cited by 367 · 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
Neural control of maternal behaviour and olfactory recognition of offspring
Kendrick, K. M., Da Costa, A. P. C., Broad, K. D., Ohkura, S., Guevara, R., Lévy, F., & Keverne, E. B. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00218-9 · Cited by 311 · see citing works
Characterization of the oxytocin system regulating affiliative behavior in female prairie voles
Ross, H. E., Cole, C. D., Smith, Y., Neumann, I. D., Landgraf, R., Murphy, A. Z., & Young, L. J. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.05.055 · Cited by 309 · see citing works
Olazábal, D. E., & Young, L. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.04.017 · Cited by 289 · see citing works
Ahern, T. H. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.017.2009 · Cited by 239 · see citing works
Olazábal, D. E., & Young, L. J. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.010 · Cited by 230 · see citing works
Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles
Bales, K. L., Kim, A. J., Lewis-Reese, A. D., & Sue Carter, C. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.01.004 · Cited by 217 · see citing works
Bales, K. L., & Carter, C. S. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00154-5 · Cited by 195 · see citing works
Bales, K. L., & Carter, C. S. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.4.854 · Cited by 155 · see citing works
Bales, K. L., Plotsky, P. M., Young, L. J., Lim, M. M., Grotte, N., Ferrer, E., & Carter, C. S. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.09.009 · Cited by 150 · see citing works
WILLIAMS, J. R., CARTER, C. S., & INSEL, T. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34393.x · Cited by 147 · see citing works
Porges, C. C., & Getz, L. (1996) · American Scientist · Cited by 122 · see citing works
Wang, Z., & Novak, M. A. (1992) · Journal of comparative psychology · doi:10.1037/0735-7036.106.2.163 · Cited by 114 · see citing works
Lonstein, J. S., & Vries, G. J. D. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00270-4 · Cited by 113 · see citing works
Ahern, T. H., Hammock, E. A. D., & Young, L. J. (2011) · Developmental Psychobiology · doi:10.1002/dev.20498 · Cited by 113 · see citing works
Bales, K. L., Pfeifer, L. A., & Carter, C. S. (2004) · Developmental Psychobiology · doi:10.1002/dev.10165 · Cited by 107 · see citing works
Developmental effects of oxytocin on stress response: Single versus repeated exposure
KRAMER, K., CUSHING, B., & CARTER, C. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00175-6 · Cited by 79 · see citing works
Oxytocin Receptors and Maternal Behavior
Insel, T. R., & SHAPIRO, L. E. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34350.x · Cited by 79 · see citing works
Evaluation of two automated metrics for analyzing partner preference tests
Ahern, T. H., Modi, M. E., Burkett, J. P., & Young, L. J. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.06.010 · Cited by 79 · see citing works
Neonatal manipulation of oxytocin affects expression of estrogen receptor alpha
Yamamoto, Y., Carter, C. S., & Cushing, B. S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.065 · Cited by 70 · see citing works
Organizational effects of oxytocin on serotonin innervation
Eaton, J. L., Roache, L., Nguyen, K. N., Cushing, B. S., Troyer, E., Papademetriou, E., & Raghanti, M. A. (2012) · Developmental Psychobiology · doi:10.1002/dev.20566 · Cited by 63 · see citing works
Olazábal, D. E., & Young, L. J. (2005) · Developmental Psychobiology · doi:10.1002/dev.20077 · Cited by 58 · see citing works
Lonstein, J. S., & Vries, G. J. D. (2001) · Journal of comparative psychology · doi:10.1037/0735-7036.115.1.53 · Cited by 55 · see citing works
Lonstein, J. S., & Vries, G. J. D. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00192-3 · Cited by 52 · see citing works
Field, E. F., Whishaw, I. Q., Forgie, M. L., & Pellis, S. M. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.6.1293 · Cited by 40 · see citing works
Kramer, K. M., Yoshida, S., Papademetriou, E., & Cushing, B. S. (2007) · BMC Neuroscience · doi:10.1186/1471-2202-8-71 · Cited by 36 · see citing works
Swithers, S. E., McCurley, M., Hamilton, E., & Doerflinger, A. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.05.009 · Cited by 30 · see citing works
Lipschitz, D. L., Crowley, W. R., & Bealer, S. L. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01052.x · Cited by 29 · see citing works
Perry, A. N., Paramadilok, A., & Cushing, B. S. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.08.021 · Cited by 26 · see citing works
Flagged first, then by citations
1 of the 48 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Oxytocin, Neural Plasticity, and Social Behavior
Froemke, R. C., & Young, L. J. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-102320-102847 · Cited by 487 · see citing works
“Prairie voles are highly nurturing, and virgin females can display spontaneous levels of maternal care depending on density of nucleus accumbens oxytocin receptors (Olazábal & Young 2006, Keebaugh & Young 2011).”
BackgroundThe 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
Numan, M., & Young, L. J. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.015 · Cited by 355 · see citing works
Self-citationEnvironmental influence in the brain, human welfare and mental health
Tost, H., Champagne, F. A., & Meyer‐Lindenberg, A. (2015) · Nature Neuroscience · doi:10.1038/nn.4108 · Cited by 349 · see citing works
Oxytocin pathway gene networks in the human brain
Quintana, D. S., Rokicki, J., van der Meer, D., Alnæs, D., Kaufmann, T., Córdova-Palomera, A., Dieset, I., Andreassen, O. A., & Westlye, L. T. (2019) · Nature Communications · doi:10.1038/s41467-019-08503-8 · Cited by 354 · see citing works
Burkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307 · see citing works
“Additionally, in prairie voles, the expression of spontaneous maternal behavior in virgin females is organized by developmental (and not adult) levels of OTR in the NACs and is prevented by OTR antagonist injected into this region (Olazabal and Young 2006a; Ross et al. 2009b; Keebaugh and Young 2011).”
Castro, D. C., & Bruchas, M. R. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.003 · Cited by 287 · 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
The oxytocin system in drug discovery for autism: Animal models and novel therapeutic strategies
Modi, M. E., & Young, L. J. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.010 · Cited by 218 · see citing works
Oxytocin signaling in the lateral septum prevents social fear during lactation
Menon, R., Grund, T., Zoicas, I., Althammer, F., Fiedler, D., Biermeier, V., Bosch, O. J., Hiraoka, Y., Nishimori, K., Eliava, M., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.02.044 · Cited by 211 · 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
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
“MLR, the NAcc, OXTR activation is necessary for prairie vole partner preference formation (35) and OXTR variation mediates individual differences in pair bonding behaviors (37-39).”
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
MacDonald, K., & Feifel, D. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00035 · Cited by 181 · see citing works
Histone deacetylase inhibitors facilitate partner preference formation in female prairie voles
Wang, H., Duclot, F., Liu, Y., Wang, Z., & Kabbaj, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3420 · Cited by 173 · see citing works
Neurobiological mechanisms of social attachment and pair bonding
Johnson, Z. V., & Young, L. J. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.01.009 · Cited by 169 · see citing works
Self-citationMarsh, A. A. (2018) · Annual Review of Psychology · doi:10.1146/annurev-psych-010418-103010 · Cited by 164 · see citing works
Oxytocin and Social Relationships: From Attachment to Bond Disruption
Bosch, O. J., & Young, L. J. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_10 · Cited by 162 · see citing works
Self-citationEarly nurture epigenetically tunes the oxytocin receptor
Perkeybile, A. M., Carter, C. S., Wroblewski, K. L., Puglia, M. H., Kenkel, W. M., Lillard, T. S., Karaoli, T., Gregory, S. G., Mohammadi, N., Epstein, L., et al. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.08.037 · Cited by 160 · see citing works
Keebaugh, A. C., Barrett, C. E., Laprairie, J. L., Jenkins, J. J., & Young, L. J. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1040893 · Cited by 150 · see citing works
Oxytocin׳s role in anxiety: A critical appraisal
MacDonald, K., & Feifel, D. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.025 · Cited by 139 · see citing works
Intranasal oxytocin increases covert attention to positive social cues
Domes, G., Sibold, M., Schulze, L., Lischke, A., Herpertz, S. C., & Heinrichs, M. (2013) · Psychological Medicine · doi:10.1017/s0033291712002565 · Cited by 130 · see citing works
