Intraspecific variation in estrogen receptor alpha and the expression of male sociosexual behavior in two populations of prairie voles

Cushing, Bruce S; Razzoli, Maria; Murphy, Anne Z; Epperson, Pamela M; Le, Wei-Wei; Hoffman, Gloria E

doi:10.1016/j.brainres.2004.05.010

Cited by 77Neuroendocrine regulation and behaviorSexual Differentiation and DisordersAnimal Behavior and Reproduction

Intraspecific variation in estrogen receptor alpha and the expression of male sociosexual behavior in two populations of prairie voles

Cushing, Bruce S, Razzoli, Maria, Murphy, Anne Z, Epperson, Pamela M, Le, Wei-Wei, Hoffman, Gloria E·2004·Brain Research

DOI 10.1016/j.brainres.2004.05.010

Open this paper in CoChat — free account

Abstract

Estrogen (E) regulates a variety of male sociosexual behaviors. We hypothesize that there is a relationship between the distribution of estrogen receptor alpha (ERalpha) and the degree of male social behavior. To test this hypothesis, ERalpha immunoreactivity (IR) was compared in prairie voles (Microtus ochrogaster) from Illinois (IL), which are highly social, and Kansas (KN), which are less social. The expression of androgen receptors (AR) in males also was compared between populations. The expression of ERalpha and AR were compared in brains from KN and IL males and females using immunocytochemistry (ICC). There were significant intrapopulational differences, with males expressing less ERalpha-IR than females in the medial preoptic area, ventromedial nucleus, ventrolateral portion of the hypothalamus, and bed nucleus of the stria terminalis (BST). IL males also displayed less ERalpha-IR in the medial amygdala (MeA) than IL females. While IL males expressed significantly less ERalpha-IR in the BST and MeA than KN males, there was no difference in AR-IR. Differences in the pattern of ERalpha-IR between KN and IL males were behaviorally relevant, as low levels of testosterone (T) were more effective in restoring sexual activity in castrated KN males than IL males. The lack of difference in AR combined with lower expression of ERalpha-IR in IL males suggests that behavioral differences in response to T are associated with aromatization of T to E and that reduced sensitivity to E may facilitate prosocial behavior in males.

Integrity signals

Registry

Crossref · 10.1016/j.brainres.2004.05.010

Cites

63 of 63 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Some population differences in prairie voles are associated with differences in estrogen receptor expression in the brain.
“However, Kansas voles are more socially and genetically monogamous than voles in an Indiana population [63] and some of these population differences are associated with differences in estrogen receptor expression in the brain [64].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [64]

