Early embryonic administration of xenoestrogens alters vasotocin system and male sexual behavior of the Japanese quail
Abstract
The copulatory behavior and the parvocellular vasotocin (VT) system of the nucleus of the stria terminalis (BST) are sexually dimorphic in the Japanese quail. Embryonic administration of estradiol benzoate (EB) induces an organizational effect determining the disappearance of such a dimorphism (male shows behavior and cerebral phenotype of the female). The VT parvocellular system can therefore be considered an accurate marker of the sexual differentiation of brain circuits and a very sensitive indicator of the activity of estrogen-like substances on neural circuits. To test this hypothesis we administered diethylstilbestrol (DES), a powerful synthetic xenoestrogen, genistein (GEN), a phytoestrogen produced by soy, and bisphenol A (BPA). After 3 days of incubation, quail eggs were injected with vehicle, EB, DES, GEN or BPA. Administration of BPA caused an early blockage of development and no further analyses were done on the BPA groups. At puberty, the copulatory behavior of EB- or DES-treated male quail was totally abolished, whereas only the highest doses of GEN determined a significant decrease of the behavior. After the tests, the animals were sacrificed and perfused. The fractional area (FA) covered by VT immunoreactivity was analyzed in BST, medial preoptic nucleus, and lateral septum by computerized image analysis. The FA was significantly reduced after treatment with EB, DES and GEN at high doses. These results confirm that the sexually dimorphic VT system of the Japan…
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GEN alters AVP and OT neuron numbers and innervation of sexually dimorphic regions associated with social and aggressive behaviors in multiple species, and is anxiogenic in males of multiple species.
“Altered AVP and OT neuron numbers and innervation of sexually dimorphic regions associated with social and aggressive behaviors in multiple species; anxiogenic in males of multiple species”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [70]
Exogenous administration of estrogen, DES, or an aromatase inhibitor during incubation fully blocked male copulatory behavior at puberty and induced the complete sex reversal of VT-ir in the preoptic area, BnST, and lateral septum.
“Exogenous administration of estrogen, diethylstilbestrol (DES), or an aromatase inhibitor during incubation fully blocked male copulatory behavior at puberty and induced the complete sex reversal of VT-ir in the preoptic area, BnST, and lateral septum (LS) (70, 81).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [70]
Multiple aspects of the quail VT system are vulnerable to EDCs including BPA, DES, and high doses of the phytoestrogen GEN.
“Seminal research dating back decades has consistently and repeatedly shown that multiple aspects of the quail VT system is vulnerable to EDCs including bisphenol A (BPA), diethylstilbestrol (DES), and high doses of the phytoestrogen genistein (GEN) (69, 70).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [70]
Cites
(2009) · Elsevier eBooks · doi:10.1016/c2009-1-03789-7 · Cited by 1,543 · see citing works
(2003) · Choice Reviews Online · doi:10.5860/choice.40-2774 · Cited by 705 · see citing works
Hormonal control of behavior in the Japanese quail.
Adkins, E., & Alder, N. T. (1972) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0033315 · Cited by 288 · see citing works
Panzica, G., Viglietti‐Panzica, C., & Balthazart, J. (1996) · Frontiers in Neuroendocrinology · doi:10.1006/frne.1996.0002 · Cited by 283 · see citing works
Self-citationvan Leeuwen, F. W., Caffe, A. R., & Vries, G. J. D. (1985) · Brain Research · doi:10.1016/0006-8993(85)90348-8 · Cited by 248 · see citing works
Sexual differentiation of brain and behavior in birds
Balthazart, J., & Ball, G. F. (1995) · Trends in Endocrinology and Metabolism · doi:10.1016/1043-2760(94)00098-o · Cited by 207 · see citing works
Aste, N., Balthazart, J., Absil, P., Grossmann, R., M�lhbauer, E., Viglietti‐Panzica, C., & Panzica, G. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980629)396:2 · Cited by 147 · see citing works
Self-citationBerg, C., Halldin, K., Fridolfsson, A., Brandt, I., & Brunström, B. (1999) · The Science of The Total Environment · doi:10.1016/s0048-9697(99)00179-5 · Cited by 131 · see citing works
Control of reproductive behavior by sex steroids in male quail.
