Estrogen receptor β and oxytocin interact to modulate anxiety-like behavior and neuroendocrine stress reactivity in adult male and female rats

Kudwa, Andrea E.; McGivern, Robert F.; Handa, Robert J.

doi:10.1016/j.physbeh.2014.03.004

Cited by 73Stress Responses and CortisolNeuroendocrine regulation and behaviorEstrogen and related hormone effects

Estrogen receptor β and oxytocin interact to modulate anxiety-like behavior and neuroendocrine stress reactivity in adult male and female rats

Open access

Kudwa, Andrea E., McGivern, Robert F., Handa, Robert J.·2014·Physiology & Behavior

DOI 10.1016/j.physbeh.2014.03.004PMC PMC5802969

Open this paper in CoChat — free account

Abstract

The hypothalamic-pituitary-adrenal (HPA) axis is activated in response to stressors and is controlled by neurons residing in the paraventricular nucleus of the hypothalamus (PVN). Although gonadal steroid hormones can influence HPA reactivity to stressors, the exact mechanism of action is not fully understood. It is known, however, that estrogen receptor β (ERβ) inhibits HPA reactivity and decreases anxiety-like behavior in rodents. Since ERβ is co-expressed with oxytocin (OT) in neurons of the PVN, an ERβ-selective agonist was utilized to test the whether ERβ decreases stress-induced HPA reactivity and anxiety-like behaviors via an OTergic pathway. Adult gonadectomized male and female rats were administered diarylpropionitrile, or vehicle, peripherally for 5days. When tested for anxiety-like behavior on the elevated plus maze (EPM), diarylpropionitrile-treated males and females significantly increased time on the open arm of the EPM compared to vehicle controls indicating that ERβ reduces anxiety-like behaviors. One week after behavioral evaluation, rats were subjected to a 20minute restraint stress. Treatment with diarylpropionitrile reduced CORT and ACTH responses in both males and females. Subsequently, another group of animals was implanted with cannulae directed at the lateral ventricle. One week later, rats underwent the same protocol as above but with the additional treatment of intracerebroventricular infusion with an OT antagonist (des Gly-NH2 d(CH2)5 [Tyr(Me)(2), Thr(4)] OVT) or VEH, 20min prior to behavioral evaluation. OT antagonist treatment blocked the effects of diarylpropionitrile on the display of anxiety-like behaviors and plasma CORT levels. These data indicate that ERβ and OT interact to modulate the HPA reactivity and the display of anxiety-like behaviors.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1016/j.physbeh.2014.03.004