The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
The Physiology of Reproduction
Legendre, M., & Jalabert, B. (1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-109-2-176_1 · Cited by 7,879 · see citing works
Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study
Simerly, R. B., Swanson, L. W., Chang, C., & Muramatsu, M. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.902940107 · Cited by 2,118 · see citing works
Hormones, Brain and Behavior
(2009) · Elsevier eBooks · doi:10.1016/c2009-1-03789-7 · Cited by 1,543 · see citing works
The Medial Extended Amygdala in Male Reproductive Behavior A Node in the Mammalian Social Behavior Network
NEWMAN, S. W. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09271.x · Cited by 1,189 · see citing works
Oxytocin in the Medial Amygdala is Essential for Social Recognition in the Mouse
Ferguson, J. N., Aldag, J. M., Insel, T. R., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-20-08278.2001 · Cited by 1,043 · see citing works
Cooperative Breeding in Mammals
(1996) · Cambridge University Press eBooks · doi:10.1017/cbo9780511574634 · Cited by 970 · see citing works
A role for central vasopressin in pair bonding in monogamous prairie voles
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. (1993) · Nature · doi:10.1038/365545a0 · Cited by 948 · see citing works
Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology
Watson, R. E., Wiegand, S. J., Clough, R. W., & Hoffman, G. E. (1986) · Peptides · doi:10.1016/0196-9781(86)90076-8 · Cited by 933 · see citing works
Self-citation
Hormones, brain and behavior
(2003) · Choice Reviews Online · doi:10.5860/choice.40-2774 · Cited by 705 · 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
The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster)
Cho, M. M., DeVries, A. C., Williams, J. R., & Carter, C. S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.1071 · Cited by 529 · see citing works
A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles
Insel, T. R., & Hulihan, T. J. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.4.782 · Cited by 528 · see citing works
The vasopressinergic innervation of the brain in normal and castrated rats
DeVries, G. J., Buijs, R. M., van Leeuwen, F. W., Caffé, A. R., & Swaab, D. F. (1985) · Journal of Comparative Neurology · doi:10.1002/cne.902330206 · Cited by 522 · see citing works
Behavioral effects of estrogen receptor gene disruption in male mice
Ogawa, S., Lubahn, D. B., Korach, K. S., & Pfaff, D. W. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.4.1476 · Cited by 498 · see citing works
Oxytocin Administered Centrally Facilitates Formation of a Partner Preference in Female Prairie Voles (Microtus ochrogaster)
Williams, 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
The mating system of the prairie vole, microtus-ochrogaster – field and laboratory evidence for pair-bonding
Getz, L. L., Carter, C. S., & Gavish, L. (1981) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00299829 · Cited by 466 · see citing works
Monogamy and the Prairie Vole
Carter, C. S., & Getz, L. L. (1993) · Scientific American · doi:10.1038/scientificamerican0693-100 · Cited by 310 · see citing works
Modifications of Testosterone-Dependent Behaviors by Estrogen Receptor-α Gene Disruption in Male Mice1
Ogawa, S., Washburn, T. F., Taylor, J. A., Lubahn, D. B., Korach, K. S., & Pfaff, D. W. (1998) · Endocrinology · doi:10.1210/endo.139.12.6358 · Cited by 290 · see citing works
Masculine Sexual Behavior Is Disrupted in Male and Female Mice Lacking a Functional Estrogen Receptor α Gene
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
Testosterone promotes paternal behaviour in a monogamous mammal via conversion to oestrogen
Trainor, B. C., & Marler, C. A. (2002) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rspb.2001.1954 · Cited by 238 · 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
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
Estrogen Receptor Messenger RNA Expression in Rat Hypothalamus as a Function of Genetic Sex and Estrogen Dose*
LAUBER, A. H., Mobbs, C. V., Muramatsu, M., & Pfaff, D. W. (1991) · Endocrinology · doi:10.1210/endo-129-6-3180 · Cited by 209 · see citing works
Oestrogen Receptor α is Essential for Female‐Directed Chemo‐Investigatory Behaviour but is not Required for the Pheromone‐Induced Luteinizing Hormone Surge in Male Mice
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
Sex differences in the effects of testosterone and its metabolites on vasopressin messenger RNA levels in the bed nucleus of the stria terminalis of rats
De Vries, G., Wang, Z., Bullock, N., & Numan, S. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-03-01789.1994 · Cited by 193 · cited 1× · see citing works
“Finally, E regulates the effects of the neuropeptides oxytocin and arginine vasopressin [ 10 ,16,22,47] .R egulating the response to oxytocin and vasopressin may be critical to the ‘‘proper’’ or species-specific expression of social behavior as these neuropeptides facilitate social interactions, such as pair bond form…”
Background
Sexual and social experience is associated with different patterns of behavior and neural activation in male prairie voles
Wang, Z., Hulihan, T. J., & Insel, T. R. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00617-3 · Cited by 169 · see citing works
Sexual Partner Preference Requires a Functional Aromatase (Cyp19) Gene in Male Mice
Bakker, J., Honda, S., Harada, N., & Balthazart, J. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2002.1805 · Cited by 155 · see citing works
Cooperative breeding and monogamy in prairie voles: influence of the sire and geographical variation
Roberts, R. L., WILLIAMS, J. R., Wang, A. S., & Carter, C. S. (1998) · Animal Behaviour · doi:10.1006/anbe.1997.0659 · Cited by 152 · see citing works
Sex with knockout models: behavioral studies of estrogen receptor α1Published on the World Wide Web on 26 April 1999.1
Rissman, E. F., Wersinger, S. R., Fugger, H. N., & Foster, T. C. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01452-3 · Cited by 150 · see citing works
Functional activities of the amygdala: an overview.
Rasia‐Filho, A. A., Londero, R. G., & Achaval, M. (2000) · PubMed Central · Cited by 140 · see citing works
Steroid Dependency of Vasopressin Neurons in the Bed Nucleus of the Stria Terminalis byin SituHybridization*
MILLER, M. A., URBAN, J. H., & DORSA, D. M. (1989) · Endocrinology · doi:10.1210/endo-125-5-2335 · Cited by 134 · see citing works
The Role of Aromatization in the Restoration of Male Rat Reproductive Behavior
Vagell, M. E., & McGinnis, M. Y. (1997) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1997.00598.x · Cited by 130 · see citing works
Testosterone effects on paternal behavior and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster)
Wang, Z., & Vries, G. J. D. (1993) · Brain Research · doi:10.1016/0006-8993(93)91203-5 · Cited by 129 · see citing works
Decline of vasopressin immunoreactivity and mRNA levels in the bed nucleus of the stria terminalis following castration
Miller, M., DeVries, G., al-Shamma, H., & Dorsa, D. (1992) · The Journal of Neuroscience · doi:10.1523/jneurosci.12-08-02881.1992 · Cited by 122 · see citing works
Organizational effects of testosterone, estradiol, and dihydrotestosterone on vasopressin mRNA expression in the bed nucleus of the stria terminalis
Han, T. M., & De Vries, G. J. (2003) · Journal of Neurobiology · doi:10.1002/neu.10157 · Cited by 116 · see citing works
Inhibition of male sex behavior by androgen receptor blockade in preoptic area or hypothalamus, but not amygdala or septum
McGinnis, M. Y., Williams, G. W., & Lumia, A. R. (1996) · Physiology & Behavior · doi:10.1016/0031-9384(96)00088-1 · Cited by 104 · see citing works
Androgen and estrogen concentrating neurons in chemosensory pathways of the male Syrian hamster brain
Wood, R. I., Brabec, R. K., Swann, J. M., & Newman, S. W. (1992) · Brain Research · doi:10.1016/0006-8993(92)91536-n · Cited by 99 · see citing works
The effects of peptides on partner preference formation are predicted by habitat in prairie voles
Cushing, B. S., Martin, J. O., Young, L. J., & Carter, C. S. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2000.1633 · Cited by 99 · see citing works
Self-citation
Infertility and Testicular Atrophy in the Antiestrogen-Treated Adult Male Rat1
Oliveira, C. A., Carnes, K. I., França, L. R., & Hess, R. A. (2001) · Biology of Reproduction · doi:10.1095/biolreprod65.3.913 · Cited by 97 · see citing works
The Distribution of Cells Containing Estrogen Receptor-α (ERα) and ERβ Messenger Ribonucleic Acid in the Preoptic Area and Hypothalamus of the Sheep: Comparison of Males and Females
Scott, C., Tilbrook, A. J., Simmons, D. M., Rawson, J. A., Chu, S., Fuller, P. J., Ing, N. H., & Clarke, I. J. (2000) · Endocrinology · doi:10.1210/endo.141.8.7622 · Cited by 95 · see citing works
Anatomical Localization of the Effects of 17β-Estradiol on Oxytocin Receptor Binding in the Ventromedial Hypothalamic Nucleus*
Johnson, A. E., Coirini, H., Ball, G. F., & McEwen, B. S. (1989) · Endocrinology · doi:10.1210/endo-124-1-207 · Cited by 94 · see citing works
Gender-Specific Steroid Metabolism in Neural Differentiation
Hutchison, J. B. (1997) · Cellular and Molecular Neurobiology · doi:10.1023/a:1022581902880 · Cited by 94 · see citing works
Estradiol, but not dihydrotestosterone, in the medial amygdala facilitates male hamster sex behavior
Wood, R. I. (1996) · Physiology & Behavior · doi:10.1016/0031-9384(95)02204-x · Cited by 89 · see citing works
Variations in concentration of oxytocin and vasopressin in the paraventricular nucleus of the hypothalamus during the estrous cycle in rats
Greer, E. R., Caldwell, J. D., Johnson, M. F., Prange, A. J., & Pedersen, C. A. (1986) · Life Sciences · doi:10.1016/0024-3205(86)90638-7 · Cited by 77 · see citing works
The Role of Gonadal Steroid Receptor Activation in the Restoration of Sociosexual Behavior in Adult Male Rats
Vagell, M. E., & McGinnis, M. Y. (1998) · Hormones and Behavior · doi:10.1006/hbeh.1998.1445 · Cited by 75 · see citing works
Brain Sexual Dimorphism and Sex Differences in Parental and Other Social Behaviorsa
Vries, G. J. D., & Villalba, C. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51926.x · Cited by 68 · see citing works
Estrogen receptor-α is required by the supporting somatic cells for spermatogenesis
Mahato, D., Goulding, E. H., Korach, K. S., & Eddy, E. M. (2001) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00410-5 · Cited by 65 · see citing works
Regional and cellular distribution of serotonin 5-hydroxytryptamine2a receptor mRNA in the nucleus accumbens, olfactory tubercle, and caudate putamen of the rat
Mijnster, M. J., Raimundo, A. G. V., Koskuba, K., Klop, H., Docter, G. J., Groenewegen, H. J., & Voorn, P. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19971208)389:1 · Cited by 59 · see citing works
Estrogen Receptor Immunoreactivity in Specific Brain Areas of the Prairie Vole (Microtus ochrogaster) is Altered by Sexual Receptivity and Genetic Sex
Hnatczuk, O. C., Lisciotto, C. A., DonCarlos, L. L., Carter, C. S., & Morrell, J. I. (1994) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1994.tb00558.x · Cited by 56 · see citing works
Parental Responsiveness Is Feminized after Neonatal Castration in Virgin Male Prairie Voles, but Is Not Masculinized by Perinatal Testosterone in Virgin Females
Lonstein, J. S., Rood, B. D., & Vries, G. J. D. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2001.1740 · Cited by 53 · see citing works
Estradiol in the male rat amygdala facilitates mounting but not ejaculation
Huddleston, G. G., Michael, R. P., Zumpe, D., & Clancy, A. N. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00114-8 · Cited by 50 · see citing works
Mechanisms of insulin-like growth factor regulation of programmed cell death of developing avian motoneurons
D'Costa, A. P., Prevette, D. M., Houenou, L. J., Wang, S., Zackenfels, K., Rohrer, H., Zapf, J., Caroni, P., & Oppenheim, R. W. (1998) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(19980905)36:3 · Cited by 49 · see citing works
Sexual differentiation of estrogen receptor concentrations in the rat brain: effects of neonatal testosterone exposure
Kühnemann, S., Brown, T. J., Hochberg, R. B., & MacLusky, N. J. (1995) · Brain Research · doi:10.1016/0006-8993(95)00640-c · Cited by 48 · see citing works
Intraspecific Variation in the Induction of Female Sexual Receptivity in Prairie Voles
Roberts, R. L., Cushing, B. S., & Carter, C. S. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00042-0 · Cited by 43 · see citing works
Self-citation
Steroid hormones and their receptors in the brain
Kawata, M., Yuri, K., Ozawa, H., Nishi, M., Ito, T., Hu, Z.-T., Lu, H., & Yoshida, M. (1998) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(98)00026-0 · Cited by 41 · see citing works
Testosterone-sensitive neurones respond to oestradiol but not to dihydrotestosterone
Kendrick, K. M., & Drewett, R. F. (1980) · Nature · doi:10.1038/286067a0 · Cited by 32 · see citing works
Sexually dimorphic cell groups in the medial preoptic area that are essential for male sex behavior and the neural pathways needed for their effects
Yahr, P., Finn, P. D., Hoffman, N. W., & Sayag, N. (1994) · Psychoneuroendocrinology · doi:10.1016/0306-4530(94)90033-7 · Cited by 31 · see citing works
Sex Differences in Male-Typical Copulatory Behaviors in Response to Androgen and Estrogen Treatment in Rats
Roselli, C. E., & Chambers, K. C. (1999) · Neuroendocrinology · doi:10.1159/000054430 · Cited by 28 · see citing works
Manipulation of aggressive behavior in male prairie voles (Microtus ochrogaster) implanted with testosterone in Silastic tubing
Gaines, M. S., Fugate, C. L., Johnson, M. L., Johnson, D., Hisey, J. R., & Quadagno, D. M. (1985) · Canadian Journal of Zoology · doi:10.1139/z85-374 · Cited by 27 · see citing works
A stereotaxic atlas of the forebrain of the bank vole (Clethrionomys glareolus)
Vandebroek, I., Bouche, K., D'Herde, K. G. M. A., Caemaert, J., Roels, F., & Ödberg, F. O. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(98)00137-3 · Cited by 6 · see citing works
Effects of androgen and estrogen receptor ligands on early postnatal expression of VP mRNA in the BNST and MA
Szot, P., & Dorsa, D. M. (1994) · Endocrine · Cited by 3 · see citing works

Flagged first, then by citations

Sorted by citations

The prairie vole: An emerging model organism for understanding the social brain
McGraw, L. A., & Young, L. J. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2009.11.006 · Cited by 276 · see citing works
Mechanisms underlying epigenetic effects of early social experience: the role of neuropeptides and steroids
CUSHING, B., & KRAMER, K. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.001 · Cited by 209 · see citing works
Self-citation
Social flexibility and social evolution in mammals: a case study of the African striped mouse ( Rhabdomys pumilio )
Carsten Schradin, A., Lindholm, A. K., Johannesen, J., Schoepf, I., Yuen, C., König, B., & Pillay, N. (2011) · Molecular Ecology · doi:10.1111/j.1365-294x.2011.05256.x · Cited by 160 · see citing works
Intraspecific variation in social organization by genetic variation, developmental plasticity, social flexibility or entirely extrinsic factors
Carsten Schradin, A. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0346 · Cited by 151 · see citing works
Low sex steroids, high steroid receptors: Increasing the sensitivity of the nonreproductive brain
Canoine, V., Fusani, L., Schlinger, B., & Hau, M. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20296 · Cited by 133 · see citing works
Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes
Horton, B. M., Hudson, W. H., Ortlund, E. A., Shirk, S., Thomas, J. W., Young, E. R., Zinzow-Kramer, W. M., & Maney, D. L. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1317165111 · Cited by 105 · see citing works
Estrogen regulation of cell proliferation and distribution of estrogen receptor‐α in the brains of adult female prairie and meadow voles
Fowler, C. D., Johnson, F., & Wang, Z. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20638 · Cited by 99 · see citing works
Estrogen receptors in the medial amygdala inhibit the expression of male prosocial behavior
Cushing, B. S., Perry, A., Musatov, S., Ogawa, S., & Papademetriou, E. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1928-08.2008 · Cited by 95 · see citing works
Self-citation
Prenatal hormones in first‐time expectant parents: Longitudinal changes and within‐couple correlations
Edelstein, R. S., Wardecker, B. M., Chopik, W. J., Moors, A. C., Shipman, E. L., & Lin, N. J. (2014) · American Journal of Human Biology · doi:10.1002/ajhb.22670 · Cited by 79 · see citing works
The effects of social context on the hormonal and behavioral responsiveness of human fathers
Storey, A. E., Noseworthy, D. E., Delahunty, K. M., Halfyard, S. J., & McKay, D. W. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.07.001 · Cited by 75 · 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
Self-citation
Polymorphism at the avpr1a locus in male prairie voles correlated with genetic but not social monogamy in field populations
Solomon, N. G., Richmond, A. R., Harding, P. A., FRIES, A., Jacquemin, S., Schaefer, R. L., Lucia, K. E., & Keane, B. (2009) · Molecular Ecology · doi:10.1111/j.1365-294x.2009.04361.x · Cited by 70 · 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
Self-citation
Estrogen Receptor-α in the Bed Nucleus of the Stria Terminalis Regulates Social Affiliation in Male Prairie Voles (Microtus ochrogaster)
Lei, K., Cushing, B. S., Musatov, S., Ogawa, S., & Kramer, K. M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008931 · Cited by 67 · see citing works
Self-citation
Oxytocin, vasopressin and estrogen receptor gene expression in relation to social recognition in female mice
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
A supergene-linked estrogen receptor drives alternative phenotypes in a polymorphic songbird
Merritt, J. R., Grogan, K. E., Zinzow-Kramer, W. M., Sun, D., Ortlund, E., Yi, S. V., & Maney, D. (2020) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2011347117 · Cited by 49 · see citing works
Sex-specific effects of perinatal FireMaster® 550 (FM 550) exposure on socioemotional behavior in prairie voles
Gillera, S. E. A., Marinello, W. P., Horman, B. M., Phillips, A. L., Ruis, M. T., Stapleton, H. M., Reif, D. M., & Patisaul, H. B. (2019) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2019.106840 · Cited by 48 · see citing works
Parenting Behavior
Lonstein, J. S., Pereira, M., Morrell, J. I., & Marler, C. A. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00051-x · Cited by 46 · 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
Differential Control of Sex Differences in Estrogen Receptor α in the Bed Nucleus of the Stria Terminalis and Anteroventral Periventricular Nucleus
Kelly, D. A., Varnum, M. M., Krentzel, A. A., Krug, S., & Forger, N. G. (2013) · Endocrinology · doi:10.1210/en.2013-1239 · Cited by 44 · see citing works
Raised without a father: monoparental care effects over development, sexual behavior, sexual reward, and pair bonding in prairie voles
Valera-Marín, G., Young, L. J., Camacho, F., Paredes, R. G., Rodríguez, V. M., Díaz, N. F., & Portillo, W. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113264 · Cited by 42 · see citing works
Morphological, Genetic, and Behavioral Comparisons of Two Prairie Vole Populations in the Field and Laboratory
Ophir, A. G., Phelps, S. M., Sorin, A. B., & Wolff, J. O. (2007) · Journal of Mammalogy · doi:10.1644/06-mamm-a-250r.1 · Cited by 40 · see citing works
True polyandry and pseudopolyandry: why does a monandrous fly remate?
Fisher, D. N., Doff, R. J., & Price, T. A. R. (2013) · BMC Evolutionary Biology · doi:10.1186/1471-2148-13-157 · Cited by 39 · see citing works
Estrogen dependent activation function of ERβ is essential for the sexual behavior of mouse females
Antal, M., Petit-Demoulière, B., Meziane, H., Chambon, P., & Krust, A. (2012) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1217668109 · Cited by 25 · see citing works
Polymorphisms in sex steroid receptors: From gene sequence to behavior
Maney, D. L. (2017) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.07.003 · Cited by 38 · see citing works
Low sex steroids, high steroid receptors: Increasing the sensitivity of the nonreproductive brain
Canoine, V., Fusani, L., Schlinger, B. A., & Hau, M. (2006) · Journal of Neurobiology · doi:10.1002/neu.20296 · Cited by 36 · see citing works
Species Differences in the Immunoreactive Expression of Oxytocin, Vasopressin, Tyrosine Hydroxylase and Estrogen Receptor Alpha in the Brain of Mongolian Gerbils (Meriones unguiculatus) and Chinese Striped Hamsters (Cricetulus barabensis)
Wang, Y., Xu, L., Pan, Y., Wang, Z., & Zhang, Z. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065807 · Cited by 33 · see citing works
Parental regulation of central patterns of estrogen receptor α
Kramer, K. M., Carr, M. S., Schmidt, J. V., & Cushing, B. S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.05.069 · Cited by 32 · see citing works
Self-citation
A mechanism for population self‐regulation: Social density suppresses GnRH expression and reduces reproductivity in voles
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
Comparison of sociability, parental care and central estrogen receptor alpha expression between two populations of mandarin voles (Microtus mandarinus)
Wu, R., Yuan, A., Yuan, Q.-W., Guo, R., Tai, F., Song, Z., & Yu, C. (2010) · Journal of Comparative Physiology A · doi:10.1007/s00359-010-0609-2 · Cited by 26 · see citing works
Estrogen Receptor Alpha Distribution and Expression in the Social Neural Network of Monogamous and Polygynous Peromyscus
Cushing, B. S. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150373 · Cited by 25 · see citing works
Self-citation
Effects of postnatal estrogen manipulations on juvenile alloparental behavior
Perry, A. N., Sue Carter, C., & Cushing, B. S. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.07.019 · Cited by 24 · see citing works
Self-citation
A neural circuit perspective on brain aromatase
Spool, J. A., Bergan, J. F., & Remage‐Healey, L. (2021) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2021.100973 · Cited by 25 · see citing works
Androgenic and oestrogenic influences on tyrosine hydroxylase-immunoreactive cells of the prairie vole medial amygdala and bed nucleus of the stria terminalis
Cavanaugh, B. L., & Lonstein, J. S. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.01958.x · Cited by 23 · see citing works
Hormonal Correlates of Paternal Care Differences in the H ylobatidae
Rafacz, M. L., MARGULIS, S., & Santymire, R. M. (2012) · American Journal of Primatology · doi:10.1002/ajp.21994 · Cited by 22 · see citing works
Alteration in oxytocin levels induced by early social environment affects maternal behavior and estrogen receptor alpha in mandarin voles (Microtus mandarinus)
Feng, T., An, S., Kinden, R., Zhang, X., Jia, R., & Tai, F. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.02.038 · Cited by 18 · see citing works
Inhibiting ERα expression in the medial amygdala increases prosocial behavior in male meadow voles (Microtus pennsylvanicus)
Stetzik, L. A., Ganshevsky, D., Lende, M. N., Roache, L. E., Musatov, S. A., & Cushing, B. S. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.05.035 · Cited by 18 · see citing works
Self-citation
Sex steroids are necessary in the second postnatal week for the expression of male alloparental behavior in prairie voles (Microtus ochragaster)
Kramer, K. M., Perry, A. N., Golbin, D., & Cushing, B. S. (2009) · Behavioral Neuroscience · doi:10.1037/a0016927 · Cited by 19 · see citing works
Self-citation
Estrogen Receptor Alpha as a Mediator of Life-History Trade-offs
Maney, D. L., Horton, B. M., & Zinzow-Kramer, W. M. (2015) · Integrative and Comparative Biology · doi:10.1093/icb/icv005 · Cited by 17 · see citing works
Sex differences and effects of neonatal aromatase inhibition on masculine and feminine copulatory potentials in prairie voles
Northcutt, K. V., & Lonstein, J. S. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.02.008 · Cited by 17 · see citing works
Individual Variation in Social Behaviours of Male Lab-reared Prairie voles (Microtus ochrogaster) is Non-heritable and Weakly Associated with V1aR Density
Vogel, A. R., Patisaul, H. B., Arambula, S. E., Tiezzi, F., & McGraw, L. A. (2018) · Scientific Reports · doi:10.1038/s41598-018-19737-9 · Cited by 17 · see citing works
Effects of castration on aggression and levels of serum sex hormones and their central receptors in mandarin voles (Microtus mandarinus)
He, F., Tai, F.-D., Zhang, Y.-H., & Zhang, X. (2012) · Journal of Comparative Physiology · doi:10.1007/s00359-012-0713-6 · Cited by 16 · see citing works
Chronic social isolation enhances reproduction in the monogamous prairie vole (Microtus ochrogaster)
Perry, A. N., Carter, C. S., & Cushing, B. S. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.02.016 · Cited by 15 · see citing works
Self-citation
BAC-Based Sequencing of Behaviorally-Relevant Genes in the Prairie Vole
McGraw, L. A., Davis, J. K., Thomas, P. J., Program, N. C. S., Young, L. J., & Thomas, J. W. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029345 · Cited by 15 · see citing works
Sexual Differentiation of Brain and Behavior
Forger, N. G., Vries, G. J. D., & Breedlove, S. M. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00047-8 · Cited by 12 · see citing works
Comparative analysis of gonadal hormone receptor expression in the postnatal house mouse, meadow vole, and prairie vole brain
Denney, K. A., Wu, M. V., Sun, S. D., Moon, S., & Tollkühn, J. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105463 · Cited by 11 · see citing works
Social environment alters central distribution of estrogen receptor alpha in juvenile prairie voles
Ruscio, M. G., Sweeny, T. D., Gomez, A. M., Parker, K., & Carter, C. S. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.06.005 · Cited by 11 · see citing works
Sodium acetate, an arterial vasodilator: haemodynamic characterisation in normal dogs.
Saragoça, M. A., Bessa, A. M., Mulinari, R. A., Draibe, S. A., Ribeiro, A. B., & Ramos, O. L. (1985) · PubMed · Cited by 11 · see citing works
Differences in Diffusion-Weighted Imaging and Resting-State Functional Connectivity Between Two Culturally Distinct Populations of Prairie Vole
Ortiz, R. J., Yee, J. R., Kulkarni, P. P., Solomon, N. G., Keane, B., Cai, X., Ferris, C. F., & Cushing, B. S. (2020) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2020.08.014 · Cited by 9 · see citing works
Self-citation
The organizational effects of oxytocin and vasopressin: Behavioral implications
Cushing, B. S. (2013) · Oxytocin, Vasopressin and Related Peptides in the Regulation of Behavior · doi:10.1017/cbo9781139017855.006 · Cited by 9 · see citing works
Self-citation
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
Estrogen and oxytocin involvement in social preference in male mice: a study using a novel long‐term social preference paradigm with aromatase, estrogen receptor‐α and estrogen receptor‐β, oxytocin, and oxytocin receptor knockout male mice
Tsuda, M. C., Nagata, K., Sagoshi, S., & Ogawa, S. (2018) · Integrative Zoology · doi:10.1111/1749-4877.12343 · Cited by 9 · see citing works
In Three Brain Regions Central to Maternal Behaviour, Neither Male Nor Female Phodopus Dwarf Hamsters Show Changes in Oestrogen Receptor Alpha Distribution with Mating or Parenthood
Timonin, M. E., Cushing, B. S., & Wynne‐Edwards, K. E. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01797.x · Cited by 9 · see citing works
Self-citation
Medial amygdala ERα expression influences monogamous behaviour of male prairie voles in the field
Lambert, C. T., Lichter, J. B., Perry, A. N., Castillo, S. A., Keane, B., Cushing, B. S., & Solomon, N. G. (2021) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2021.0318 · Cited by 7 · see citing works
Self-citation
Maternal and paternal origin differentially affect prosocial behavior and neural mechanisms in prairie voles
Stetzik, L. A., Payne, R. E., Roache, L. E., Ickes, J. R., & Cushing, B. S. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.12.001 · Cited by 7 · see citing works
Self-citation
Expression of Oestrogen Receptor α in the Brain of Brandt’s Voles (Lasiopodomys brandtii ): Sex Differences and Variations During Ovarian Cycles
Pan, Y., Xu, L., Wang, Z., & Zhang, Z. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02210.x · Cited by 7 · see citing works
Effects of the gender factor and neonatal androgenization on the dendroarchitectonics of neurons in the dorsomedial nucleus of the amygdaloid body of the brain
Ахмадеев, А. В. (2007) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-007-0048-x · Cited by 7 · see citing works
Functional Connectivity Differences Between Two Culturally Distinct Prairie Vole Populations: Insights Into the Prosocial Network