Adkins, E., & Pniewski, E. E. (1978) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077523 · Cited by 131 · see citing works
Sexual Differentiation of Brain and Behavior in Birds
Balthazart, J., & Adkins–Regan, E. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50068-8 · Cited by 112 · see citing works
Viglietti‐Panzica, C., Aste, N., Balthazart, J., & Panzica, G. (1994) · Brain Research · doi:10.1016/0006-8993(94)90965-2 · Cited by 105 · see citing works
Self-citationBalthazart, J., Dupiereux, V., Aste, N., Viglietti‐Panzica, C., Barrese, M., & Panzica, G. (1994) · Cell and Tissue Research · doi:10.1007/bf00343944 · Cited by 102 · see citing works
Self-citationPanzica, G., Aste, N., Castagna, C., Viglietti‐Panzica, C., & Balthazart, J. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00118-7 · Cited by 99 · see citing works
Self-citationOrganization of vasotocin‐immunoreactive cells and fibers in the canary brain
Kiss, J. Z., Voorhuis, T. A. M., van Eekelen, J. A. M., de Kloet, E. R., & de Wied, D. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902630304 · Cited by 97 · see citing works
Balthazart, J. (1992) · Hormones and Behavior · doi:10.1016/0018-506x(92)90041-s · Cited by 89 · see citing works
Castagna, C., Absil, P., Foidart, A., & Balthazart, J. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.1.233 · Cited by 86 · see citing works
Viglietti‐Panzica, C., Anselmetti, G., Balthazart, J., Aste, N., & Panzica, G. (1992) · Cell and Tissue Research · doi:10.1007/bf00302963 · Cited by 81 · see citing works
Self-citationSchumacher, M., Sulon, J., & Balthazart, J. (1988) · Journal of Endocrinology · doi:10.1677/joe.0.1180127 · Cited by 72 · see citing works
Jurkevich, A., Barth, S., & Grossmann, R. (1996) · Cell and Tissue Research · doi:10.1007/s004410050732 · Cited by 68 · see citing works
Immunoreactive vasotocin in the zebra finch brain (Taeniopygia guttata)
Voorhuis, T. A. M., & de Kloet, E. R. (1992) · Developmental Brain Research · doi:10.1016/0165-3806(92)90116-e · Cited by 65 · see citing works
Neuroendocrine and Behavioral Implications of Endocrine Disrupting Chemicals in Quail
Ottinger, M. A., Abdelnabi, M. A., Henry, P. F. P., McGary, S., Thompson, N., & Wu, J. M. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1695 · Cited by 64 · see citing works
Sexual differentiation in quail: Critical period and hormonal specificity
Schumacher, M., Jc, H., & Balthazart, J. (1989) · Hormones and Behavior · doi:10.1016/0018-506x(89)90080-9 · Cited by 63 · see citing works
Panzica, G., García‐Ojeda, E., Viglietti‐Panzica, C., Thompson, N., & Ottinger, M. A. (1996) · Brain Research · doi:10.1016/0006-8993(95)01386-5 · Cited by 61 · see citing works
Self-citationEstradiol Mediates Effects of Testosterone on Vasotocin Immunoreactivity in the Adult Quail Brain
Viglietti‐Panzica, C., Balthazart, J., Plumari, L., Fratesi, S., Absil, P., & Panzica, G. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1710 · Cited by 49 · see citing works
Self-citationAbsil, P., Papello, M., Viglietti‐Panzica, C., Balthazart, J., & Panzica, G. (2002) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(02)00017-0 · Cited by 39 · see citing works
Self-citationViglietti-Panzica, C., Mura, E., & Panzica, G. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.12.003 · Cited by 37 · see citing works
Self-citationOntogenetic and seasonal changes in immunoreactive vasotocin in the canary brain
Voorhuis, T. A. M., de Kloet, E. R., & de Wied, D. (1991) · Developmental Brain Research · doi:10.1016/0165-3806(91)90110-5 · Cited by 34 · see citing works
Vasotocin and reproductive functions of the domestic chicken
Jurkevich, A., & Grossmann, R. (2003) · Domestic Animal Endocrinology · doi:10.1016/s0739-7240(03)00048-1 · Cited by 34 · see citing works
Panzica, G., Pessatti, M., Viglietti‐Panzica, C., Großmann, R., & Balthazart, J. (1999) · Brain Research · doi:10.1016/s0006-8993(99)02098-3 · Cited by 33 · see citing works