Cites

65 of 65 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Gonadal steroids can act in a synergistic manner to decrease HPA axis gain and anxiety-related behaviors.
“Gonadal steroids can act in a synergistic manner to decrease HPA axis gain and anxiety-related behaviors (Kudwa, McGivern, & Handa, 2014; McCarthy, McDonald, Brooks, & Goldman, 1996)”
From Hypothalamic–pituitary–adrenal and hypothalamic–pituitary–gonadal axes: sex differences in regulation of stress responsivity (2017) · cites this paper as Kudwa, McGivern, & Handa, 2014
The Abstract (page unavailable) reports that activating estrogen receptor β reduced anxiety-like behavior and stress-induced HPA hormone responses in gonadectomized rats. The Introduction (page unavailable) describes an interaction with an oxytocin pathway, but oxytocin is not a gonadal steroid; the paper does not establish that gonadal steroids act synergistically to produce these effects. (LLM, conf=0.86)
Experimental — accuracy not yet measured
A subpopulation of parvocellular PVN OT and AVP neurons, along with ERβ and coordinating input from the BnST, is thought to be involved in the stress response, supporting the possibility that EDCs may influence the hypothalamic-pituitary-adrenal axis.
“Finally, a subpopulation of parvocellular PVN OT and AVP neurons, along with ERβ and coordinating input from the BnST, is thought to be involved in the stress response (135, 139, 140) supporting the possibility that EDCs may influence the hypothalamic–pituitary–adrenal axis.”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [135]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
ERβ in the PVN and associated structures, including the BnST, plays a fundamental role in mediating motivational and anxiety-related behaviors.
“Although the functional role of limbic ERβ remains ambiguous, ERβ in the PVN and associated structures, including the BnST, plays a fundamental role in mediating motivational and anxiety-related behaviors (134–136).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [135]
The Introduction and Discussion (page numbers unavailable) support a role for ERβ in anxiety-like behavior and identify ERβ in the PVN. But the Discussion says the site of ERβ’s action on anxiety is unknown and names the BnST only as a possible site. The copy does not establish a fundamental role for PVN and BnST ERβ in motivational behavior. (LLM, conf=0.88)
Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The oxytocin receptor system: structure, function, and regulation
Gimpl, G., & Fahrenholz, F. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.629 · Cited by 3,089 · see citing works
Evoked axonal oxytocin release in the central amygdala attenuates fear response
Knobloch, H. S., Charlet, A., Hoffmann, L. C., Eliava, M., Khrulev, S., Cetin, A. H., Osten, P., Schwarz, M. K., Seeburg, P. H., Stoop, R., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.030 · Cited by 1,049 · see citing works
Estrogen Receptor-β Potency-Selective Ligands: Structure−Activity Relationship Studies of Diarylpropionitriles and Their Acetylene and Polar Analogues
Meyers, M. J., Sun, J., Carlson, K. E., Marriner, G. A., Katzenellenbogen, B. S., & Katzenellenbogen, J. A. (2001) · Journal of Medicinal Chemistry · doi:10.1021/jm010254a · Cited by 678 · see citing works
Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat
VIAU, V., & MEANEY, M. J. (1991) · Endocrinology · doi:10.1210/endo-129-5-2503 · Cited by 666 · see citing works
Evidence That Oxytocin Exerts Anxiolytic Effects via Oxytocin Receptor Expressed in Serotonergic Neurons in Mice
Yoshida, M., Takayanagi, Y., Inoue, K., Kimura, T., Young, L. J., Onaka, T., & Nishimori, K. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5593-08.2009 · Cited by 608 · see citing works
Sex difference in resting pituitary-adrenal function in the rat
Critchlow, V., Liebelt, R. A., Bar-Sela, M., Mountcastle, W., & Lipscomb, H. S. (1963) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1963.205.5.807 · Cited by 499 · see citing works
Chronic estrogen-induced alterations in adrenocorticotropin and corticosterone secretion, and glucocorticoid receptor-mediated functions in female rats
Burgess, L. H., & Handa, R. J. (1992) · Endocrinology · doi:10.1210/endo.131.3.1324155 · Cited by 445 · see citing works
Self-citation
Novel Actions of Estrogen Receptor-β on Anxiety-Related Behaviors
Lund, T. D., Rovis, T., Chung, W. C. J., & Handa, R. J. (2005) · Endocrinology · doi:10.1210/en.2004-1158 · Cited by 436 · see citing works
Self-citation
Brain oxytocin: differential inhibition of neuroendocrine stress responses and anxiety-related behaviour in virgin, pregnant and lactating rats
Neumann, I. D., Torner, L., & Wigger, A. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00433-9 · Cited by 402 · see citing works
An estrogen-dependent four-gene micronet regulating social recognition: A study with oxytocin and estrogen receptor-α and -β knockout mice
Choleris, E., Gustafsson, J.-Å., Korach, K. S., Muglia, L. J., Pfaff, D. W., & Ogawa, S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0631699100 · Cited by 386 · see citing works
Anxiety and stress responses in female oxytocin deficient mice
Amico, J. A., Mantella, R. C., Vollmer, R. R., & Li, X. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.0953-8194.2004.01161.x · Cited by 327 · see citing works
Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and foot shock stressors
Handa, R. J., Nunley, K. M., Lorens, S. A., Louie, J. P., McGivern, R. F., & Bollnow, M. R. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90018-3 · Cited by 325 · see citing works
Self-citation
Brain oxytocin inhibits the (re)activity of the hypothalamo–pituitary–adrenal axis in male rats: involvement of hypothalamic and limbic brain regions
Neumann, I. D., Krömer, S. A., Toschi, N., & Ebner, K. (2000) · Regulatory Peptides · doi:10.1016/s0167-0115(00)00197-x · Cited by 285 · see citing works
Increased anxiety and synaptic plasticity in estrogen receptor β-deficient mice
Krężel, W., Dupont, S., Krust, A., Chambon, P., & Chapman, P. F. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.221451898 · Cited by 279 · see citing works
Estrogen impairs glucocorticoid dependent negative feedback on the hypothalamic–pituitary–adrenal axis via estrogen receptor alpha within the hypothalamus
Weiser, M. J., & Handa, R. J. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2008.12.058 · Cited by 250 · see citing works
Self-citation
Stress Integration after Acute and Chronic Predator Stress: Differential Activation of Central Stress Circuitry and Sensitization of the Hypothalamo-Pituitary-Adrenocortical Axis
Figueiredo, H. F., Bodie, B., Tauchi, M., Dolgas, C. M., & Herman, J. P. (2003) · Endocrinology · doi:10.1210/en.2003-0713 · Cited by 245 · see citing works
The Androgen 5α-Dihydrotestosterone and Its Metabolite 5α-Androstan-3β, 17β-Diol Inhibit the Hypothalamo–Pituitary–Adrenal Response to Stress by Acting through Estrogen Receptor β-Expressing Neurons in the Hypothalamus
Lund, T. D., Hinds, L. R., & Handa, R. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3777-05.2006 · Cited by 236 · see citing works
Self-citation
Gonadal Steroid Replacement Reverses Gonadectomy‐Induced Changes in the Corticosterone Pulse Profile and Stress‐Induced Hypothalamic‐Pituitary‐Adrenal Axis Activity of Male and Female Rats
Seale, J. V., Wood, S. A., Atkinson, H. C., Harbuz, M. S., & Lightman, S. L. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2004.01258.x · Cited by 235 · see citing works
ERβ-Selective Estrogen Receptor Modulators Produce Antianxiety Behavior when Administered Systemically to Ovariectomized Rats
Walf, A. A., & Frye, C. A. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300713 · Cited by 229 · see citing works
Lack of functional estrogen receptor β influences anxiety behavior and serotonin content in female mice
Imwalle, D. B., Gustafsson, J.-Α., & Rissman, E. F. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.11.002 · Cited by 225 · see citing works
Gender differences in corticotropin and corticosterone secretion and corticotropin-releasing factor mRNA expression in the paraventricular nucleus of the hypothalamus and the central nucleus of the amygdala in response to footshock stress or psychological stress in rats
Iwasaki-Sekino, A., Mano‐Otagiri, A., Ohata, H., Yamauchi, N., & Shibasaki, T. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.09.003 · Cited by 222 · see citing works
Female oxytocin-deficient mice display enhanced anxiety-related behavior
Mantella, R. C., Vollmer, R. R., Li, X., & Amico, J. A. (2003) · Endocrinology · doi:10.1210/en.2002-0197 · Cited by 200 · see citing works
Estrogen receptor beta regulates the expression of tryptophan-hydroxylase 2 mRNA within serotonergic neurons of the rat dorsal raphe nuclei
Donner, N. C., & Handa, R. J. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.06.046 · Cited by 197 · see citing works
Self-citation
Antidepressant effects of ERβ-selective estrogen receptor modulators in the forced swim test
Walf, A. A., Rhodes, M. E., & Frye, C. A. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2004.03.023 · Cited by 179 · see citing works
Effects of Estrogen Antagonists and Agonists on the ACTH Response to Restraint Stress in Female Rats
Young, E. A. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00301-3 · Cited by 171 · see citing works
Estrogen receptor-β regulates transcript levels for oxytocin and arginine vasopressin in the hypothalamic paraventricular nucleus of male mice
Nomura, M., McKenna, E., Korach, K. S., Pfaff, D. W., & Ogawa, S. (2002) · Molecular Brain Research · doi:10.1016/s0169-328x(02)00525-9 · Cited by 167 · see citing works
Stimuli and consequences of dendritic release of oxytocin within the brain
Neumann, I. D. (2007) · Biochemical Society Transactions · doi:10.1042/bst0351252 · Cited by 161 · see citing works
Oxytocin, But Not Oxytocin Receptor, is Regulated by Oestrogen Receptor β in the Female Mouse Hypothalamus
Patisaul, H. B., Scordalakes, E. M., Young, L. J., & Rissman, E. F. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01061.x · Cited by 160 · see citing works
Estrogen modulation of oxytocin and its relation to behavior.
McCarthy, M. M. (1995) · PubMed · Cited by 157 · see citing works
Effects of stress and glucocorticoids on CNS oxytocin receptor binding
Liberzon, I., & Young, E. A. (1997) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(97)00045-0 · Cited by 147 · see citing works
New roles for estrogen receptor β in behavior and neuroendocrinology☆
Bodo, C., & Rissman, E. F. (2006) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2006.02.004 · Cited by 141 · see citing works
Effects of estrogen on oxytocin receptor messenger ribonucleic acid expression in the uterus, pituitary, and forebrain of the female rat
Quiñones-Jenab, V., Jenab, S., Ogawa, S., Adan, R. A. M., Burbach, P. H., & Pfaff, D. W. (2008) · Neuroendocrinology · doi:10.1159/000127160 · Cited by 134 · see citing works
Sex differences and phase of light cycle modify chronic stress effects on anxiety and depressive-like behavior
Huynh, T. N., Krigbaum, A. M., Hanna, J. J., & Conrad, C. D. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.03.038 · Cited by 129 · see citing works
Estrogen Receptor-β Agonist Diarylpropionitrile: Biological Activities of R- and S-Enantiomers on Behavior and Hormonal Response to Stress
Weiser, M. J., Wu, T. J., & Handa, R. J. (2009) · Endocrinology · doi:10.1210/en.2008-1355 · Cited by 124 · see citing works
Self-citation
Estrogen receptor‐β in oxytocin and vasopressin neurons of the rat and human hypothalamus: Immunocytochemical and in situ hybridization studies
Hrabovszky, E., Kalló, I., Steinhauser, A., Merchenthaler, I., Coen, C. W., Petersen, S. L., & Liposits, Z. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.20127 · Cited by 118 · see citing works
Relationships among estrogen receptor, oxytocin and vasopressin gene expression and social interaction in male mice
Murakami, G., Hunter, R. G., Fontaine, C., Ribeiro, A., & Pfaff, D. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07761.x · Cited by 99 · see citing works
Anxiolytic Effects and Neuroanatomical Targets of Estrogen Receptor-β (ERβ) Activation by a Selective ERβ Agonist in Female Mice
Oyola, M. G., Portillo, W., Reyna, A., Foradori, C. D., Kudwa, A., Hinds, L., Handa, R. J., & Mani, S. K. (2012) · Endocrinology · doi:10.1210/en.2011-1674 · Cited by 99 · see citing works
Self-citation
Estrogen receptor‐β, but not estrogen receptor‐α, is expressed in prolactin neurons of the female rat paraventricular and supraoptic nuclei: Comparison with other neuropeptides
Suzuki, S., & Handa, R. J. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20457 · Cited by 97 · see citing works
Self-citation
Testosterone-dependent variations in plasma and intrapituitary corticosteroid binding globulin and stress hypothalamic-pituitary-adrenal activity in the male rat
Viau, V., & Meaney, M. (2004) · Journal of Endocrinology · doi:10.1677/joe.0.1810223 · Cited by 93 · see citing works
Molecular Basis for the Subtype Discrimination of the Estrogen Receptor-β-Selective Ligand, Diarylpropionitrile
Sun, J., Baudry, J. Y., Katzenellenbogen, J. A., & Katzenellenbogen, B. S. (2003) · Molecular Endocrinology · doi:10.1210/me.2002-0341 · Cited by 91 · see citing works
WAY-200070, a selective agonist of estrogen receptor beta as a potential novel anxiolytic/antidepressant agent
Hughes, Z. A., Liu, F., Platt, B. J., Dwyer, J. M., Pulicicchio, C. M., Zhang, G., Schechter, L. E., Rosenzweig-Lipson, S., & Day, M. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.03.004 · Cited by 88 · cited 1× · see citing works
“Moreover, activation of ERβ by a variety of ERβ agonists attenuates stress-induced hypothalamic-pituitary-adrenal (HPA) activity and decreases the display of anxiety-like behaviors in rodents [31, 32].”
Background
Ovariectomy/Orchidectomy in Rodents
Idris, A. I. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-415-5_34 · Cited by 88 · see citing works
Central nervous system actions of oxytocin and modulation of behavior in humans
McCarthy, M. M., & Altemus, M. M. (1997) · Molecular Medicine Today · doi:10.1016/s1357-4310(97)01058-7 · Cited by 88 · see citing works
Distribution of estrogen receptor beta containing cells in the brains of bacterial artificial chromosome transgenic mice
Milner, T. A., Thompson, L. I., Wang, G., Kievits, J. A., Martin, E. M., Zhou, P., McEwen, B. S., Pfaff, D. W., & Waters, E. M. (2010) · Brain Research · doi:10.1016/j.brainres.2010.06.038 · Cited by 82 · see citing works
Dihydrotestosterone may inhibit hypothalamo–pituitary–adrenal activity by acting through estrogen receptor in the male mouse
Lund, T. D., Munson, D. J., Haldy, M. E., & Handa, R. J. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.04.035 · Cited by 81 · see citing works
Self-citation
Oxytocin binding sites in rat limbic and hypothalamic structures: Site-specific modulation by adrenal and gonadal steroids
Patchev, V. K., Schlosser, S. F., Hassan, A. H., & Almeida, O. F. X. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90003-x · Cited by 77 · see citing works
Oxytocin-stimulated release of adrenocorticotropin from the rat pituitary is mediated by arginine vasopressin receptors of the V1b type
Schlosser, S. F., Almeida, O. F., Patchev, V. K., Yassouridis, A., & Elands, J. (1994) · Endocrinology · doi:10.1210/endo.135.5.7956927 · Cited by 75 · see citing works
Enhanced corticosterone concentrations and attenuated Fos expression in the medial amygdala of female oxytocin knockout mice exposed to psychogenic stress
Mantella, R. C., Vollmer, R. R., Rinaman, L., Li, X., & Amico, J. A. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00387.2004 · Cited by 71 · see citing works
Oxytocin in the medial preoptic area facilitates male sexual behavior in the rat
Gil, M., Bhatt, R., Picotte, K. B., & Hull, E. M. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.12.012 · Cited by 70 · cited 1× · see citing works
“Although OVT has been previously reported to not influence locomotor activity when delivered to the medial preoptic area [59], it is still possible that there is an overall effect of OVT in these studies that could counter the effects of R-DPN.”
Background
Enhanced Up‐Regulation of Corticotropin‐Releasing Hormone Gene Expression in Response to Restraint Stress in the Hypothalamic Paraventricular Nucleus of Oxytocin Gene‐Deficient Male Mice
Nomura, M., Saito, J., Ueta, Y., Muglia, L. J., Pfaff, D. W., & Ogawa, S. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01095.x · Cited by 69 · see citing works
Sex and age differences in the impact of the forced swimming test on the levels of steroid hormones
Martı́nez-Mota, L., Ulloa, R. E., Herrera‐Perez, J. J., Chavira, R., & Fernández‐Guasti, A. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.05.027 · Cited by 63 · see citing works
Androgen receptor expressing neurons that project to the paraventricular nucleus of the hypothalamus in the male rat
Williamson, M., & Viau, V. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21411 · Cited by 54 · see citing works
Oxytocin receptor binding in the hypothalamus during gestation in rats
Bealer, S. L., Lipschitz, D. L., Ramoz, G., & Crowley, W. R. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00766.2005 · Cited by 54 · see citing works
Modulation of responses to stress by estradiol benzoate and selective estrogen receptor agonists
Serova, L. I., Harris, H. A., Maharjan, S., & Sabban, E. L. (2010) · Journal of Endocrinology · doi:10.1677/joe-10-0029 · Cited by 54 · see citing works
Stress‐induced pressor and corticosterone responses in oxytocin‐deficient mice
Bernátová, I., Rigatto, K., Key, M. P., & Morris, M. (2004) · Experimental Physiology · doi:10.1113/expphysiol.2004.027714 · Cited by 51 · see citing works
Behavioral effects of intracerebroventricularly administered neurohypophyseal hormone analogs in mice
Meisenberg, G., & Simmons, W. H. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90242-8 · Cited by 51 · see citing works
Diarylpropionitrile (DPN) Enantiomers: Synthesis and Evaluation of Estrogen Receptor β-Selective Ligands
Carroll, V. M., Jeyakumar, M., Carlson, K. E., & Katzenellenbogen, J. A. (2011) · Journal of Medicinal Chemistry · doi:10.1021/jm201436k · 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
The Androgen Metabolite, 5α-Androstane-3β,17β-Diol (3β-Diol), Activates the Oxytocin Promoter Through an Estrogen Receptor-β Pathway
Hiroi, R., Lacagnina, A. F., Hinds, L. R., Carbone, D. G., Uht, R. M., & Handa, R. J. (2013) · Endocrinology · doi:10.1210/en.2012-2253 · Cited by 48 · see citing works
Self-citation
Centrally administered oxytocin elicits exaggerated grooming in oxytocin null mice
Amico, J. A., Vollmer, R. R., Karam, J. R., Lee, P. R., Li, X., Koenig, J. I., & McCarthy, M. M. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2004.04.006 · Cited by 46 · see citing works
The ERβ Ligand 5α-androstane, 3β,17β-diol (3β-diol) Regulates Hypothalamic Oxytocin (Oxt) Gene Expression
Sharma, D., Handa, R. J., & Uht, R. M. (2012) · Endocrinology · doi:10.1210/en.2011-1002 · Cited by 45 · see citing works
Self-citation
The Role of Oestradiol in Sexually Dimorphic Hypothalamic‐Pituitary‐Adrena Axis Responses to Intracerebroventricular Ethanol Administration in the Rat
Larkin, J. W., Binks, S. L., Li, Y., & Selvage, D. J. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01934.x · Cited by 40 · see citing works
Systemic administration of diarylpropionitrile (DPN) or phytoestrogens does not affect anxiety-related behaviors in gonadally intact male rats
Patisaul, H. B., Burke, K. T., Hinkle, R. E., Adewale, H. B., & Shea, D. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.11.004 · Cited by 38 · see citing works
Rat estrous cycle influences the sexual diergism of HPA axis stimulation by nicotine
Rhodes, M. E., Kennell, J. S., Belz, E. E., Czambel, R. K., & Rubín, R. T. (2004) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2004.06.011 · Cited by 38 · see citing works
Effects of Estrogen on Stress‐induced Activation of Peptide Neurons in PVN of Ovariectomized Rats
Hara, Y., Kohno, T., Takamata, A., Ueyama, T., & Morimoto, K. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1410.042 · Cited by 1 · see citing works

Flagged first, then by citations

Research works printed but not linked: 2

[9]Handa RJ Nunley KM Lorens SA Louie JP McGivern RF Bollnow MR 1994b Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and foot shock stressors Physiol Behav 55 117 124 8140154
[53]Laflamme N Nappi RE Drolet G Labrie C Rivest S 1998 Expression and neuropeptidergic characterization of estrogen receptors (ERalpha and ERbeta) throughout the rat brain: anatomical evidence of distinct roles of each subtype J Neurobiol 36 357 78 9733072

Sorted by citations

Hypothalamic–pituitary–adrenal and hypothalamic–pituitary–gonadal axes: sex differences in regulation of stress responsivity
Oyola, M. G., & Handa, R. J. (2017) · Stress · doi:10.1080/10253890.2017.1369523 · Cited by 710 · see citing works
Self-citation
Is Dysregulation of the HPA-Axis a Core Pathophysiology Mediating Co-Morbid Depression in Neurodegenerative Diseases?
Du, X., & Pang, T. Y. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00032 · Cited by 211 · see citing works
Estrogen Receptors Modulation of Anxiety-Like Behavior
Borrow, A. P., & Handa, R. J. (2017) · Vitamins and Hormones · doi:10.1016/bs.vh.2016.08.004 · Cited by 146 · see citing works
Self-citation
Oxytocin and Estrogen Receptor β in the Brain: An Overview
Acevedo-Rodriguez, A., Mani, S. K., & Handa, R. J. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00160 · Cited by 124 · see citing works
Self-citation
The Anxiolytic and Antidepressant-like Effects of Testosterone and Estrogen in Gonadectomized Male Rats
Carrier, N., Saland, S. K., Duclot, F., He, H., Mercer, R. S., & Kabbaj, M. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.12.024 · Cited by 116 · see citing works
Roles for androgens in mediating the sex differences of neuroendocrine and behavioral stress responses
Zuloaga, D. G., Heck, A., Guzman, R. M. D., & Handa, R. J. (2020) · Biology of Sex Differences · doi:10.1186/s13293-020-00319-2 · Cited by 96 · see citing works
Self-citation
A novel model for neuroendocrine toxicology: neurobehavioral effects of BPA exposure in a prosocial species, the prairie vole (Microtus ochrogaster)
Sullivan, A. W., Beach, E. C., Stetzik, L. A., Perry, A., D'Addezio, A. S., Cushing, B. S., & Patisaul, H. B. (2014) · Endocrinology · doi:10.1210/en.2014-1379 · Cited by 79 · see citing works
The potential role of the novel hypothalamic neuropeptides nesfatin-1, phoenixin, spexin and kisspeptin in the pathogenesis of anxiety and anorexia nervosa
Pałasz, A., Janas-Kozik, M. H., Borrow, A. P., Arias-Carrión, Ó., & Worthington, J. J. (2017) · Neurochemistry International · doi:10.1016/j.neuint.2017.12.006 · Cited by 58 · see citing works
The impact of oxytocin on stress: the role of sex
Love, T. M. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.06.018 · Cited by 56 · see citing works
The functions of estrogen receptor beta in the female brain: A systematic review
Vargas, K. G., Milić, J., Začiragić, A., Wen, K., Jaspers, L., Nano, J., Dhana, K., Bramer, W. M., Kraja, B., van Beeck, E., et al. (2016) · Maturitas · doi:10.1016/j.maturitas.2016.05.014 · Cited by 58 · see citing works
Endocrine Disruption of Vasopressin Systems and Related Behaviors
Patisaul, H. B. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00134 · Cited by 54 · see citing works
Distribution and chemical composition of estrogen receptor β neurons in the paraventricular nucleus of the female and male mouse hypothalamus
Oyola, M. G., Thompson, M. K., Handa, A. Z., & Handa, R. J. (2017) · Journal of Comparative Neurology · doi:10.1002/cne.24295 · Cited by 53 · see citing works
Self-citation
Elevation of natural killer cell activity and alleviation of mental stress by the consumption of yogurt containing Lactobacillus gasseri SBT2055 and Bifidobacterium longum SBT2928 in a double-blind, placebo-controlled clinical trial
Nishihira, J., Kagami‐Katsuyama, H., Tanaka, A., Nishimura, M., Kobayashi, T., & Kawasaki, Y. (2014) · Journal of Functional Foods · doi:10.1016/j.jff.2014.09.002 · Cited by 53 · see citing works
The interplay of oxytocin and sex hormones
Quintana, D. S., Glaser, B. D., Kang, H., Kildal, E. S.-M., Audunsdottir, K., Sartorius, A. M., & Barth, C. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105765 · Cited by 54 · see citing works
Prolonged Social Isolation, Started Early in Life, Impairs Cognitive Abilities in Rats Depending on Sex
Krupina, N. A., Shirenova, S. D., & Khlebnikova, N. N. (2020) · Brain Sciences · doi:10.3390/brainsci10110799 · Cited by 47 · see citing works
Effects of neural estrogen receptor beta deletion on social and mood-related behaviors and underlying mechanisms in male mice
Dombret, C., Naulé, L., Trouillet, A., Parmentier, C., Hardin‐Pouzet, H., & Mhaouty‐Kodja, S. (2020) · Scientific Reports · doi:10.1038/s41598-020-63427-4 · Cited by 40 · see citing works
Histone Deacetylase Inhibition Induces Long-Lasting Changes in Maternal Behavior and Gene Expression in Female Mice
Stolzenberg, D. S., Stevens, J. S., & Rissman, E. F. (2014) · Endocrinology · doi:10.1210/en.2013-1946 · Cited by 40 · see citing works
Sex-specific Effects of Endocrine-disrupting Chemicals on Brain Monoamines and Cognitive Behavior
Hilz, E. N., & Gore, A. C. (2022) · Endocrinology · doi:10.1210/endocr/bqac128 · Cited by 38 · see citing works
Role of estrogen in treatment of female depression
Sun, Q., Li, G., Zhao, F., Dong, M., Xie, W., Liu, Q., Yang, W., & Cui, R. (2024) · Aging · doi:10.18632/aging.205507 · Cited by 37 · see citing works
Sex Differences in Acute Neuroendocrine Responses to Stressors in Rodents and HumansPreprint
Handa, R. J., Sheng, J. A., Castellanos, E., Templeton, H., & McGivern, R. F. (2022) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a039081 · Cited by 38 · see citing works
Self-citation
Neurochemical Characterization of Neurons Expressing Estrogen Receptor β in the Hypothalamic Nuclei of Rats Using in Situ Hybridization and Immunofluorescence
Kanaya, M., Higo, S., & Ozawa, H. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms21010115 · Cited by 36 · see citing works
Daidzein Alleviates Hypothalamic-Pituitary-Adrenal Axis Hyperactivity, Ameliorates Depression-Like Behavior, and Partly Rectifies Circulating Cytokine Imbalance in Two Rodent Models of Depression
Chen, L., Wang, X., Zhang, Y., Zhong, H., Wang, C., Gao, P., & Li, B. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.671864 · Cited by 35 · see citing works
Oxytocin and Steroid Actions
Jirikowski, G. F., Ochs, S. D., & Caldwell, J. D. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_9 · Cited by 32 · see citing works
The hypothalamic paraventricular nucleus as a central hub for the estrogenic modulation of neuroendocrine function and behavior
Grassi, D., Marraudino, M., García‐Segura, L. M., & Panzica, G. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2021.100974 · Cited by 30 · see citing works
25 years of ERβ: a personal journey
Warner, M. N., Fan, X., Ström, A., Wu, W., & Gustafsson, J.-Α. (2021) · Journal of Molecular Endocrinology · doi:10.1530/jme-21-0121 · Cited by 30 · see citing works
Androgens and Their Role in Regulating Sex Differences in the Hypothalamic/Pituitary/Adrenal Axis Stress Response and Stress-Related Behaviors
Sheng, J. A., Tan, S. M. L., Hale, T. M., & Handa, R. J. (2021) · Androgens Clinical Research and Therapeutics · doi:10.1089/andro.2021.0021 · Cited by 30 · see citing works
Self-citation
Palatable food reduces anxiety-like behaviors and HPA axis responses to stress in female rats in an estrous-cycle specific manner
Egan, A. E., Seemiller, L. R., Packard, A. E. B., Solomon, M. B., & Ulrich‐Lai, Y. M. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.07.005 · Cited by 28 · see citing works
Detection and Characterization of Estrogen Receptor Beta Expression in the Brain with Newly Developed Transgenic Mice
Sagoshi, S., Maejima, S., Morishita, M., Takenawa, S., Otubo, A., Takanami, K., Sakamoto, T., Sakamoto, H., Tsukahara, S., & Ogawa, S. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.04.047 · Cited by 28 · see citing works
Therapeutic uses of oxytocin in stress-related neuropsychiatric disorders
Zhang, S., Zhang, Y., Shi, D., & Wang, Z. (2023) · Cell & Bioscience · doi:10.1186/s13578-023-01173-6 · Cited by 28 · see citing works
The behavioral and molecular evaluation of effects of social instability stress as a model of stress-related disorders in adult female rats
Nowacka-Chmielewska, M. M., Liśkiewicz, D., Barski, J. J., Obuchowicz, E., & Małecki, A. (2017) · Stress · doi:10.1080/10253890.2017.1376185 · Cited by 26 · see citing works
Peripubertal Stress With Social Support Promotes Resilience in the Face of Aging
Morrison, K. E., Narasimhan, S., Fein, E. C., & Bale, T. L. (2016) · Endocrinology · doi:10.1210/en.2015-1876 · Cited by 22 · see citing works
Treatment with oestrogen‐receptor agonists or oxytocin in conjunction with exercise protects against myocardial infarction in ovariectomized rats
Bulut, E. C., Abueid, L., Ercan, F., Süleymanoğlu, S., Ağırbaşlı, M. A., & Yeğen, B. Ç. (2016) · Experimental Physiology · doi:10.1113/ep085708 · Cited by 20 · see citing works
Behavioral responses to emotional challenges in female rats living in a seminatural environment: The role of estrogen receptors
Moëne, O. L., & Ågmo, A. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.10.013 · Cited by 20 · see citing works
Maternal Diabetes-Induced Suppression of Oxytocin Receptor Contributes to Social Deficits in Offspring
Liu, J., Liang, Y., Jiang, X., Xu, J., Sun, Y., Wang, Z., Lin, L., Niu, Y., Song, S., Zhang, H., et al. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.634781 · Cited by 20 · 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
Effects of circulating estradiol on physiological, behavioural, and subjective correlates of anxiety: A double-blind, randomized, placebo-controlled trial
Nouri, S., Biedermann, S. V., Joue, G., Auer, M. K., Sommer, T., & Fuß, J. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105682 · Cited by 17 · see citing works
The identification of cianidanol as a selective estrogen receptor beta agonist and evaluation of its neuroprotective effects on Parkinson's disease models
Rymbai, E., Sugumar, D., Chakkittukandiyil, A., Kothandan, R., Selvaraj, J., & Selvaraj, D. (2023) · Life Sciences · doi:10.1016/j.lfs.2023.122144 · Cited by 18 · see citing works
Chronic mild stress induces differential depression-like symptoms and c-Fos and 5HT1A protein levels in high-anxiety female Long Evans rats
Calhoun, C. A., Lattouf, C., Lewis, V., Barrientos, H., & Donaldson, S. T. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114202 · Cited by 17 · see citing works
Postnatal separation prevents the development of prenatal stress‐induced anxiety in association with changes in oestrogen receptor and oxytocin immunoreactivity in female mandarin vole (Microtus mandarinus) offspring
He, F., Wang, Z., & Guo, G. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13788 · Cited by 17 · see citing works
Effects of maternal deprivation and environmental enrichment on anxiety-like and depression-like behaviors correlate with oxytocin system and CRH level in the medial-lateral habenula
Wei, F., Xian, D., He, Y., Yan, Z., Deng, X. Y., Chen, Y., Zhao, L., Zhang, Y., Li, W., Ma, B., et al. (2022) · Peptides · doi:10.1016/j.peptides.2022.170882 · Cited by 17 · see citing works
Aromatized testosterone attenuates contextual generalization of fear in male rats
Lynch, J. F., Vanderhoof, T. S., Winiecki, P., Latsko, M. S., Riccio, D. C., & Jasnow, A. M. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.06.007 · Cited by 15 · see citing works
Interaction of estrogen receptor β and negative life events in susceptibility to major depressive disorder in a Chinese Han female population
Zhang, J., Chen, L., Ma, J., Qiao, Z., Zhao, M., Dong, Q., Zhao, Y. H., Ban, B., Zhu, X., He, J., et al. (2016) · Journal of Affective Disorders · doi:10.1016/j.jad.2016.08.083 · Cited by 15 · see citing works
Sexual experience confers resilience to restraint stress in female rats
Arnold, M. R., Thallon, C. L., Pitkofsky, J. A., & Meerts, S. H. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.12.003 · Cited by 13 · see citing works
Sex-specific prefrontal-hypothalamic control of behavior and stress responding
Schaeuble, D., Wallace, T., Pace, S. A., Hentges, S. T., & Myers, B. (2023) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2023.106413 · Cited by 11 · see citing works
Presence and Absence of Sex Differences in Structure and Function of the Brain Oxytocin System: Implications for Understanding the Regulation of Social Behavior
Dumais, K. M., & Veenema, A. H. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-802114-9.00011-1 · Cited by 11 · see citing works
The gender differences in the inhibitory action of UVB ‐induced melanocyte activation by the administration of tranexamic acid
Hiramoto, K., Yamate, Y., Sugiyama, D., Takahashi, Y., & Mafune, E. (2015) · Photodermatology Photoimmunology & Photomedicine · doi:10.1111/phpp.12231 · Cited by 11 · see citing works
Antidepressant‐Like Effect of Lipid Extract of Channa striatus in Postpartum Model of Depression in Rats
Shukkoor, M. S. A., Baharuldin, M. T. H., Jais, A. M. M., Moklas, M. A. M., Fakurazi, S., & Basir, R. (2017) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2017/1469209 · Cited by 10 · see citing works
Male and female immediate fear reaction to white noise in a semi‐natural environment: A detailed behavioural analysis of the role of sex and oestrogen receptors
Moëne, O. L., Ramírez‐Rentería, M. L., & Ågmo, A. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12902 · Cited by 9 · see citing works
Effects of treadmill exercise on anxiety-like behavior in association with changes in estrogen receptors ERα, ERβ and oxytocin of C57BL/6J female mice
He, F., Fan, M., Hui, Y.-N., Lai, R.-J., Chen, X., Yang, M.-J., Cheng, X., Wang, Z.-J., Yu, B., Yan, B.-J., et al. (2021) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2021.10.001 · Cited by 9 · see citing works
Molecular programs underlying differences in the expression of mood disorders in males and females
Mena, F., & Benoit, L. (2019) · Brain Research · doi:10.1016/j.brainres.2019.05.016 · Cited by 9 · see citing works
Reiterated male-to-female violence disrupts hippocampal estrogen receptor β expression, prompting anxiety-like behavior
Agrimi, J., Bernardele, L., Sbaiti, N., Brondi, M., D’Angelo, D., Canato, M., Marchionni, I., Oeing, C. U., Barbàra, G., Vignoli, B., et al. (2024) · iScience · doi:10.1016/j.isci.2024.110585 · Cited by 8 · see citing works
Prenatal Progestin Exposure-Mediated Oxytocin Suppression Contributes to Social Deficits in Mouse Offspring
Huang, S., Zeng, J., Sun, R., Yu, H. Y., Zhang, H., Su, X., & Yao, P. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.840398 · Cited by 8 · see citing works
Reframing oxytocin as a behavioral flexibility hormone
Walle, K. M., Sartorius, A. M., Deilhaug, E., Kang, H., Nærland, T., Andreassen, O. A., Westlye, L. T., & Quintana, D. S. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106628 · Cited by 8 · see citing works
Estrogen Receptor β in the Lateral Septum Mediates Estrogen Regulation of Social Anxiety-like Behavior in Male Mice
Hasunuma, K., Murakawa, T., Takenawa, S., Mitsui, K., Hatsukano, T., Sano, K., Nakata, M., & Ogawa, S. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.11.019 · Cited by 8 · see citing works
An evolutionary perspective on oxytocin and its behavioral effects
Gangestad, S. W. (2015) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2015.08.016 · Cited by 7 · see citing works
Isoflavone quantitation in soymilk: Genistein content and its biological effect
Freddo, N., Nardi, J., Bertol, C. D., Dallegrave, E., Leal, M. B., Barreto, F., de Assunção, I. B. F., & Rossato‐Grando, L. G. (2019) · CyTA - Journal of Food · doi:10.1080/19476337.2018.1544590 · Cited by 6 · see citing works
Intranasal oxytocin compensates for estrus cycle-specific reduction of conditioned safety memory in rats: Implications for psychiatric disorders
Kreutzmann, J. C., & Fendt, M. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100313 · Cited by 6 · see citing works
Gender and Stress
Handa, R. J., & Chung, W. C. J. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813146-6.00014-x · Cited by 5 · see citing works
Self-citation
M3S-GRPred: a novel ensemble learning approach for the interpretable prediction of glucocorticoid receptor antagonists using a multi-step stacking strategy
Schaduangrat, N., Chuntakaruk, H., Rungrotmongkol, T., Mookdarsanit, P., & Shoombuatong, W. (2025) · BMC Bioinformatics · doi:10.1186/s12859-025-06132-1 · Cited by 5 · see citing works
Estrogen receptors ERα and ERβ participation in hypothalamus–pituitary–adrenal axis activation by hemorrhagic stress
Alves, L. M. S., Filho, P. C. G. D. B., & Franci, C. R. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.03.001 · Cited by 5 · see citing works
Hormonal mechanisms of women’s risk in the face of traumatic stress
Stevens, J. S., Davis, M., Hinojosa, C. A., Hinrichs, R. C., Roeckner, A. R., Oliver, K. I., Taylor, L., Santos, J. L., Zeleke, H., Lin, E., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2524903122 · Cited by 2 · see citing works
Dietary phytoestrogens recalibrate socioemotional behavior in C57Bl/6J mice in a sex- and timing-dependent manner
Roux, C. L., Farthing, A. L., & Lucas, E. K. (2025) · Hormones and Behavior · doi:10.1016/j.yhbeh.2025.105678 · Cited by 1 · see citing works
Association of fermented food intake with the prevalence of depressive symptoms and suicidal ideation in men and women stratified by age: the Korea National Health and Nutrition Examination Survey 2014–2022
Kim, T., & Park, Y. (2026) · Frontiers in Nutrition · doi:10.3389/fnut.2026.1707954 · Cited by 1 · see citing works
Neural, Hormonal and Experiential Control of Sex-Typical Expression of Social Behavior
Ogawa, S., Tsuda, M. C., Sano, K., Tsukahara, S., & Musatov, S. A. (2015) · Interdisciplinary Information Sciences · doi:10.4036/iis.2015.b.02
Effects of reproductive experiences on age-related neural and behavioral changes in female rats
Belgrave, S. K. (2015) · CUNY Academic Works (City University of New York)
Pharmacological Characterisation of Novel Oxytocin and Vasopressin Receptor Ligands
Gulliver, D. W. (2021) · The Sydney eScholarship Repository (The University of Sydney)
Association between duration of birth control pill use and risk of depression among US women
Sun, Y., & Zhang, C. (2025) · The International Journal of Psychiatry in Medicine · doi:10.1177/00912174251334309
Flaxseed Administration Improves Affective and Cognitive Functions in Fructose Diet Wistar Rats
Elkaoui, H., Chakit, M., Mesfioui, A., & Elhessni, A. (2025) · Egyptian Journal of Veterinary Science · doi:10.21608/ejvs.2025.369553.2713
Effets de l’exposition aux phtalates sur les comportements de reproduction de la souris femelle
Adam, N. (2022) · theses.fr (ABES) · doi:10.70675/f8535eb9z782dz40b8zb1d0z583132d3fd1b
The expression of calbindin, calretinin, and parvalbumin, markers of gamma-aminobutyric acid neurons, is reduced in the dentate gyrus and hippocampus proper of oestrogen receptor β-deficient female mice
Gąsiorowska, S., Bogus‐Nowakowska, K., & Kalinowski, D. (2026) · Brain Mechanisms · doi:10.1016/j.bramec.2026.202559
Estrogen receptor β in the prefrontal cortex mediates stress-induced anxiety-like behaviors in female mice
Woodward, E. M., & Coutellier, L. D. (2026) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2026.108028
Natural products as selective estrogen receptor modulators in depression-related disorders: Balancing antidepressant efficacy and safety
Chen, R., Luo, J., He, K., Yang, D., & Zhao, H. (2026) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2026.119937
Early Postnatal Androgenic Activity Inhibition Produces Differential Long‐Term Alterations in Anxiety‐Like Behavior in Young Adult Male and Female Wistar Rats
Primo, U., Fernández‐García, J. M., García-Úbeda, R., Collado, P., Carrillo, B., & Pinos, H. (2026) · Developmental Psychobiology · doi:10.1002/dev.70211

A Role for the Androgen Metabolite, 5α‐Androstane‐3β,17β‐Diol, in Modulating Oestrogen Receptor β‐Mediated Regulation of Hormonal Stress Reactivity
Handa, R. J., Weiser, M. J., & Zuloaga, D. G. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01840.x · Cited by 95 · see citing works
Self-citation
Anxiolytic Effects and Neuroanatomical Targets of Estrogen Receptor-β (ERβ) Activation by a Selective ERβ Agonist in Female Mice
Oyola, M. G., Portillo, W., Reyna, A., Foradori, C. D., Kudwa, A., Hinds, L., Handa, R. J., & Mani, S. K. (2012) · Endocrinology · doi:10.1210/en.2011-1674 · Cited by 99 · see citing works
Self-citation
A Role for the Androgen Metabolite, 5alpha Androstane 3beta, 17beta Diol (3?-Diol) in the Regulation of the Hypothalamo-Pituitary?Adrenal Axis
Handa, R. J., Sharma, D., & Uht, R. M. (2011) · Frontiers in Endocrinology · doi:10.3389/fendo.2011.00065 · Cited by 52 · see citing works
Self-citation
Estrogen receptor beta activation prevents glucocorticoid receptor-dependent effects of the central nucleus of the amygdala on behavior and neuroendocrine function
Weiser, M. J., Foradori, C. D., & Handa, R. J. (2010) · Brain Research · doi:10.1016/j.brainres.2010.03.098 · Cited by 66 · see citing works
Self-citation
Estrogen receptor β in the paraventricular nucleus of hypothalamus regulates the neuroendocrine response to stress and is regulated by corticosterone
Isgor, C., Cecchi, M., Kabbaj, M., Akil, H., & Watson, S. J. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00561-x · Cited by 107 · see citing works

Authors: Kudwa, A. E., McGivern, R. F., & Handa, R. J.
Affiliations: Colorado State University (US)
San Diego State University (US)
University of Arizona College of Medicine- Phoenix (US)
ORCID: McGivern, Robert F.
Handa, Robert J.
Venue: Physiology & Behavior
Publisher: Elsevier BV
Published: 2014-04
Volume: 129
Pages: 287-296
ISSN: 0031-9384 (ISSN-L)
DOI: 10.1016/j.physbeh.2014.03.004
PMC: PMC5802969
OpenAlex: W2079429876
Cited by: 73
References: 65
Citations by year: 2026: 6 · 2025: 5 · 2024: 3 · 2023: 4 · 2022: 8 · 2021: 7 · 2020: 5 · 2019: 6 · 2018: 3 · 2017: 9 · 2016: 6 · 2015: 8 · 2014: 3
FWCI: 4.25
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Physiology & Behavior (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: NIH (R01-NS039951)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Keywords: estrogen receptor beta, oxytocin, anxiety-like behavior, hypothalamic-pituitary-adrenal axis, stress reactivity, paraventricular nucleus, diarylpropionitrile, corticosterone, ACTH, oxytocin antagonist, sex differences, sex steroids
MeSH terms: Adrenocorticotropic Hormone, Animals, Anxiety, Central Nervous System Agents, Corticosterone, Depressive Disorder, Exploratory Behavior, Female, Male, Nitriles, Ornipressin, Oxytocin, Propionates, Restraint, Physical, Sex Factors, Stress, Psychological, Rats, Sprague-Dawley, Maze Learning, Estrogen Receptor beta

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

Estrogen receptor β and oxytocin interact to modulate anxiety-like behavior and neuroendocrine stress reactivity in adult male and female rats

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks