A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits
Open accessAbstract
We tested the hypothesis that genes encoded on the sex chromosomes play a direct role in sexual differentiation of brain and behavior. We used mice in which the testis-determining gene (Sry) was moved from the Y chromosome to an autosome (by deletion of Sry from the Y and subsequent insertion of an Sry transgene onto an autosome), so that the determination of testis development occurred independently of the complement of X or Y chromosomes. We compared XX and XY mice with ovaries (females) and XX and XY mice with testes (males). These comparisons allowed us to assess the effect of sex chromosome complement (XX vs XY) independent of gonadal status (testes vs ovaries) on sexually dimorphic neural and behavioral phenotypes. The phenotypes included measures of male copulatory behavior, social exploration behavior, and sexually dimorphic neuroanatomical structures in the septum, hypothalamus, and lumbar spinal cord. Most of the sexually dimorphic phenotypes correlated with the presence of ovaries or testes and therefore reflect the hormonal output of the gonads. We found, however, that both male and female mice with XY sex chromosomes were more masculine than XX mice in the density of vasopressin-immunoreactive fibers in the lateral septum. Moreover, two male groups differing only in the form of their Sry gene showed differences in behavior. The results show that sex chromosome genes contribute directly to the development of a sex difference in the brain.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The male Y chromosome contributes to the masculinized expression of AVP-ir fibers in the LS.
“Furthermore, in addition to the activational and organizational effects of gonadal steroid hormones, the male Y chromosome also contributes to the masculinized expression of AVP-ir fibers in the LS (De Vries et al., 2002).”
From Quantitative mapping reveals age and sex differences in vasopressin, but not oxytocin, immunoreactivity in the rat social behavior neural network (2017) · cites this paper as De Vries et al., 2002
The FCG mouse model allows for an independent assessment of gonadal hormones and sex chromosomal effects.
“we used the Four Core Genotypes (FCG) mouse model, which allows for an independent assessment of gonadal hormones and sex chromosomal effects [47–49].”
From Sex chromosomes and sex hormones differently shape microglial properties during normal physiological conditions in the adult mouse hippocampus (2025) · cites this paper as [49]
Various rodent species show consistent sex differences in VP-immunoreactive neurons and fiber density in the brain.
“various rodent species show consistent sex differences in VP-immunoreactive neurons and fiber density in the brain”
From Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior (2016) · cites this paper as De Vries et al., 2002
The sex difference in vasopressin expression is driven primarily by organizational effects of steroid hormones, although hormone-independent influences of sex chromosomes play a role.
“The sex difference in AVP expression is driven primarily by organizational effects of steroid hormones, although hormone-independent influences of sex chromosomes play a role (67).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [67]
The Four Core Genotypes mouse model uncouples chromosomal effects (X and Y) from gonadal influences (ovaries and testes), allowing each to be studied separately by generating four genotypes.
“The Four Core Genotypes mouse model uncouples chromosomal effects (X and Y) from gonadal influences (ovaries and testes), allowing each to be studied separately by generating four genotypes: XX mice with ovaries, XX mice with testes, XY mice with ovaries, and XY mice with testes. 91”
From Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know (2019) · cites this paper as [91]
Cites
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
Estimation of nuclear population from microtome sections
Abercrombie, M. (1946) · The Anatomical Record · doi:10.1002/ar.1090940210 · Cited by 4,363 · 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
Gonadal Steroid Induction of Structural Sex Differences in the Central Nervous System
Arnold, A. P., & Gorski, R. A. (1984) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.07.030184.002213 · Cited by 1,198 · see citing works
Self-citationA role for central vasopressin in pair bonding in monogamous prairie voles
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. (1993) · Nature · doi:10.1038/365545a0 · Cited by 948 · cited 1× · see citing works
“These differences in VP-ir fiber density and aggressive behavior may also be causally related because VP has been implicated in aggressive behavior in rats and voles (Koolhaas et al., 1990, 1991; Winslow et al., 1993).”
BackgroundSexual differentiation of the brain
McEwen, B. S. (1981) · Nature · doi:10.1038/291610a0 · Cited by 902 · see citing works
Ericson, J., Brenner‐Morton, S., Kawakami, A., Roelink, H., & Jessell, T. M. (1996) · Cell · doi:10.1016/s0092-8674(00)81386-0 · Cited by 870 · see citing works
Evidence from Turner's syndrome of an imprinted X-linked locus affecting cognitive function
Skuse, D. H., James, R. S., Bishop, D. V. M., Coppin, B., Dalton, P., Aamodt-Leeper, G., Bacarese-Hamilton, M., Creswell, C., McGurk, R., & Jacobs, P. A. (1997) · Nature · doi:10.1038/42706 · Cited by 747 · see citing works
Genetic variation among 129 substrains and its importance for targeted mutagenesis in mice
Simpson, E. M., Linder, C. C., Sargent, E. E., Davisson, M. T., Mobraaten, L. E., & Sharp, J. J. (1997) · Nature Genetics · doi:10.1038/ng0597-19 · Cited by 686 · see citing works
Early Stages of Motor Neuron Differentiation Revealed by Expression of Homeobox Gene <i>Islet-1</i>
Ericson, J., Thor, S., Edlund, T., Jessell, T. M., & Yamada, T. (1992) · Science · doi:10.1126/science.1350865 · Cited by 620 · see citing works
Hormone Accumulation in a Sexually Dimorphic Motor Nucleus of the Rat Spinal Cord
Breedlove, S. M., & Arnold, A. P. (1980) · Science · doi:10.1126/science.7423210 · Cited by 594 · see citing works
Self-citationSRY AND SEX DETERMINATION IN MAMMALS
Goodfellow, P. N., & Lovell-Badge, R. H. (1993) · Annual Review of Genetics · doi:10.1146/annurev.ge.27.120193.000443 · Cited by 429 · see citing works
Self-citationA first-generation X-inactivation profile of the human X chromosome
Carrel, L., Cottle, A. A., Goglin, K. C., & Willard, H. F. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.25.14440 · Cited by 358 · see citing works
Hormone-neurotransmitter interactions in the control of sexual behavior
Hull, E. M., Lorrain, D. S., Du, J., Matuszewich, L., Lumley, L. A., Putnam, S. K., & Moses, J. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00086-8 · Cited by 329 · see citing works
Sawchenko, P. E., & Swanson, L. W. (1981) · Brain Research · doi:10.1016/0006-8993(81)90882-9 · Cited by 311 · see citing works
Lovell-Badge, R., & Robertson, E. (1990) · Development · doi:10.1242/dev.109.3.635 · Cited by 311 · see citing works
Self-citationSex chromosome genes directly affect brain sexual differentiation
Carruth, L. L., Reisert, I., & Arnold, A. P. (2002) · Nature Neuroscience · doi:10.1038/nn922 · Cited by 298 · see citing works
Self-citationZechner, U., Wilda, M., Kehrer‐Sawatzki, H., Vogel, W., Fundele, R., & Hameister, H. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(01)02446-5 · Cited by 272 · see citing works
Sex differences in sex chromosome gene expression in mouse brain
Xu, J. (2002) · Human Molecular Genetics · doi:10.1093/hmg/11.12.1409 · Cited by 269 · see citing works
Wersinger, S. R., Sannen, K., Villalba, C., Lubahn, D. B., Rissman, E. F., & Vries, G. J. D. (1997) · Hormones and Behavior · doi:10.1006/hbeh.1997.1419 · Cited by 240 · see citing works
Self-citationSimerly, R. B., Zee, M. C., Pendleton, J. W., Lubahn, D. B., & Korach, K. S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.25.14077 · Cited by 237 · see citing works
Self-citationVom Saal, F. S., & Bronson, F. H. (1978) · Biology of Reproduction · doi:10.1095/biolreprod19.4.842 · Cited by 236 · see citing works
Mahadevaiah, S. K. (1998) · Human Molecular Genetics · doi:10.1093/hmg/7.4.715 · Cited by 228 · see citing works
Anatomy, Development, and Function of Sexually Dimorphic Neural Circuits in the Mammalian Brain
Vries, G. J. D., & Simerly, R. B. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50066-4 · Cited by 218 · see citing works
Self-citationEdinburgh study of growth and development of children with sex chromosome abnormalities. III.
Ratcliffe, S. G., Tierney, I., Nshaho, J., et al. (1979) · PubMed · Cited by 209 · see citing works
Dulai, K. S., von Dornum, M., Mollon, J. D., & Hunt, D. M. (1999) · Genome Research · doi:10.1101/gr.9.7.629 · Cited by 207 · see citing works
Wersinger, S. R., & Rissman, E. F. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00418.x · Cited by 198 · see citing works
Self-citationInverted repeat structure of the Sry locus in mice.
Gubbay, J., Vivian, N., Economou, A., Jackson, D., Goodfellow, P. N., & Lovell-Badge, R. H. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.17.7953 · Cited by 194 · see citing works
Self-citationEstrogen Receptors Are Essential for Female Sexual Receptivity
Rissman, E. F., Early, A. H., Taylor, J. A., Korach, K. S., & Lubahn, D. B. (1997) · Endocrinology · doi:10.1210/endo.138.1.4985 · Cited by 188 · see citing works
Self-citationAn H–YDb epitope is encoded by a novel mouse Y chromosome gene
Greenfield, A., Scott, D. M., Pennisi, D. J., Ehrmann, I. E., Ellis, P., Cooper, L. T., Simpson, E., & Koopman, P. A. (1996) · Nature Genetics · doi:10.1038/ng1296-474 · Cited by 181 · see citing works
The genetic basis of XX-XY differences present before gonadal sex differentiation in the mouse
Burgoyne, P. S., Thornhill, A. R., Boudrean, S. K., Darling, S. M., Bishop, C. E., & Evans, E. P. (1995) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.1995.0159 · Cited by 168 · see citing works
Self-citationBeyer, C., Pilgrim, C., & Reisert, I. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-05-01325.1991 · Cited by 159 · see citing works
Sex determination in marsupials: evidence for a marsupial—eutherian dichotomy
Renfree, M. B., & Short, R. V. (1988) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1988.0112 · Cited by 156 · see citing works
Functional testicular tissue does not masculinize development of the zebra finch song system.
Wade, J., & Arnold, A. P. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.11.5264 · Cited by 154 · see citing works
Self-citationKay, G. F., Ashworth, A., Penny, G. D., Dunlop, M. M., Swift, S., Brockdorff, N., & Rastant, S. (1991) · Nature · doi:10.1038/354486a0 · Cited by 140 · see citing works
Some fluorescent counterstains for neuroanatomical studies.
Schmued, L. C., Swanson, L. W., & Sawchenko, P. E. (1982) · Journal of Histochemistry & Cytochemistry · doi:10.1177/30.2.6174560 · Cited by 139 · see citing works
The Y-chromosomal genes SRY and ZFY are transcribed in adult human brain
Mayer, A., Lahr, G., Swaab, D. F., Pilgrim, C., & Reisert, I. (1998) · Neurogenetics · doi:10.1007/s100480050042 · Cited by 137 · see citing works
Differential lateral septal vasopressin innervation in aggressive and nonaggressive male mice
Compaan, J. C., Buijs, R. M., Pool, C. W., De Ruiter, A. J. H., & koolhaas, J. M. (1993) · Brain Research Bulletin · doi:10.1016/0361-9230(93)90032-7 · Cited by 135 · see citing works
Medial amygdala and aggressive behavior: Interaction between testosterone and vasopressin
Koolhaas, J. M., Brink, T. H. C. V. D., Roozendaal, B., & Boorsma, F. (1990) · Aggressive Behavior · doi:10.1002/1098-2337(1990)16:3/4 · Cited by 134 · see citing works
Agoulnik, A. I., Mitchell, M. J., Lerner, J. L., Woods, D., & Bishop, C. E. (1994) · Human Molecular Genetics · doi:10.1093/hmg/3.6.873 · Cited by 132 · see citing works
Sex differences in hormonal responses of vasopressin pathways in the rat brain
De Vries, G. J., & Al‐Shamma, H. A. (1990) · Journal of Neurobiology · doi:10.1002/neu.480210503 · Cited by 129 · see citing works
Self-citationTranscription of the Y chromosomal gene,Sry, in adult mouse brain
Lahr, G., Maxson, S. C., Mayer, A., Just, W., Pilgrim, C., & Reisert, I. (1995) · Molecular Brain Research · doi:10.1016/0169-328x(95)00136-g · Cited by 123 · see citing works
Wang, Z., Bullock, N. A., & De Vries, G. J. (1993) · Endocrinology · doi:10.1210/endo.132.6.8504734 · Cited by 123 · see citing works
Self-citationY353/B: a candidate multiple-copy spermiogenesis gene on the mouse Y chromosome
Conway, S. J., Mahadevaiah, S. K., Darling, S. M., Capel, B., Rattigan, Á., & Burgoyne, P. S. (1994) · Mammalian Genome · doi:10.1007/bf00360546 · Cited by 117 · see citing works
Self-citationA perspective on color vision in platyrrhine monkeys
Jacobs, G. H. (1998) · Vision Research · doi:10.1016/s0042-6989(97)00405-7 · Cited by 103 · see citing works
Dopamine Activates Masculine Sexual Behavior Independent of the Estrogen Receptor α
Wersinger, S. R., & Rissman, E. F. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04248.2000 · Cited by 100 · see citing works
Self-citationMazeyrat, S., Saut, N., Sargent, C. A., Grimmond, S. M., Longepied, G., Ehrmann, I. E., Ellis, P. S., Greenfield, A., Affara, N. A., & Mitchell, M. J. (1998) · Human Molecular Genetics · doi:10.1093/hmg/7.11.1713 · Cited by 99 · see citing works
Paredes, R. G., Lopez, M., & Baum, M. J. (1998) · Hormones and Behavior · doi:10.1006/hbeh.1998.1435 · Cited by 90 · see citing works
Ehrmann, I. E., Ellis, P. S., Mazeyrat, S., Duthie, S. M., Brockdorff, N., Mattéi, M., Gavin, M. A., Affara, N. A., Brown, G. M., Simpson, E., et al. (1998) · Human Molecular Genetics · doi:10.1093/hmg/7.11.1725 · Cited by 90 · see citing works
Maxson, S. C., Ginsburg, B. E., & Trattner, A. (1979) · Behavior Genetics · doi:10.1007/bf01071302 · Cited by 82 · see citing works
Aggression in wild house mice: Current state of affairs
Sluyter, F., van Oortmerssen, G. A., de Ruiter, A. J. H., & Koolhaas, J. M. (1996) · Behavior Genetics · doi:10.1007/bf02359753 · Cited by 75 · see citing works
Domı́nguez-Salazar, E. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00674-6 · Cited by 74 · see citing works
Co-segregation of intermale aggression with the pseudoautosomal region of the Y chromosome in mice.
Roubertoux, P. L., Carlier, M., Degrelle, H., Haas-Dupertuis, M. C., Phillips, J., & Moutier, R. (1994) · Genetics · doi:10.1093/genetics/136.1.225 · Cited by 71 · see citing works
Reisert, I., Schuster, R., Zienecker, R., et al. (1990) · Developmental Brain Research · doi:10.1016/0165-3806(90)90010-v · Cited by 70 · see citing works
Neurosteroids and brain sexual differentiation
Schlinger, B. A., Soma, K. K., & London, S. E. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01855-5 · Cited by 69 · see citing works
Searching for candidate genes with effects on an agonistic behavior, offense, in mice
Maxson, S. C. (1996) · Behavior Genetics · doi:10.1007/bf02359751 · Cited by 67 · see citing works
Tdy -negative XY, XXY and XYY female mice: breeding data and synaptonemal complex analysis
Mahadevaiah, S. K., Lovell-Badge, R. H., & Burgoyne, P. S. (1993) · Reproduction · doi:10.1530/jrf.0.0970151 · Cited by 63 · see citing works
Self-citationSibug, R. M., Küppers, E., Beyer, C., Maxson, S. C., Pilgrim, C., & Reisert, I. (1996) · Developmental Brain Research · doi:10.1016/0165-3806(96)00024-7 · Cited by 60 · see citing works
Genomic Imprinting in Mice: Its Function and Mechanism1
Leighton, P. A., Saam, J. R., Ingram, R. S., et al. (1996) · Biology of Reproduction · doi:10.1095/biolreprod54.2.273 · Cited by 56 · see citing works
Guillot, P. V., Carlier, M., Maxson, S. C., & Roubertoux, P. L. (1995) · Behavior Genetics · doi:10.1007/bf02197285 · Cited by 55 · see citing works
Wee, B. E. F., & Clemens, L. G. (1987) · Brain Research · doi:10.1016/0006-8993(87)91475-2 · Cited by 54 · see citing works
Gonadal steroids influence neurophysin II distribution in the forebrain of normal and mutant mice
Mayes, C. R., Watts, A. G., McQueen, J., Fink, G., & Charlton, H. M. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90054-1 · Cited by 54 · see citing works
Beyer, C., Eusterschulte, B., Pilgrim, C., & Reisert, I. (1992) · Cell and Tissue Research · doi:10.1007/bf00645057 · Cited by 54 · see citing works
Pre- and postnatal development of dopaminergic neuron numbers in the male and female mouse midbrain
Lieb, K., Andersen, C., Lazarov, N., Zienecker, R., Urban, I., Reisert, I., & Pilgrim, C. (1996) · Developmental Brain Research · doi:10.1016/0165-3806(96)00063-6 · Cited by 52 · see citing works
Does sex determination start at conception?
Erickson, R. P. (1997) · BioEssays · doi:10.1002/bies.950191113 · Cited by 51 · see citing works
Beyer, C., Kolbinger, W., Froehlich, U., et al. (1992) · Brain Research · doi:10.1016/0006-8993(92)91315-6 · Cited by 49 · see citing works
Zambrowicz, B., Zimmermann, J. W., Harendza, C. J., et al. (1994) · Development · doi:10.1242/dev.120.6.1549 · Cited by 48 · see citing works
Taketo, T., Saeed, J., Nishioka, Y., et al. (1991) · Developmental Biology · doi:10.1016/0012-1606(91)90240-4 · Cited by 47 · see citing works
Age-dependent capacity for somatosensory cortex reorganization in chronic spinal cats
McKinley, P. A., Jenkins, W. M., Smith, J. L., et al. (1987) · Developmental Brain Research · doi:10.1016/0165-3806(87)90092-7 · Cited by 43 · see citing works
Hauser, K. F., & Toran‐Allerand, C. D. (1989) · Brain Research · doi:10.1016/0006-8993(89)90677-x · Cited by 42 · see citing works
Spatial ability of XY sex-reversed female mice
Stavnezer, A. J., McDowell, C. S., Hyde, L. A., et al. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00174-1 · Cited by 27 · see citing works
Wagner, C. K., & Clemens, L. G. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90303-x · Cited by 26 · see citing works
Autosomal and Y chromosomal effects on the stereotyped response to apomorphine in wild house mice
Sluyter, F., Bohus, B., Beldhuis, H. J. A., & van Oortmerssen, G. A. (1995) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)00092-b · Cited by 25 · see citing works
Linkage between brain serotonin concentration and the sex-specific part of the Y-chromosome in mice
Tordjman, S., Roubertoux, P. L., Carlier, M., Moutier, R., Anderson, G. M., Launay, M., & Degrelle, H. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(94)11148-c · Cited by 24 · see citing works
An analysis of meiotic impairment and of sex chromosome associations throughout meiosis in XYY mice
Mahadevaiah, S. K., Evans, E. P., & Burgoyne, P. S. (2000) · Cytogenetic and Genome Research · doi:10.1159/000015585 · Cited by 22 · see citing works
Self-citationY chromosomal effects on hippocampal mossy fiber distributions in mice selected for aggression
Hensbroek, R. A., Sluyter, F., Guillot, P. V., van Oortmerssen, G. A., & Crusio, W. E. (1995) · Brain Research · doi:10.1016/0006-8993(95)00270-z · Cited by 20 · see citing works
Neonatal adrogen treatment and sexual behavior in males of three inbred strains of mice
Vale, J. R., Ray, D., & Vale, C. A. (1974) · Developmental Psychobiology · doi:10.1002/dev.420070512 · Cited by 18 · see citing works
Experimental Analysis of Sexual Differentiation of the Zebra Finch Brain
Arnold, A. P. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00232-3 · Cited by 18 · see citing works
Self-citationIssues in the Search for Candidate Genes in Mice as Potential Animal models of Human Aggression
Maxson, S. C. (2007) · Novartis Foundation symposium · doi:10.1002/9780470514825.ch2 · Cited by 17 · see citing works
Sex differences in genetic mechanisms for mammalian brain and behavior
Maxson, S. C. (1997) · Biomedical Reviews · doi:10.14748/bmr.v7.165 · Cited by 15 · see citing works
Androstenedione Effects on the Vasopressin Innervation of the Rat Brain
Villalba, C., Auger, C. J., & Vries, G. J. D. (1999) · Endocrinology · doi:10.1210/endo.140.7.6934 · Cited by 14 · see citing works
Self-citationY353/B: a candidate multiple-copy spermiogenesis gene on the mouse Y chromosome
Conway, S. J. (1994) · Trends in Genetics · doi:10.1016/0168-9525(90)90002-n · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
A meta-analysis of sex differences in human brain structure
Ruigrok, A. N. V., Salimi-Khorshidi, G., Lai, M.-C., Baron-Cohen, S., Lombardo, M. V., Tait, R. J., & Suckling, J. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.12.004 · Cited by 1,192 · see citing works
Sex differences in pain and pain inhibition: multiple explanations of a controversial phenomenon
Mogil, J. S. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3360 · Cited by 1,065 · see citing works
Studying sex and gender differences in pain and analgesia: a consensus report
Greenspan, J. D., Craft, R. M., LeResche, L., Arendt-Nielsen, L., Berkley, K. J., Fillingim, R. B., Gold, M. S., Holdcroft, A., Lautenbacher, S., Mayer, E. A., et al. (2007) · Pain · doi:10.1016/j.pain.2007.10.014 · Cited by 1,033 · see citing works
Sex Differences in the Brain: The Not So Inconvenient Truth
McCarthy, M. M., Arnold, A. P., Ball, G. F., Blaustein, J. D., & De Vries, G. J. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5372-11.2012 · Cited by 724 · see citing works
Self-citationGillies, G. E., & McArthur, S. (2010) · Pharmacological Reviews · doi:10.1124/pr.109.002071 · Cited by 733 · see citing works
Consensus statement on management of intersex disorders
Hughes, I. A., Houk, C., Ahmed, S. F., & Lee, P. A. (2006) · Journal of Pediatric Urology · doi:10.1016/j.jpurol.2006.03.004 · Cited by 684 · see citing works
Arnold, A. P., & Chen, X. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.11.001 · Cited by 587 · see citing works
Self-citationDumais, K. M., & Veenema, A. H. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.04.003 · Cited by 520 · see citing works
“(2013) Golden hamsters PVN Delville et al. (1994) Macaques BNSN, MeA, PVN, SCN, SON, dorsomedial hypothalamus, LC, NTS, diagonal band Caffé et al.”
BackgroundInfluentialSex Differences in Traumatic Brain Injury: What We Know and What We Should Know
Gupte, R. P., Brooks, W. M., Vukas, R. R., Pierce, J. D., & Harris, J. L. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6171 · Cited by 533 · see citing works
Minireview: sex differences in adult and developing brains: compensation, compensation, compensation
De Vries, G. J. (2004) · Endocrinology · doi:10.1210/en.2003-1504 · Cited by 486 · see citing works
Self-citationSex differences in the physiology of eating
Asarian, L., & Geary, N. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00446.2012 · Cited by 513 · see citing works
Mechanisms of sex differences in Alzheimer’s disease
Lopez-Lee, C., Torres, E. R. S., Carling, G., & Gan, L. (2024) · Neuron · doi:10.1016/j.neuron.2024.01.024 · Cited by 376 · see citing works
Studying both sexes: a guiding principle for biomedicine
Clayton, J. A. (2016) · The FASEB Journal · doi:10.1096/fj.15-279554 · Cited by 358 · see citing works
De Vries, G. J., & Panzica, G. C. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.050 · Cited by 346 · see citing works
The Number of X Chromosomes Causes Sex Differences in Adiposity in Mice
Chen, X., McClusky, R., Chen, J., Beaven, S. W., Tontonoz, P., Arnold, A. P., & Reue, K. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002709 · Cited by 326 · see citing works
Self-citationFetal Testosterone Influences Sexually Dimorphic Gray Matter in the Human Brain
Lombardo, M. V., Ashwin, E., Auyeung, B., Chakrabarti, B., Taylor, K., Hackett, G., Bullmore, E. T., & Baron-Cohen, S. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4389-11.2012 · Cited by 302 · see citing works
Bakker, J., De Mees, C., Douhard, Q., Balthazart, J., Gabant, P., Szpirer, J., & Szpirer, C. (2006) · Nature Neuroscience · doi:10.1038/nn1624 · Cited by 305 · see citing works
Sleep, rhythms, and the endocrine brain: influence of sex and gonadal hormones
Mong, J. A., Baker, F. C., Mahoney, M. M., Paul, K. N., Schwartz, M. D., Semba, K., & Silver, R. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4175-11.2011 · Cited by 295 · see citing works
Chakrabarti, B., Dudbridge, F., Kent, L., Wheelwright, S., Hill‐Cawthorne, G., Allison, C., Banerjee‐Basu, S., & Baron‐Cohen, S. (2009) · Autism Research · doi:10.1002/aur.80 · Cited by 295 · see citing works
Gender Differences in Human Brain: A Review
Zaidi, Z. F. (2010) · The Open Anatomy Journal · doi:10.2174/1877609401002010037 · Cited by 229 · see citing works
Topical Review: Fetal Testosterone and Sex Differences in Typical Social Development and in Autism
Knickmeyer, R. C., & Baron-Cohen, S. (2006) · Journal of Child Neurology · doi:10.1177/08830738060210101601 · Cited by 230 · 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
Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition
Gabor, C. S., Phan, A., Clipperton-Allen, A. E., Kavaliers, M., & Choleris, E. (2012) · Behavioral Neuroscience · doi:10.1037/a0026464 · Cited by 221 · 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
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
Self-citationBurgoyne, P. S., & Arnold, A. P. (2016) · Biology of Sex Differences · doi:10.1186/s13293-016-0115-5 · Cited by 154 · see citing works
Self-citationRood, B. D., Stott, R. T., You, S., Smith, C. J. W., Woodbury, M. E., & De Vries, G. J. (2013) · Journal of Comparative Neurology · doi:10.1002/cne.23288 · Cited by 120 · see citing works
The importance of having two X chromosomes
Arnold, A. P., Reue, K., Eghbali, M., Vilain, E., Chen, X., Ghahramani, N., Itoh, Y., Li, J., Link, J. C., Ngun, T., et al. (2016) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0113 · Cited by 114 · see citing works
Self-citationComing of age in the Kisspeptin Era: Sex differences, development, and puberty
Kauffman, A. S. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.01.017 · Cited by 106 · see citing works
Itoh, Y., Mackie, R., Kampf, K., Domadia, S., Brown, J. D., O’Neill, R., & Arnold, A. P. (2015) · BMC Research Notes · doi:10.1186/s13104-015-0986-2 · Cited by 109 · see citing works
Self-citationCorre, C., Friedel, M., Vousden, D. A., Metcalf, A., Spring, S., Qiu, L. R., Lerch, J. P., & Palmert, M. R. (2016) · Brain Structure and Function · doi:10.1007/s00429-014-0952-0 · Cited by 98 · see citing works
A new view of sexual differentiation of mammalian brain
McCarthy, M. M. (2020) · Journal of Comparative Physiology A · doi:10.1007/s00359-019-01376-8 · Cited by 85 · see citing works
The Role of Genetic Sex in Affect Regulation and Expression of GABA-Related Genes Across Species
Seney, M. L., Chang, L.-C., Oh, H., Wang, X., Tseng, G. C., Lewis, D. A., & Sibille, E. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00104 · Cited by 78 · see citing works
DiBenedictis, B. T., Nussbaum, E. R., Cheung, H. K., & Veenema, A. H. (2017) · Journal of Comparative Neurology · doi:10.1002/cne.24216 · Cited by 74 · see citing works
“Furthermore, in addition to the activational and organizational effects of gonadal steroid hormones, the male Y chromosome also contributes to the masculinized expression of AVP-ir fibers in the LS (De Vries et al., 2002).”
BackgroundChen, X., Wang, L., Loh, D. H., Colwell, C. S., Taché, Y., Reue, K., & Arnold, A. P. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.07.020 · Cited by 64 · see citing works
Self-citationSex differences in brain expression of X- and Y-linked genes
Xu, J., & Disteche, C. M. (2006) · Brain Research · doi:10.1016/j.brainres.2006.08.049 · Cited by 63 · 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
Amphetamine reward in the monogamous prairie vole
Aragona, B. J., Detwiler, J. M., & Wang, Z. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.03.019 · Cited by 45 · see citing works
Lonstein, J. S., Rood, B. D., & De Vries, G. J. (2005) · Endocrinology · doi:10.1210/en.2004-1315 · Cited by 33 · see citing works
Bobotis, B. C., Khakpour, M., Braniff, O., de Andrade, E. G., Gargus, M., Allen, M., Carrier, M., Baillargeon, J., Rangachari, M., & Tremblay, M.-È. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03341-6 · Cited by 17 · see citing works
“…roles of sex chromosomes and gonadal hormones in driving differences in microglial properties between sexes during normal physiological conditions, we used the Four Core Genotypes (FCG) mouse model, which allows for an independent assessment of gonadal hormones and sex chromosomal effects [47–49].”
Sex differences in androgen regulation of metabolism in nonhuman primates
True, C., Abbott, D. H., Roberts, C. T., & Varlamov, O. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-70178-3_24 · Cited by 10 · see citing works
- Authors
- De Vries, G. J., Rissman, E. F., Simerly, R. B., Yang, L.-Y., Scordalakes, E. M., Auger, C. J., Swain, A., Lovell-Badge, R., Burgoyne, P. S., & Arnold, A. P.
- Affiliations
- University of Virginia (US)
- Oregon National Primate Research Center (US)
- University of California, Los Angeles (US)
- University of Massachusetts Amherst (US)
- Institute of Cancer Research (GB)
- National Institute for Medical Research (GB)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2002-10-15
- Volume
- 22
- Issue
- 20
- Pages
- 9005-9014
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6757680
- OpenAlex
- W4294333306
- Cited by
- 509
- References
- 82
- Citations by year
- 2026: 19 · 2025: 21 · 2024: 32 · 2023: 32 · 2022: 28 · 2021: 20 · 2020: 21 · 2019: 20 · 2018: 20 · 2017: 17 · 2016: 26 · 2015: 19 · 2014: 21 · 2013: 28 · 2012: 25
- FWCI
- 6.74
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- Funders
- National Institutes of Health (U54-HD28-934, HD28934)
- Directorate for Biological Sciences
- National Institute of Mental Health (R01 MH 57759, K02 MH-01349, K02MH001349, R01MH057759)
- National Institute of Child Health and Human Development (U54-HD28934)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (N01-HD-73263, U54HD028934, U54-HD-28934)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- sex chromosomes, sexual differentiation of the brain, SRY, testis-determining gene, Y chromosome, gonadal hormones, sexually dimorphic behavior, mating behavior, social exploration, lateral septum, vasopressin, hypothalamus, lumbar spinal cord, sex differences in brain structure
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
