The comparative distribution of forebrain receptors for neurohypophyseal peptides in monogamous and polygamous mice
Abstract
Several recent studies have suggested that the neurohypophyseal peptide oxytocin may have a role within the brain to mediate various forms of affiliative behavior. As the regulation of oxytocin function may be largely determined by the number and distribution of its membrane bound receptor, we investigated oxytocin receptor distribution in two Peromyscus species selected for differences in affiliative behavior. Using in vitro receptor autoradiography with the selective oxytocin receptor ligand [125I]d(CH2)5[Tyr(Me)2,Tyr-NH9(2)]OVT ([125I]OTA), we compared Peromyscus maniculatus, a polygamous species, to Peromyscus californicus, a monogamous species. Marked species differences in the distribution of [125I]OTA were apparent in several brain areas, including olfactory pathways, bed nucleus of the stria terminalis, amygdala, dorsal lateral septum, and several cortical regions. In addition, gender differences in the binding pattern were evident in several regions, mostly due to sexually dimorphic patterns in the polygamous species, P. maniculatus. To further compare these species, the binding of a [3H]arginine-vasopressin antagonist was assessed in alternate sections from those used for [125I]OTA. Relative to oxytocin receptors, binding to arginine-vasopressin receptors showed fewer species differences, although the monogamous species appeared to have more arginine-vasopressin receptors in the neocortex and lateral septum. The striking differences in oxytocin receptor distribution are consistent with earlier studies in other rodents, suggesting that oxytocin may have an important role for mediating species-typical patterns of social affiliation.
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In Peromyscus maniculatus and P. californicus mice, no sex differences were found for VP receptor binding in any brain region analyzed, except higher binding in the centromedial thalamic nucleus in females.
“In Peromyscus (P.) maniculatus and P. californicus mice, no sex differences were found for VP receptor binding in any of the brain regions analyzed, except for higher binding in the centromedial thalamic nucleus in females”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Insel et al., 1991
The sex-specific effects of the VP system appear independent of whether sex differences in VP and/or V1aR binding are present.
“Interestingly, these sex-specific effects seem to be independent of whether sex differences are found in VP and/or V1aR binding (rats; Figs. 1 and 2) or whether no sex differences are found in VP and/or V1aR binding (prairie voles: Insel et al., 1991; Smeltzer et al., 2006; humans: Loup et al., 1991).”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Insel et al., 1991
Sex differences in OTR binding were found in multiple brain regions in rodent studies that used a more comprehensive analysis (deer mice: 8 out of 20 brain regions; rats: 9 out of 15 forebrain regions).
“Similar to V1aR, sex differences in OTR binding were found in multiple brain regions in those rodent studies that used a more comprehensive analysis (deer mice: 8 out of 20 brain regions; Insel et al., 1991; rats: 9 out of 15 forebrain regions; Dumais et al., 2013).”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as Insel et al., 1991
There were no sex differences in OTR expression.
“There were no sex differences in OTR expression, consistent with previous reports in other species (53, 54).”
From Oxytocin receptors in the anteromedial bed nucleus of the stria terminalis promote stress-induced social avoidance in female California mice (2018) · cites this paper as [54]
Cites
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 induces maternal behavior in virgin female rats
Pedersen, C. A., Ascher, J. A., Monroe, Y. L., & Prange, A. J. (1982) · Science · doi:10.1126/science.7071605 · Cited by 770 · see citing works
Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size.
Jacobs, L. F., Gaulin, S. J. C., Sherry, D. F., & Hoffman, G. E. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.16.6349 · Cited by 366 · see citing works
Possible Role for Endogenous Oxytocin in Estrogen-Facilitated Maternal Behavior in Rats
Fahrbach, S. E., Morrell, J. I., & Pfaff, D. W. (2008) · Neuroendocrinology · doi:10.1159/000124125 · Cited by 322 · see citing works
The biparental care system of the California mouse, Peromyscus californicus.