Dogs' endocrine and behavioural responses at reunion are affected by how the human initiates contact
Rehn, T., Handlin, L., Uvnäs‐Moberg, K., & Keeling, L. J. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.10.009 · Cited by 127 · see citing works
Bethlehem, R. A. I., Baron-Cohen, S., van Honk, J., Auyeung, B., & Bos, P. A. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00048 · Cited by 120 · see citing works
The neurobiological causes and effects of alloparenting
Kenkel, W. M., Perkeybile, A. M., & Carter, C. S. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22465 · Cited by 120 · see citing works
Oxytocin receptor is not required for social attachment in prairie voles
Berendzen, K. M., Sharma, R., Alvarado, M., Wei, Y., Rogers, F. D., Simmons, T. C., Seelke, A. M. H., Bond, J. M., Larios, R., Goodwin, N. L., et al. (2023) · Neuron · doi:10.1016/j.neuron.2022.12.011 · Cited by 120 · see citing works
Barrett, C. E., Arambula, S. E., & Young, L. J. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.73 · Cited by 115 · see citing works
Oxytocin Acts in Nucleus Accumbens to Attenuate Methamphetamine Seeking and Demand
Cox, B. M., Bentzley, B. S., Regen-Tuero, H. C., See, R. E., Reichel, C. M., & Aston‐Jones, G. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.11.011 · Cited by 98 · see citing works
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
Flexibility and adaptation of the neural substrate that supports maternal behavior in mammals
Olazábal, D. E., Pereira, M., Agrati, D., Ferreira, A., Fleming, A. S., González-Mariscal, G., Lévy, F., Lucion, A. B., Morrell, J. I., Numan, M., et al. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.04.004 · Cited by 97 · see citing works
Pohl, T. T., Young, L. J., & Bosch, O. J. (2019) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2017.12.011 · Cited by 83 · see citing works
Self-citationThe Monogamy Paradox: What Do Love and Sex Have to Do With It?
Carter, C. S., & Perkeybile, A. M. (2018) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2018.00202 · Cited by 85 · see citing works
Oxytocin during Development: Possible Organizational Effects on Behavior
Miller, T. V., & Caldwell, H. K. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00076 · Cited by 79 · see citing works
Perkeybile, A. M., Delaney-Busch, N., Hartman, S., Grimm, K. J., & Bales, K. L. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00191 · Cited by 76 · see citing works
Loth, M. K., & Donaldson, Z. R. (2020) · Endocrinology · doi:10.1210/endocr/bqaa223 · Cited by 74 · see citing works
Oxytocin in Schizophrenia: Pathophysiology and Implications for Future Treatment
Goh, K. K., Chen, C.-H., & Lane, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22042146 · 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
Numan, M. (2020) · doi:10.1093/oso/9780190848675.001.0001 · Cited by 101 · see citing works
Sex- and context-dependent effects of oxytocin on social sharing
Ma, X., Zhao, W., Luo, R., Zhou, F., Geng, Y., Xu, L., Gao, Z., Zheng, X., Becker, B., & Kendrick, K. M. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.08.004 · Cited by 64 · see citing works
Improving the precision of intranasal oxytocin research
Winterton, A., Westlye, L. T., Steen, N. E., Andreassen, O. A., & Quintana, D. S. (2020) · Nature Human Behaviour · doi:10.1038/s41562-020-00996-4 · Cited by 62 · see citing works
Titi Monkeys as a Novel Non-Human Primate Model for the Neurobiology of Pair Bonding .
Bales, K. L., Razo, R. A., Conklin, Q. A., Hartman, S., Mayer, H. S., Rogers, F. D., Simmons, T. C., Smith, L. K., Williams, A. V., Williams, D. R., et al. (2017) · Europe PMC (PubMed Central) · Cited by 62 · 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
New opportunities in vasopressin and oxytocin research: a perspective from the amygdala.
Stoop, R., Hegoburu, C., & van den Burg, E. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-033904 · Cited by 56 · see citing works
Region Specific Up-Regulation of Oxytocin Receptors in the Opioid Oprm1−/− Mouse Model of Autism
Gigliucci, V., Leonzino, M., Busnelli, M., Luchetti, A., Palladino, V. S., D’Amato, F. R., & Chini, B. (2014) · Frontiers in Pediatrics · doi:10.3389/fped.2014.00091 · Cited by 56 · see citing works
Glasper, E. R., Kenkel, W. M., Bick, J. R., & Rilling, J. K. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.02.005 · Cited by 54 · see citing works
Neurogenomics of Behavioral Plasticity
Harris, R. M., & Hofmann, H. A. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-7347-9_8 · Cited by 49 · see citing works
Duclot, F., Wang, H., Youssef, C., Liu, Y., Wang, Z., & Kabbaj, M. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.04.001 · Cited by 52 · see citing works
The interplay of oxytocin and sex hormones
Quintana, D. S., Glaser, B. D., Kang, H., Kildal, E. S.-M., Audunsdottir, K., Sartorius, A. M., & Barth, C. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105765 · Cited by 54 · see citing works
Wang, B., Wang, L., Wang, K., & Tai, F. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.02.043 · Cited by 50 · see citing works
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
Developmental effects of oxytocin neurons on social affiliation and processing of social information
Nunes, A. R., Gliksberg, M., Varela, S. A. M., Teles, M., Wircer, E., Blechman, J., Petri, G., Levkowitz, G., & Oliveira, R. F. (2021) · The Journal of Neuroscience · doi:10.1523/jneurosci.2939-20.2021 · Cited by 47 · see citing works
Role of oxytocin in parental behaviour
Olazábal, D. E. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12594 · Cited by 47 · see citing works
Sexual dimorphism of oxytocin and vasopressin in social cognition and behavior
Lu, Q., Lai, J., Du, Y., Huang, T., Prukpitikul, P., Xu, Y., & Hu, S. (2019) · Psychology Research and Behavior Management · doi:10.2147/prbm.s192951 · Cited by 45 · 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
Paraventricular nucleus oxytocin subsystems promote active paternal behaviors in mandarin voles
He, Z., Zhang, L., Hou, W., Zhang, X., Young, L. J., Li, L., Liu, L., Ma, H., Xun, Y., Lv, Z., et al. (2021) · The Journal of Neuroscience · doi:10.1523/jneurosci.2864-20.2021 · Cited by 45 · see citing works
Self-citationLudmer, J. A., González, A., Kennedy, J. L., Masellis, M., Meinz, P., & Atkinson, L. R. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.04.006 · Cited by 45 · see citing works
Jiménez, A., Young, L. J., Río, R. T.-D., LaPrairie, J. L., & González‐Mariscal, G. (2015) · Brain Research · doi:10.1016/j.brainres.2015.10.043 · Cited by 41 · see citing works
Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles
Borie, A. M., Agezo, S., Lunsford, P., Boender, A. J., Guo, J.-D., Zhu, H., Berman, G. J., Young, L. J., & Liu, R. C. (2022) · Current Biology · doi:10.1016/j.cub.2022.01.014 · Cited by 39 · see citing works
Prounis, G. S., Thomas, K., & Ophir, A. G. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24450 · Cited by 36 · see citing works
Olazábal, D. E. (2014) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2014.10.002 · Cited by 35 · see citing works
Barrett, C. E., Modi, M. E., Zhang, B. C., Walum, H., Inoue, K., & Young, L. J. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.05.041 · Cited by 34 · see citing works
Self-citationInoue, K., Burkett, J. P., & Young, L. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.03.035 · Cited by 31 · see citing works
Oxytocin, vasopressin and social behavior in the age of genome editing: a comparative perspective
Boender, A. J., & Young, L. J. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104780 · Cited by 30 · see citing works
Oxytocin’s dynamic role across the lifespan
Audunsdottir, K., & Quintana, D. S. (2022) · Aging Brain · doi:10.1016/j.nbas.2021.100028 · Cited by 28 · see citing works
BAXTER, A. B., Anderson, M., Seelke, A. M. H., Kinnally, E. L., Freeman, S. M., & Bales, K. L. (2020) · Scientific Reports · doi:10.1038/s41598-020-74243-1 · Cited by 26 · see citing works
Edwards, P. D., Coral, F.-L., Palme, R., & Boonstra, R. (2021) · Journal of Animal Ecology · doi:10.1111/1365-2656.13430 · Cited by 27 · see citing works
Bosch, O. J., Pohl, T. T., Neumann, I. D., & Young, L. J. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.12.034 · Cited by 26 · see citing works
Penalva-Tena, A., Bedke, J., Gaudin, A., Barrios, J. P., Bertram, E. P. L., & Douglass, A. D. (2018) · doi:10.1101/444026 · Cited by 41 · see citing works
Greenberg, G. D., van Westerhuyzen, J. A., Bales, K. L., & Trainor, B. C. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.063 · Cited by 24 · see citing works
Oxytocin signaling is necessary for synaptic maturation of adult-born neuronsPreprint
Pekarek, B. T., Kochukov, M. Y., Lozzi, B., Wu, T., Hunt, P. J., Tepe, B., Moss, E. H., Tantry, E. K., Swanson, J., Dooling, S. W., et al. (2022) · Genes & Development · doi:10.1101/gad.349930.122 · Cited by 24 · see citing works
González‐Mariscal, G., Caba, M., Hoffman, K. L., & Melo, Á. I. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00003-1 · Cited by 23 · see citing works
Penalva-Tena, A., Bedke, J., Gaudin, A., Barrios, J. P., Bertram, E. P., & Douglass, A. D. (2024) · Current Biology · doi:10.1016/j.cub.2024.11.037 · Cited by 19 · see citing works
Lecompte, V., Robins, S., King, L., Solomonova, E., Khan, N., Moss, E., Nagy, C., Feeley, N., Gold, I., Hayton, B. C., et al. (2020) · Attachment & Human Development · doi:10.1080/14616734.2019.1708422 · Cited by 20 · see citing works
The neurobiology of parenting and infant-evoked aggression
Kaplan, H. S., Horvath, P. M., Rahman, M. M., & Dulac, C. G. (2024) · Physiological Reviews · doi:10.1152/physrev.00036.2023 · Cited by 20 · see citing works
Hiura, L. C., & Ophir, A. G. (2018) · Integrative Zoology · doi:10.1111/1749-4877.12338 · Cited by 18 · see citing works
Harder, H. J., Searles, C. T., Vogt, M. E., & Murphy, A. Z. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105384 · Cited by 16 · see citing works
Oxytocin receptors in the nucleus accumbens shell are necessary for the onset of maternal behavior
Witchey, S. K., Haupt, A., & Caldwell, H. K. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1356448 · Cited by 16 · see citing works
Fu, Y., & Depue, R. A. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.026 · Cited by 16 · see citing works
Morales, L. K. N., Boender, A. J., Young, L. J., Lamprea, M. R., & Smith, A. S. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1409316 · Cited by 13 · see citing works
Taylor, J. H., Intorre, A. A., & French, J. A. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00181 · Cited by 15 · see citing works
Sex differences of oxytocin and vasopressin in social behaviors
Lu, Q., & Hu, S. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-820107-7.00005-7 · Cited by 17 · see citing works
On the origins of diversity in social behavior
YOUNG, L. J., & ZHANG, Q. (2021) · Japanese Journal of Animal Psychology · doi:10.2502/janip.71.1.4 · Cited by 13 · see citing works
Borland, J. M. (2025) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2025.101175 · Cited by 12 · see citing works
Mate Selection, Sexual Orientation, and Pair Bonding
Balthazart, J., & Young, L. J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00048-x · Cited by 12 · see citing works
The Role of Early Life Experience and Species Differences in Alcohol Intake in Microtine Rodents
Anacker, A. M. J., Ahern, T. H., Young, L. J., & Ryabinin, A. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039753 · Cited by 12 · see citing works
Keebaugh, A. C., Modi, M. E., Barrett, C., Jin, C., & Young, L. J. (2012) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-10-54 · Cited by 12 · see citing works
Quintana, D. S. (2018) · OSF Preprints (OSF Preprints) · Cited by 12 · see citing works
The neural circuits of monogamous behavior
López-Gutiérrez, M. F., Mejía-Chávez, S., Alcauter, S., & Portillo, W. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.978344 · Cited by 11 · see citing works
The Neurobiology and Genetics of Affiliation and Social Bonding in Animal Models
Donaldson, Z. R., & Young, L. J. (2016) · Springer eBooks · doi:10.1007/978-1-4939-3777-6_4 · Cited by 11 · see citing works
Paiva, L., Sabatier, N., Leng, G., & Ludwig, M. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12454 · Cited by 11 · see citing works
Quintana, D. S., Rokicki, J., van der Meer, D., Alnæs, D., Kaufmann, T., Córdova‐Palomera, A., Dieset, I., Andreassen, O. A., & Westlye, L. T. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/149526 · Cited by 12 · see citing works
Taylor, J. H., & Grieb, Z. A. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.100996 · Cited by 10 · see citing works
Neuropeptide Regulation of Social Attachment: The Prairie Vole Model
Tabbaa, M., Paedae, B., Liu, Y., & Wang, Z. (2017) · Comprehensive physiology · doi:10.1002/j.2040-4603.2017.tb00738.x · Cited by 9 · see citing works
Association between parental behaviors and structural plasticity in the brain of male rodents
Inada, K., & Miyamichi, K. (2023) · Neuroscience Research · doi:10.1016/j.neures.2023.06.007 · Cited by 9 · see citing works
Rethinking the Architecture of Attachment: New Insights into the Role for Oxytocin Signaling
Berendzen, K. M., & Manoli, D. S. (2022) · Affective Science · doi:10.1007/s42761-022-00142-5 · Cited by 9 · see citing works
Tsukamoto, M., Nagai, L. A., Inoue, K., Kandasamy, L. C., Pires, M. F., Shin, M., Nagasawa, Y., Sambuu, T., Nakai, K., Itohara, S., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.01.518660 · Cited by 8 · see citing works
Loth, M. K., Schmidt, J. C., Gonzalez, C. A., Brusman, L. E., Sadino, J. M., Winther, K. E., Protter, D. S. W., & Donaldson, Z. R. (2025) · Scientific Reports · doi:10.1038/s41598-025-06367-1 · Cited by 7 · see citing works
Wu, R., Song, Z., & Tai, F. (2018) · Journal of Comparative Physiology A · doi:10.1007/s00359-018-1262-4 · Cited by 6 · see citing works
Fricker, B. A., Boender, A. J., Young, L. J., & Kelly, A. M. (2025) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2025.107496 · Cited by 5 · see citing works
Perkeybile, A. M., Kenkel, W. M., Yee, J. R., Waugh, R. E., Lillard, T. S., Ferris, C. F., Carter, C. S., & Connelly, J. J. (2025) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-025-07868-7 · Cited by 4 · see citing works
- Authors
- Keebaugh, A. C., & Young, L. J.
- Affiliations
- Emory University (US)
- Corresponding author
- Keebaugh, Alaine C.
- ORCID
- Young, Larry J.
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 2011-11
- Volume
- 60
- Issue
- 5
- Pages
- 498-504
- ISSN
- 0018-506X (ISSN-L)
- PMC
- PMC3210320
- OpenAlex
- W1969779840
- Cited by
- 154
- References
- 48
- Citations by year
- 2026: 3 · 2025: 12 · 2024: 9 · 2023: 11 · 2022: 10 · 2021: 10 · 2020: 23 · 2019: 7 · 2018: 17 · 2017: 7 · 2016: 10 · 2015: 12 · 2014: 6 · 2013: 11 · 2012: 5
- FWCI
- 10.01
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Hormones and Behavior (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (MH064692, RR00165)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
- Keywords
- oxytocin receptor, nucleus accumbens, Microtus ochrogaster, mate preferences, prepubertal development, oxytocin, organizational effects, activational effects, affiliative behavior, female social behavior, gene overexpression
- MeSH terms
- Animals, Arvicolinae, Female, Nucleus Accumbens, Pair Bond, Receptors, Oxytocin
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