Self-citationOrganizational effects of diethylstilbestrol on brain vasotocin and sexual behavior in male quail
Viglietti‐Panzica, C., Montoncello, B., Mura, E., Pessatti, M., & Panzica, G. (2004) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2004.11.018 · Cited by 26 · see citing works
Self-citationPanzica, G., Bakthazart, J., Pessatti, M., & Viglietti‐Panzica, C. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.02110s3423 · Cited by 26 · see citing works
Self-citationPlumari, L., Plateroti, S., Deviche, P., & Panzica, G. (2003) · Brain Research · doi:10.1016/j.brainres.2003.10.037 · Cited by 26 · see citing works
Self-citationGender‐related changes in the avian vasotocin system during ontogeny
Jurkevich, A., Großmann, R., Balthazart, J., & Viglietti‐Panzica, C. (2001) · Microscopy Research and Technique · doi:10.1002/jemt.1153 · Cited by 17 · see citing works
Self-citation- Self-citation
Ciliax (1999) · doi:10.1002/(sici)1096-9861(19990621)409:1
Self-citation
Flagged first, then by citations
1 of the 36 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
NTP‐CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A
Chapin, R. E., Adams, J., Boekelheide, K., Gray, L. E., Hayward, S. W., Lees, P. S. J., Mcintyre, B., Portier, K. M., Schnorr, T. M., Selevan, S. G., et al. (2008) · Birth Defects Research Part B Developmental and Reproductive Toxicology · doi:10.1002/bdrb.20147 · Cited by 504 · see citing works
Current concepts in neuroendocrine disruption
León‐Olea, M., Martyniuk, C. J., Orlando, E. F., Ottinger, M. A., Rosenfeld, C. S., Wolstenholme, J. T., & Trudeau, V. L. (2014) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2014.02.005 · Cited by 144 · see citing works
Bisphenol A and phthalate endocrine disruption of parental and social behaviors
Rosenfeld, C. S. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00057 · Cited by 119 · see citing works
Ottinger, M. A., Lavoie, E. T., Thompson, N., Barton, A., Whitehouse, K., Barton, M., Abdelnabi, M. A., Quinn, M. A., Panzica, G., & Viglietti‐Panzica, C. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.08.011 · Cited by 99 · see citing works
Self-citationNTP‐CERHR expert panel report on the reproductive and developmental toxicity of genistein
Rozman, K. K., Bhatia, J. J. S., Calafat, A. M., Chambers, C., Culty, M., Etzel, R. A., Flaws, J. A., Hansen, D. K., Hoyer, P. B., Jeffery, E. H., et al. (2006) · Birth Defects Research Part B Developmental and Reproductive Toxicology · doi:10.1002/bdrb.20087 · Cited by 85 · see citing works
The Phytoestrogen Genistein Affects Zebrafish Development through Two Different Pathways
Sassi-Messai, S., Gibert, Y., Bernard, L., Nishio, S., Ferri, K. F., Molina-Molina, J.-M., Andersson‐Lendahl, M., Benoit, G., Balaguer, P., & Laudet, V. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004935 · Cited by 83 · see citing works
Neuroactive steroids: Old players in a new game
Melcangi, R. C., & Panzica, G. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.066 · Cited by 80 · see citing works
Self-citationAchieving <scp>CLARITY</scp> on bisphenol A, brain and behaviour
Patisaul, H. B. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12730 · Cited by 76 · see citing works
Milestones on Steroids and the Nervous System: 10 Years of Basic and Translational Research
Panzica, G., Balthazart, J., Frye, C. A., García‐Segura, L. M., Herbison, A. E., Mensah‐Nyagan, A. G., McCarthy, M. M., & Melcangi, R. C. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02265.x · Cited by 55 · see citing works
Self-citationEndocrine 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
“Exogenous administration of estrogen, diethylstilbestrol (DES), or an aromatase inhibitor during incubation fully blocked male copulatory behavior at puberty and induced the complete sex reversal of VT-ir in the preoptic area, BnST, and lateral septum (LS) (70, 81).”
BackgroundPatisaul, H. B. (2021) · Advances in pharmacology · doi:10.1016/bs.apha.2021.03.007 · Cited by 42 · see citing works
Witchey, S. K., Fuchs, J., & Patisaul, H. B. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.06.007 · Cited by 40 · see citing works
Ma, A., Yang, X., Wang, Z., Shi, D., & Chen, Y. (2008) · Reproductive Toxicology · doi:10.1016/j.reprotox.2007.12.007 · Cited by 32 · see citing works
Wilhelms, K. W., Scanes, C. G., & Anderson, L. L. (2006) · Poultry Science · doi:10.1093/ps/85.11.1885 · Cited by 31 · see citing works
Panzica, G., Mura, E., Miceli, D., Martini, M., Gotti, S., & Viglietti‐Panzica, C. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2008.03628.x · Cited by 21 · see citing works
Self-citationRochester, J. R., Klasing, K. C., Stevenson, L., Denison, M. S., Berry, W. D., & Millam, J. R. (2008) · Reproductive Toxicology · doi:10.1016/j.reprotox.2008.11.056 · Cited by 20 · see citing works
Mattsson, A., & Brunström, B. (2017) · PLoS ONE · doi:10.1371/journal.pone.0180548 · Cited by 19 · see citing works
Yiğit, F., & Dağlioğlu, S. (2010) · PROTOPLASMA · doi:10.1007/s00709-010-0140-x · Cited by 16 · see citing works
Effects of bisphenol-A on male reproductive success in adult Kadaknath chicken
Singh, R. P., Shafeeque, C. M., Sharma, S. K., Singh, R., Maharajan, K., Sastry, K. V. H., Raghunandanan, S., Mohan, J., & Azeez, P. A. (2016) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2016.02.012 · Cited by 15 · see citing works
Environmental Endocrine Disruption of Brain and Behavior
Gore, A. C., & Crews, D. P. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00056-5 · Cited by 15 · see citing works
Corbitt, C., Satre, D., Adamson, L. A., COBBS, G. A., & Bentley, G. E. (2007) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2007.06.026 · Cited by 15 · see citing works
Lilienthal, H., Heikkinen, P., Andersson, P. L., & Viluksela, M. (2013) · Toxicology · doi:10.1016/j.tox.2013.01.025 · Cited by 13 · see citing works
Eldefrawy, F., Xu, H. S., Pusch, E. A., Karkoura, A. A., Alsafy, M., El‐Gendy, S. A. A., Williams, S. M., Navara, K. J., & Guo, T. L. (2021) · Reproductive Toxicology · doi:10.1016/j.reprotox.2021.06.010 · Cited by 10 · see citing works
Endocrine disrupting chemicals and behavior: Re-evaluating the science at a critical turning point
Barrett, E. S., & Patisaul, H. B. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.09.010 · Cited by 10 · see citing works
Bonaldo, B., Casile, A., Bettarelli, M., Gotti, S., Panzica, G., & Marraudino, M. (2021) · European Journal of Histochemistry · doi:10.4081/ejh.2021.3272 · Cited by 9 · see citing works
Self-citationWang, J., Jin, S., Fu, W., Liang, Y., Yang, Y., & Xu, X. (2021) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2021.112843 · Cited by 9 · see citing works
Organizational effects of DDE on brain vasotocin system in male Japanese quail
Mura, E., Barale, C., Quinn, M. J., Panzica, G., Ottinger, M. A., & Viglietti‐Panzica, C. (2009) · NeuroToxicology · doi:10.1016/j.neuro.2009.01.012 · Cited by 8 · see citing works
Self-citationTesticular Functions and Sexual Behavior in Male Japanese Quail after Exposure to Bisphenol A
Hanafy, A. M., Khalil, H. A., Abdel-Rahi, W. M., & Abdel-Ghan, A. M. (2015) · Asian Journal of Poultry Science · doi:10.3923/ajpsaj.2016.40.51 · Cited by 8 · see citing works
Effects of Lactational Exposure to Soy Isoflavones on Reproductive System in Neonatal Female Rats*
Liu, Z., Zhang, X., Li, L., Zhang, W., Cui, W., Song, Y., Wang, W. J., Jia, X., Li, N., & Yan, W. (2007) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/j.1742-7843.2007.00172.x · Cited by 8 · see citing works
Environmental Endocrine Disruption of Brain and Behavior
Patisaul, H. B., Gore, A. C., & Crews, D. P. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00094-8 · Cited by 3 · see citing works
Phytoestrogens and phytosterols
Hendrich, S. (2009) · Elsevier eBooks · doi:10.1533/9781845695743.4.437 · Cited by 2 · see citing works
Hertamawati, R. T., Nusantoro, S., & Rahma, R. (2021) · IOP Conference Series Earth and Environmental Science · doi:10.1088/1755-1315/672/1/012043 · Cited by 2 · see citing works
Miranda, R. A. (2013) · ProQuest Demo Repository
Komisaruk, B. R., & González-Mariscal, G. (2017) · CRC Press eBooks · doi:10.1201/9781315388069-15
Shenoy, K. (2012) · UKnowledge (University of Kentucky)
Perumal, S., Kolluri, G., Singh, R. P., Mohan, J., & Tyagi, J. S. (2026) · Environmental Toxicology · doi:10.1002/tox.70079
MATTOS, A. P., FERREIRA, J. H., Ventura, R. R., & Ruginsk, S. G. (2026) · Reproductive Toxicology · doi:10.1016/j.reprotox.2026.109356
- Authors
- Panzica, G., Mura, E., Pessatti, M., & Viglietti-Panzica, C.
- Affiliations
- University of Turin (IT)
- Corresponding author
- Panzica, GianCarlo
- ORCID
- Panzica, GianCarlo
- Venue
- Domestic Animal Endocrinology
- Publisher
- Elsevier BV
- Published
- 2005-08
- Volume
- 29
- Issue
- 2
- Pages
- 436-445
- ISSN
- 0739-7240 (ISSN-L)
- OpenAlex
- W2023978173
- Cited by
- 38
- References
- 36
- Citations by year
- 2026: 2 · 2024: 1 · 2021: 5 · 2019: 2 · 2017: 4 · 2016: 2 · 2015: 2 · 2014: 1 · 2013: 2 · 2012: 1
- FWCI
- 2.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Domestic Animal Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Institutional Research Information System University of Turin (University of Turin) (submittedVersion)
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- xenoestrogens, male sexual behavior, mating behavior, Japanese quail, estradiol benzoate, diethylstilbestrol, genistein, bisphenol A, sexual differentiation of the brain, medial preoptic nucleus, lateral septum, sexual dimorphism
- MeSH terms
- Bisphenol A Compounds, Animals, Benzhydryl Compounds, Coturnix, Diethylstilbestrol, Embryo, Nonmammalian, Estrogens, Female, Male, Phenols, Septal Nuclei, Sexual Behavior, Animal, Vasotocin, Genistein, Phytoestrogens
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