Gubernick, D. J., & Alberts, J. R. (1987) · Journal of comparative psychology · doi:10.1037/0735-7036.101.2.169 · Cited by 274 · see citing works
Oxytocin facilitates the sexual receptivity of estrogen-treated female rats
Caldwell, J. D., Prange, A. J., & Pedersen, C. A. (1986) · Neuropeptides · doi:10.1016/0143-4179(86)90093-4 · Cited by 229 · see citing works
Sex Differences in Neurotransmitter Systems
Vries, G. J. D. (1990) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1990.tb00385.x · Cited by 226 · see citing works
Gonadal hormone actions on the morphology of the vasopressinergic innervation of the adult rat brain
De Vries, G. J., Buijs, R. M., & Sluiter, A. A. (1984) · Brain Research · doi:10.1016/0006-8993(84)91157-0 · Cited by 224 · see citing works
Tribollet, E., Audigier, S., Dubois-Dauphin, M., & Dreifuss, J. J. (1990) · Brain Research · doi:10.1016/0006-8993(90)90232-z · Cited by 203 · see citing works
Birdsall, D. A., & Nash, D. (1973) · Evolution · doi:10.1111/j.1558-5646.1973.tb05922.x · Cited by 175 · see citing works
Insel, T. R. (1990) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1990.tb00445.x · Cited by 164 · see citing works
Self-citationOxytocin improves male copulatory performance in rats
Arletti, R., Bazzani, C., Castelli, M., & Bertolini, A. (1985) · Hormones and Behavior · doi:10.1016/0018-506x(85)90002-9 · Cited by 155 · see citing works
A Selective Oxytocin Antagonist Attenuates Progesterone Facilitation of Female Sexual Behavior
Witt, D. M., & Insel, T. R. (1991) · Endocrinology · doi:10.1210/endo-128-6-3269 · Cited by 138 · see citing works
Self-citationOxytocin antiserum delays onset of ovarian steroid-induced maternal behavior
Pedersen, C. A., Caldwell, J. D., Johnson, M. F., Fort, S. A., & Prange, A. J. (1985) · Neuropeptides · doi:10.1016/0143-4179(85)90108-8 · Cited by 137 · see citing works
Localized actions of progesterone in hypothalamus involve oxytocin.
Schumacher, M., Coirini, H., Frankfurt, M., & McEwen, B. S. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.17.6798 · Cited by 130 · see citing works
Comparative neuroanatomy of the sexually dimorphic hypothalamus in monogamous and polygamous voles
Shapiro, L. E., Leonard, C. M., Sessions, C. E., Dewsbury, D. A., & Insel, T. R. (1991) · Brain Research · doi:10.1016/0006-8993(91)91023-t · Cited by 123 · see citing works
Self-citationPostpartum Increases in Brain Oxytocin Binding
Insel, T. R. (2008) · Neuroendocrinology · doi:10.1159/000124694 · Cited by 116 · see citing works
Self-citationEstradiol induces oxytocin binding sites in rat hypothalamic ventromedial nucleus
de Kloet, E. R., Voorhuis, T. A. M., & Elands, J. (1985) · European Journal of Pharmacology · doi:10.1016/0014-2999(85)90679-x · Cited by 116 · see citing works
Oxytocin-induced facilitation of lordosis behaviour in rats is progesterone-dependent
Gorzalka, B. B. (1987) · Neuropeptides · doi:10.1016/0143-4179(87)90089-8 · Cited by 97 · see citing works
Regulation of neuronal oxytocin mRNA by ovarian steroids in the mature and developing hypothalamus.
Miller, F. D., Ozimek, G., Milner, R. J., & Bloom, F. E. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.7.2468 · Cited by 95 · see citing works
HORMONAL CONTROL OF OVIPOSITION AND PARTURITION IN LIZARDS
Jones, R. E. (1982) · Cited by 93 · see citing works
Oxytocin Receptor Binding in Female Prairie Voles: Endogenous and Exogenous Oestradiol Stimulation
Witt, D. M., Carter, C. S., & Lnsel, T. R. (1991) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1991.tb00258.x · Cited by 91 · see citing works
Johnson, A. E., Ball, G. F., Coirini, H., Harbaugh, C. R., McEwen, B. S., & Insel, T. R. (1989) · Endocrinology · doi:10.1210/endo-125-3-1414 · Cited by 87 · see citing works
Self-citationBirdsall, D. A., & Nash, D. (1973) · Evolution · doi:10.2307/2407124 · Cited by 77 · see citing works
Neurohypophyseal hormones and excessive grooming behaviour
Greidanus, T. B. V. W., Kroodsma, J.-M., Pot, M., Stevens, M., & Maigret, C. (1990) · European Journal of Pharmacology · doi:10.1016/0014-2999(90)90334-3 · Cited by 69 · see citing works
Raggenbass, M., Tribollet, E., Dubois‐Dauphin, M., & Dreifuss, J. J. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.2.750 · Cited by 59 · see citing works
Testosterone Modulates Oxytocin Binding in the Hypothalamus of Castrated Male Rats
Johnson, A. E., Coirini, H., McEwen, B. S., & Insel, T. R. (2008) · Neuroendocrinology · doi:10.1159/000125222 · Cited by 40 · see citing works
Self-citationOxytocinergic innervation of the brain of the garden dormouse (Eliomys quercinus L.)
Hermes, M. L. H. J., Buijs, R. M., Masson‐Pévet, M., & Pévet, P. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902730209 · Cited by 32 · see citing works
Papadopoulos, G. C., Karamanlidis, A. N., Michaloudi, H. C., Dinopoulos, A., Antonopoulos, J., & Parnavelas, J. G. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90357-x · Cited by 17 · see citing works
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Cited by
Sorted by citations
Insel, T. R. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.005 · Cited by 1,044 · see citing works
Self-citationOxytocin: The Great Facilitator of Life
Lee, H.-J., Macbeth, A. H., Pagani, J., & Young, W. S. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.04.001 · Cited by 1,037 · see citing works
The oxytocin receptor: from intracellular signaling to behavior
Jurek, B., & Neumann, I. D. (2018) · Physiological Reviews · doi:10.1152/physrev.00031.2017 · Cited by 999 · 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
Self-citationPlasma oxytocin levels in autistic children
Modahl, C., Green, L. A., Fein, D., Morris, M., Waterhouse, L., Feinstein, C., & Levin, H. (1998) · Biological Psychiatry · doi:10.1016/s0006-3223(97)00439-3 · Cited by 728 · see citing works
Goodson, J. L., & Bass, A. H. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00043-1 · Cited by 632 · 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
Dumais, K. M., & Veenema, A. H. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.04.003 · Cited by 520 · see citing works
“Similar to V1aR, sex differences in OTR binding were found in multiple brain regions in those rodent studies that used a more comprehensive analysis (deer mice: 8 out of 20 brain regions; Insel et al., 1991; rats: 9 out of 15 forebrain regions; Dumais et al., 2013).”
BackgroundInfluentialWilliams, 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
Self-citationInsel, T. R. (1992) · Psychoneuroendocrinology · doi:10.1016/0306-4530(92)90073-g · Cited by 487 · see citing works
Self-citationOxytocin Makes a Face in Memory Familiar
Rimmele, U., Hediger, K., Heinrichs, M., & Klaver, P. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4260-08.2009 · Cited by 402 · see citing works
Oxytocin, motherhood and bonding
Kendrick, K. M. (2000) · Experimental Physiology · doi:10.1111/j.1469-445x.2000.tb00014.x · Cited by 378 · see citing works
A psychobiological theory of attachment
Kraemer, G. W. (1992) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00069752 · Cited by 359 · 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
Bester‐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
A conditional knockout mouse line of the oxytocin receptor
Lee, H.-J., Caldwell, H. K., Macbeth, A. H., Tolu, S. G., & Young, W. S. (2008) · Endocrinology · doi:10.1210/en.2007-1710 · Cited by 269 · see citing works
The 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
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
Sex differences in the parental behavior of rodents
Lonstein, J. S., & De Vries, G. J. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00036-1 · Cited by 226 · see citing works
Life in groups: the roles of oxytocin in mammalian sociality
Anacker, A. M. J., & Beery, A. K. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00185 · Cited by 216 · see citing works
Neuroendocrinology of social information processing in rats and mice
Choleris, E., Clipperton-Allen, A. E., Phan, A., & Kavaliers, M. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.003 · Cited by 205 · see citing works
Goodson, J. L., & Kabelik, D. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.007 · Cited by 204 · 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
Pagani, J. H., Zhao, M., Cui, Z., Williams Avram, S. K., Caruana, D. A., Dudek, S. M., & Young, W. S. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.47 · Cited by 204 · see citing works
Albers, H. E. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.07.001 · Cited by 200 · see citing works
Oxytocin-Induced Analgesia and Scratching Are Mediated by the Vasopressin-1A Receptor in the Mouse
Schorscher-Petcu, A., Sotocinal, S., Ciura, S., Dupre, A., Ritchie, J., Sorge, R. E., Crawley, J. N., Hu, S.-B., Nishimori, K., Young, L. J., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1594-10.2010 · Cited by 189 · see citing works
Lukas, M., Bredewold, R., Neumann, I. D., & Veenema, A. H. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.06.020 · Cited by 183 · see citing works
Duque-Wilckens, N., Steinman, M. Q., Busnelli, M., Chini, B., Yokoyama, S., Pham, M., Laredo, S. A., Hao, R., Perkeybile, A. M., Minie, V. A., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.08.024 · Cited by 181 · see citing works
Neuroendocrine basis of social recognition
Winslow, J. T., & Insel, T. R. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.009 · Cited by 180 · see citing works
Self-citationGoodson, & Adkins‐Regan (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00284.x · Cited by 171 · see citing works
Localization of oxytocin receptor messenger ribonucleic acid in the rat brain.
Yoshimura, R., Kiyama, H., Kimura, T., Araki, T., Maeno, H., Tanizawa, O., & Tohyama, M. (1993) · Endocrinology · doi:10.1210/endo.133.3.8396014 · Cited by 161 · see citing works
2006 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
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
Hormones Associated with Non-Maternal Infant Care: A Review of Mammalian and Avian Studies
Ziegler, T. E. (2000) · Folia Primatologica · doi:10.1159/000021726 · Cited by 142 · see citing works
The social brain: Neurobiological basis of affiliative behaviours and psychological well-being
Walker, S. C., & McGlone, F. P. (2013) · Neuropeptides · doi:10.1016/j.npep.2013.10.008 · Cited by 138 · see citing works
Vasopressin 1a receptor knockout mice have a subtle olfactory deficit but normal aggression
Wersinger, S. R., Caldwell, H. K., Martinez, L. A., Gold, P. W., Hu, S.-B., & Young, W. S. (2006) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2006.00281.x · Cited by 139 · see citing works
Vasopressin and oxytocin receptors
Zingg, H. H. (1996) · Baillière s Clinical Endocrinology and Metabolism · doi:10.1016/s0950-351x(96)80314-4 · Cited by 137 · see citing works
The role of central oxytocin in obsessive compulsive disorder and related normal behavior
Leckman, J. F., Goodman, W. K., North, W. G., Chappell, P. B., Price, L. H., Pauls, D. L., Anderson, G. M., Riddle, M. A., McDougle, C. J., Barr, L. C., et al. (1994) · Psychoneuroendocrinology · doi:10.1016/0306-4530(94)90021-3 · 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
Central vasopressin and oxytocin receptor distributions in two species of singing mice
Polly Campbell, A., Ophir, A. G., & Phelps, S. M. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22116 · Cited by 128 · see citing works
The Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00004-8 · Cited by 128 · see citing works
Oxytocin-messages via the cerebrospinal fluid: Behavioral effects; a review
Veening, J. G., A, T. R. D. J., & Barendregt, H. P. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.05.004 · 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
Gonadal steroids have paradoxical effects on brain oxytocin receptors
Insel, T. R., Young, L., Witt, D. M., & Crews, D. (1993) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1993.tb00531.x · Cited by 113 · see citing works
Self-citationSex-dependent regulation of social reward by oxytocin: an inverted U hypothesis
Borland, J. M., Rilling, J. K., Frantz, K. J., & Albers, H. E. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-018-0129-2 · Cited by 116 · see citing works
González‐Mariscal, G., & Poindron, P. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50005-6 · Cited by 115 · see citing works
Functional Significance of Hormonal Changes in Mammalian Fathers
Saltzman, W., & Ziegler, T. E. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12176 · Cited by 114 · see citing works
Schorscher-Petcu, A., Dupré, A., & Tribollet, E. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.06.016 · Cited by 111 · see citing works
The Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50006-8 · Cited by 109 · 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
Social structure influences effects of pair-housing on wound healing
Glasper, E. R., & DeVries, A. C. (2004) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2004.03.002 · Cited by 109 · see citing works
Oxytocin as a natural antipsychotic: a study using oxytocin knockout mice
Caldwell, H. K., Stephens, S. L., & Young, W. S. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002150 · Cited by 108 · see citing works
Brown, R. E. (1993) · Behavioural Processes · doi:10.1016/0376-6357(93)90009-g · Cited by 102 · see citing works
Lin, Y.-T., & Hsu, K. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.10.003 · Cited by 97 · see citing works
Kalamatianos, T., Faulkes, C. G., Oosthuizen, M. K., Poorun, R., Bennett, N. C., & Coen, C. W. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22302 · Cited by 92 · see citing works
Oxytocin and Stress: Neural Mechanisms, Stress-Related Disorders, and Therapeutic Approaches
Matsushita, H., Latt, H. M., Koga, Y., Nishiki, T., & Matsui, H. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.07.046 · Cited by 92 · see citing works
Oxytocin and vasopressin in the rodent hippocampus
Cilz, N. I., Cymerblit‐Sabba, A., & Young, W. S. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12535 · Cited by 88 · see citing works
Lin, Y.-T., Huang, C., & Hsu, K. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2429-12.2012 · Cited by 87 · see citing works
Charvet, C. J., Striedter, G. F., & Finlay, B. L. (2011) · Brain Behavior and Evolution · doi:10.1159/000329851 · Cited by 87 · see citing works
Yu, G.-Z., Kaba, H., Okutani, F., Takahashi, S., Higuchi, T., & Seto, K. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00599-4 · Cited by 83 · see citing works
Oxytocin receptor dynamics in the brain across development and species
Vaidyanathan, R., & Hammock, E. A. D. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22403 · Cited by 82 · see citing works
The 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 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
Self-citationGoodson, J. L., EIBACH, R., Sakata, J. T., & Adkins–Regan, E. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00066-7 · Cited by 77 · 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
Antisocial oxytocin: Complex effects on social behavior
Beery, A. K. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.11.006 · Cited by 74 · 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
Rubin, L. H., Connelly, J. J., Reilly, J. L., Carter, C. S., Drogos, L. L., Pournajafi‐Nazarloo, H., Ruocco, A. C., Keedy, S., Matthew, I., Tandon, N., et al. (2015) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2015.10.003 · Cited by 72 · see citing works
Estrogen receptor‐α distribution in male rodents is associated with social organization
Cushing, B. S., & Wynne‐Edwards, K. E. (2006) · Journal of Comparative Neurology · doi:10.1002/cne.20826 · Cited by 101 · see citing works
Oxytocin: Parallel Processing in the Social Brain?
Dölen, G. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12284 · Cited by 65 · see citing works
Oxytocin and sex differences in behavior
Caldwell, H. K. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.02.002 · Cited by 64 · see citing works
Caldwell, H. K. (2012) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4614-1704-0_12 · Cited by 58 · see citing works
Sexually dimorphic oxytocin receptor-expressing neurons in the preoptic area of the mouse brain
Sharma, K., LeBlanc, R. M., Haque, M., Nishimori, K., Reid, M. M., & Teruyama, R. (2019) · PLoS ONE · doi:10.1371/journal.pone.0219784 · Cited by 63 · see citing works
Ophir, A. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00397 · Cited by 62 · see citing works
Harony-Nicolas, H., Mamrut, S., Brodsky, L., Shahar-Gold, H., Barki-Harrington, L., & Wagner, S. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.10.004 · Cited by 61 · see citing works
Clipperton‐Allen, A. E., Lee, A. W., Reyes, A., Devidze, N., Phan, A., Pfaff, D. W., & Choleris, E. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.10.025 · Cited by 58 · see citing works
Tribollet, E., Barberis, C., Dubois‐Dauphin, M., & Dreifuss, J. J. (1992) · Brain Research · doi:10.1016/0006-8993(92)91156-9 · Cited by 58 · see citing works
Dubois-Dauphin, M., Barberis, C., & de Bilbao, F. (1996) · Brain Research · doi:10.1016/s0006-8993(96)01019-0 · Cited by 57 · see citing works
Smith, C. J. W., DiBenedictis, B. T., & Veenema, A. H. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.02.001 · Cited by 59 · see citing works
Nonapeptides and the Evolution of Social Group Sizes in Birds
Goodson, J. L., & Kingsbury, M. A. (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00013 · Cited by 59 · see citing works
Bester‐Meredith, J. K., MARTIN, P. A., & Marler, C. A. (2005) · Aggressive Behavior · doi:10.1002/ab.20075 · Cited by 57 · see citing works
INSEL, T. R., YOUNG, L., & WANG, Z. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51928.x · Cited by 56 · see citing works
Self-citationSex Differences in the Embryonic Development of the Central Oxytocin System in Mice
Tamborski, S., Mintz, E. M., & Caldwell, H. K. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12364 · Cited by 55 · see citing works
Beyond “oxytocin = good”: neural complexities and the flipside of social bonds
van Anders, S. M., Goodson, J. L., & Kingsbury, M. A. (2013) · Archives of Sexual Behavior · doi:10.1007/s10508-013-0134-9 · Cited by 52 · see citing works
Autism: Oxytocin, serotonin, and social reward
Dölen, G. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1087875 · Cited by 51 · see citing works
Behavioural studies using temporal and spatial inactivation of the oxytocin receptor
LEE, H., CALDWELL, H., MACBETH, A., & YOUNGIII, W. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00407-x · Cited by 49 · see citing works
Zheng, D., Larsson, B., Phelps, S. M., & Ophir, A. G. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.02.024 · Cited by 48 · see citing works
Insel, T. R., Winslow, J. T., WILLIAMS, J. R., Hastings, N., Shapiro, L. E., & Carter, C. S. (1993) · Regulatory Peptides · doi:10.1016/0167-0115(93)90194-d · Cited by 44 · see citing works
Self-citationDewan, A., Ramey, M. L., & Tricas, T. C. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.10.002 · Cited by 44 · see citing works
Olazábal, D. E., & Sandberg, N. Y. (2019) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2019.113337 · Cited by 41 · see citing works
Lakhdar‐Ghazal, N., Dubois‐Dauphin, M., Hermes, M. L. H. J., Buijs, R. M., Bengelloun, W. A., & Pévet, P. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903580404 · Cited by 41 · see citing works
The impact of sex as a biological variable in the search for novel antidepressants
Williams, A. V., & Trainor, B. C. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.05.003 · Cited by 40 · see citing works
Evolution and Genetics of Precocious Burrowing Behavior in Peromyscus Mice
Metz, H. C., Bedford, N. L., Pan, Y. L., & Hoekstra, H. E. (2017) · Current Biology · doi:10.1016/j.cub.2017.10.061 · Cited by 39 · see citing works
The Role of Intranasal Oxytocin in the Treatment of Patients with Schizophrenia: A Systematic Review
Berardis, D. D., Marini, S., Iasevoli, F., Tomasetti, C., de Bartolomeis, A., Mazza, M., Valchera, A., Fornaro, M., Cavuto, M., Srinivasan, V., et al. (2013) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527311312020012 · Cited by 38 · see citing works
Kolodziejski, J. A., Nelson, B. S., & Smith, G. T. (2004) · Journal of Neurobiology · doi:10.1002/neu.20095 · Cited by 38 · see citing works
Chapter 1.4 Vasopressin binding sites in the central nervous system: Distribution and regulation
Tribollet, E., Arsenijévic, Y., & Barberis, C. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)61561-7 · Cited by 37 · see citing works
Althammer, F., Jirikowski, G. F., & Grinevich, V. (2018) · Peptides · doi:10.1016/j.peptides.2018.09.003 · Cited by 35 · see citing works
Oxytocin mechanisms of stress response and aggression in a territorial finch
Goodson, J. L., Schrock, S. E., & Kingsbury, M. A. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.01.016 · Cited by 34 · see citing works
Nair, H. P., Gutman, A. R., Davis, M., & Young, L. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2524-05.2005 · Cited by 36 · see citing works
Smith, A. L., Freeman, S. M., Stehouwer, J. S., Inoue, K., Voll, R. J., Young, L. J., & Goodman, M. M. (2012) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2012.02.019 · Cited by 35 · see citing works
- Authors
- Insel, T. R., Gelhard, R., & Shapiro, L. E.
- Affiliations
- National Institute of Mental Health (US)
- Corresponding author
- Insel, T.R.
- ORCID
- Insel, T.R.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 1991-01
- Volume
- 43
- Issue
- 2-3
- Pages
- 623-630
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W1992791641
- Cited by
- 209
- References
- 28
- Citations by year
- 2026: 6 · 2025: 3 · 2024: 10 · 2023: 6 · 2022: 7 · 2021: 4 · 2020: 5 · 2019: 9 · 2018: 11 · 2017: 7 · 2016: 6 · 2015: 11 · 2014: 7 · 2013: 14 · 2012: 5
- FWCI
- 20.03
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- oxytocin receptor, arginine vasopressin receptor, neurohypophyseal peptides, monogamy, polygamy, deer mouse, Peromyscus californicus, affiliative behavior, social behavior, sexual dimorphism, species differences, bed nucleus of the stria terminalis, amygdala, lateral septum, olfactory pathway, neocortex, receptor autoradiography
- MeSH terms
- Animals, Autoradiography, Oxytocin, Peromyscus, Receptors, Angiotensin, Sexual Behavior, Animal, Sex Characteristics, Tissue Distribution, Vasopressins, Prosencephalon, Receptors, Oxytocin, Mice
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