Ortiz, R. J., Wagler, A. E., Yee, J. R., Kulkarni, P. P., Cai, X., Ferris, C. F., & Cushing, B. S. (2021) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2021.11.007 · Cited by 7 · see citing works
Self-citation
How Fathers Evolve: A Functional Analysis of Fathering Behavior
Storey, A. E., & Walsh, C. J. (2010) · National symposium on family issues · doi:10.1007/978-1-4419-7361-0_2 · Cited by 7 · see citing works
Developmental expression of estrogen receptor beta in the brain of prairie voles (Microtus ochrogaster)
Ploskonka, S. D., Eaton, J. L., Carr, M. S., Schmidt, J. V., & Cushing, B. S. (2016) · Developmental Psychobiology · doi:10.1002/dev.21367 · Cited by 7 · see citing works
Self-citation
Progesterone receptor expression in the brain of the socially monogamous and paternal male prairie vole
Williams, B., Northcutt, K. V., Rusanowsky, R. D., Mennella, T. A., Lonstein, J. S., & Quadros-Mennella, P. S. (2013) · Brain Research · doi:10.1016/j.brainres.2013.01.011 · Cited by 6 · see citing works
Neural control of sex differences in affiliative and prosocial behaviors
Mikulovic, S., & Lenschow, C. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106039 · Cited by 5 · see citing works
Sexual cues influence cocaine‐induced locomotion, anxiety and the immunoreactivity of oestrogen receptor alpha and tyrosine hydroxylase in both sexes
He, C., Wang, J.-L., Ma, M., & Wang, H. (2019) · Journal of neuroendocrinology · doi:10.1111/jne.12720 · Cited by 4 · see citing works
Differences in auditory brainstem responses between laboratory-reared and wild-caught prairie voles (Microtus ochrogaster)
Joseph, L., Colon-Rivera, N., New, E. M., Joseph, D. M., Hurd, J. A., Sergott, C. E., & McCullagh, E. A. (2026) · PLoS ONE · doi:10.1371/journal.pone.0335120 · Cited by 2 · see citing works
Bases hormonals de la conducta prosocial: una revisió de la literatura
Lerma, F. S., Manuel, M. V., & Susana, L. T. (2016) · Anuari de Psicologia de la Societat Valenciana de Psicologia · doi:10.7203/anuari.psicologia.16.1.189 · Cited by 2 · see citing works
The Influence of Neonatal Oxytocin on Neuronal Apoptosis in Female Prairie Voles
Nguyen, K. N. (2009) · OhioLink ETD Center (Ohio Library and Information Network) · Cited by 1 · see citing works
Developmental, but not activational, roles for estradiol and its receptor in paternal and sexual behaviour of Phodopus campbelli males
Timonin, M. E. (2008) · QSpace (Queen's University Library) · Cited by 1 · see citing works
Comparative analysis of gonadal hormone receptor expression in the house mouse, meadow vole, and prairie vole brainPreprint
Denney, K. A., Wu, M. V., Sun, S. D., Moon, S., & Tollkühn, J. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.12.540606 · Cited by 1 · see citing works
Morphogenetic effects of neonatal androgenization on neuron dendroarchitectonics in amygdala dorsomedial nucleus
Ахмадеев, А. В. (2006) · Russian Journal of Developmental Biology · doi:10.1134/s1062360406050067
Estrogen Receptor Beta mRNA: Localization in the Prairie Vole (Microtus ochrogaster)
Koenig, A. S. (2013) · OhioLink ETD Center (Ohio Library and Information Network)
BASES HORMONALS DE LA CONDUCTA PROSOCIAL: UNA REVISIÓ DE LA LITERATURA BASES HORMONALES DE LA CONDUCTA PROSOCIAL: UNA REVISIÓN DE LA LITERATURA HORMONAL BASES OF PROSOCIAL BEHAVIOR: A REVIEW OF THE LITERATURE
Suay, F., Vilar, M. M., & Susana, L. T. (2015)
Bases hormonals de la conducta prosocial: una revisió de la literatura
Lerma, F. S., Manuel, M. V., & Susana, L. T. (2016) · Anuari de Psicologia de la Societat Valenciana de Psicologia · doi:10.7203/anuari.psicologia.15.2.189
Clomiphene citrate treatment during perinatal development alters adult partner preference, mating behaviour and androgen receptor and vasopressin in the male mandarin vole Microtus mandarinus
He, F., Yan, B., Tian, Z., Wang, B., Cheng, X.-X., Wang, Z., & Yu, B. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15793
Effects of prenatal cocaine exposure on estrous cycle, and behavior and expression of estrogen receptor alpha and oxytocin during estrus and diestrus in mice offspring
Zheng, Y., Cheng, G., Lin, X., & Wang, J. (2024) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000791
Genetic variation of cytochrome b in the prairie vole (Microtus ochrogaster)
Robinson, J. J., Solomon, N. G., Berg, D. J., & Keane, B. (2025) · Mammalia · doi:10.1515/mammalia-2024-0105
Sex-specific disruption of estrogen receptor alpha (ERα) density in the social brain neural network by Firemaster 550
Cao, J., Gillera, S. E. A., Marinello, W. P., & Patisaul, H. B. (2026) · Journal of the Endocrine Society · doi:10.1210/jendso/bvag050
Bidirectional control of aggression by estrogen receptor α in key neural circuits: A dynamic balance underlying behavioral plasticity
Chen, Y., Mao, Z., Lan, S., Cai, S., Ma, Z., Zhu, C., Li, F., Xie, Y., Qiu, Y., & Pan, Y. (2026) · Hormones and Behavior · doi:10.1016/j.yhbeh.2026.105951

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
Self-citation
Estrogen Receptor-α in the Bed Nucleus of the Stria Terminalis Regulates Social Affiliation in Male Prairie Voles (Microtus ochrogaster)
Lei, K., Cushing, B. S., Musatov, S., Ogawa, S., & Kramer, K. M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008931 · Cited by 67 · see citing works
Self-citation
Estrogen receptors in the medial amygdala inhibit the expression of male prosocial behavior
Cushing, B. S., Perry, A., Musatov, S., Ogawa, S., & Papademetriou, E. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1928-08.2008 · Cited by 95 · see citing works
Self-citation
Estrogen Receptor-a in the Bed Nucleus of the Stria Terminalis Regulates Social Affiliation in Male Prairie
Ochrogaster, V. (., Lei, K., Cushing, B. S., Musatov, S. A., Ogawa, S., & Kramer, K. M. (2013)
Self-citation
Inhibiting ERα expression in the medial amygdala increases prosocial behavior in male meadow voles (Microtus pennsylvanicus)
Stetzik, L. A., Ganshevsky, D., Lende, M. N., Roache, L. E., Musatov, S. A., & Cushing, B. S. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.05.035 · Cited by 18 · see citing works
Self-citation

Authors: Cushing, B. S., Razzoli, M., Murphy, A. Z., Epperson, P. M., Le, W.-W., & Hoffman, G. E.
Affiliations: University of Illinois Chicago (US)
University of North Carolina at Chapel Hill (US)
Georgia State University (US)
University of Maryland, Baltimore (US)
Corresponding author: Cushing, Bruce S
ORCID: Cushing, Bruce S
Razzoli, Maria
Murphy, Anne Z
Venue: Brain Research
Publisher: Elsevier BV
Published: 2004-08
Volume: 1016
Issue: 2
Pages: 247-254
ISSN: 0006-8993 (ISSN-L)
DOI: 10.1016/j.brainres.2004.05.010
OpenAlex: W2045267898
Cited by: 77
References: 63
Citations by year: 2026: 3 · 2025: 2 · 2024: 1 · 2023: 2 · 2022: 1 · 2021: 5 · 2020: 2 · 2019: 3 · 2018: 4 · 2017: 2 · 2016: 5 · 2015: 4 · 2014: 4 · 2013: 7 · 2012: 4
FWCI: 4.64
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Brain Research (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5k05mh001050-03)
Centers for Disease Control and Prevention (ND 11111)
National Institute of Mental Health (MH 01992, MH01050, K01MH001992)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01HD038490, HD38490)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords: estrogen receptor alpha, Microtus ochrogaster, androgen receptor, testosterone, aromatization, medial amygdala, bed nucleus of the stria terminalis, medial preoptic area, ventromedial hypothalamus, hypothalamus, intraspecific variation, prosocial behavior, sexual activity, population differences
MeSH terms: Animals, Behavior, Animal, Brain, Castration, Cell Count, Arvicolinae, Dose-Response Relationship, Drug, Female, Illinois, Immunohistochemistry, Kansas, Male, Receptors, Androgen, Receptors, Estrogen, Sexual Behavior, Animal, Sex Characteristics, Social Behavior, Species Specificity, Testosterone Propionate, Estrogen Receptor alpha

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

Intraspecific variation in estrogen receptor alpha and the expression of male sociosexual behavior in two populations of prairie voles

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks