{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,11]],"date-time":"2025-12-11T20:58:45Z","timestamp":1765486725900,"version":"build-2065373602"},"reference-count":72,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2022,1,20]],"date-time":"2022-01-20T00:00:00Z","timestamp":1642636800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000066","name":"National Institute of Environmental Health Sciences","doi-asserted-by":"publisher","award":["RO1 ES023254, RO1 ES029464"],"award-info":[{"award-number":["RO1 ES023254, RO1 ES029464"]}],"id":[{"id":"10.13039\/100000066","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Toxics"],"abstract":"<jats:p>Endocrine-disrupting chemicals (EDCs) lead to endocrine and neurobehavioral changes, particularly due to developmental exposures during gestation and early life. Moreover, intergenerational and transgenerational phenotypic changes may be induced by germline exposure (F2) and epigenetic germline transmission (F3) generation, respectively. Here, we assessed reproductive and sociosexual behavioral outcomes of prenatal Aroclor 1221 (A1221), a lightly chlorinated mix of PCBs known to have weakly estrogenic mechanisms of action; estradiol benzoate (EB), a positive control; or vehicle (3% DMSO in sesame oil) in F1-, F2-, and F3-generation male and female rats. Treatment with EDCs was given on embryonic day (E) 16 and 18, and F1 offspring monitored for development and adult behavior. F2 offspring were generated by breeding with untreated rats, phenotyping of F2s was performed in adulthood, and the F3 generation were similarly produced and phenotyped. Although no effects of treatment were found on F1 or F3 development and physiology, in the F2 generation, body weight in males and uterine weight in females were increased by A1221. Mating behavior results in F1 and F2 generations showed that F1 A1221 females had a longer latency to lordosis. In males, the F2 generation showed decreased mount frequency in the EB group. In the F3 generation, numbers of ultrasonic vocalizations were decreased by EB in males, and by EB and A1221 when the sexes were combined. Finally, partner preference tests in the F3 generation revealed that na\u00efve females preferred F3-EB over untreated males, and that na\u00efve males preferred untreated over F3-EB or F3-A1221 males. As a whole, these results show that each generation has a unique, sex-specific behavioral phenotype due to direct or ancestral EDC exposure.<\/jats:p>","DOI":"10.3390\/toxics10020047","type":"journal-article","created":{"date-parts":[[2022,1,20]],"date-time":"2022-01-20T22:59:57Z","timestamp":1642719597000},"page":"47","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Transgenerational Effects of Prenatal Endocrine Disruption on Reproductive and Sociosexual Behaviors in Sprague Dawley Male and Female Rats"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8237-3641","authenticated-orcid":false,"given":"Bailey A.","family":"Kermath","sequence":"first","affiliation":[{"name":"Institute for Neuroscience, The University of Texas at Austin, Austin, TX 78712, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lindsay M.","family":"Thompson","sequence":"additional","affiliation":[{"name":"Division of Pharmacology & Toxicology, College of Pharmacy, The University of Texas at Austin, Austin, TX 78712, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Justin R.","family":"Jefferson","sequence":"additional","affiliation":[{"name":"Division of Pharmacology & Toxicology, College of Pharmacy, The University of Texas at Austin, Austin, TX 78712, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mary H. B.","family":"Ward","sequence":"additional","affiliation":[{"name":"Division of Pharmacology & Toxicology, College of Pharmacy, The University of Texas at Austin, Austin, TX 78712, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5549-6793","authenticated-orcid":false,"given":"Andrea C.","family":"Gore","sequence":"additional","affiliation":[{"name":"Institute for Neuroscience, The University of Texas at Austin, Austin, TX 78712, USA"},{"name":"Division of Pharmacology & Toxicology, College of Pharmacy, The University of Texas at Austin, Austin, TX 78712, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,1,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"4097","DOI":"10.1210\/en.2012-1422","article-title":"Endocrine-Disrupting Chemicals and Public Health Protection: A Statement of Principles from The Endocrine Society","volume":"153","author":"Zoeller","year":"2012","journal-title":"Endocrinology"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"E1","DOI":"10.1210\/er.2015-1010","article-title":"EDC-2: The Endocrine Society\u2019s Second Scientific Statement on Endocrine-Disrupting Chemicals","volume":"36","author":"Gore","year":"2015","journal-title":"Endocr. Rev."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1023\/A:1025388901248","article-title":"The developmental origins of adult disease","volume":"18","author":"Barker","year":"2003","journal-title":"Eur. J. Epidemiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1037\/com0000103","article-title":"Application of a Novel Social Choice Paradigm to Assess Effects of Prenatal Endocrine-Disrupting Chemical Exposure in Rats (Rattus norvegicus)","volume":"132","author":"Reilly","year":"2018","journal-title":"J. Comp. Psychol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.yhbeh.2015.06.002","article-title":"The effects of prenatal PCBs on adult social behavior in rats","volume":"73","author":"Reilly","year":"2015","journal-title":"Horm. Behav."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/j.mce.2018.09.010","article-title":"Social and neuromolecular phenotypes are programmed by prenatal exposuRes to endocrine-disrupting chemicals","volume":"479","author":"Topper","year":"2019","journal-title":"Mol. Cell Endocrinol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1016\/j.yhbeh.2012.02.011","article-title":"Perinatal BPA exposure demasculinizes males in measuRes of affect but has no effect on water maze learning in adulthood","volume":"61","author":"Jones","year":"2012","journal-title":"Horm. Behav."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1002\/syn.20746","article-title":"Prenatal and postnatal exposure to bisphenol a induces anxiolytic behaviors and cognitive deficits in mice","volume":"64","author":"Tian","year":"2010","journal-title":"Synapse"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.mce.2018.03.017","article-title":"Impairment of learning and memory performances induced by BPA: Evidences from the literature of a MoA mediated through an ED","volume":"475","author":"Belzunces","year":"2018","journal-title":"Mol. Cell Endocrinol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/j.yhbeh.2012.09.009","article-title":"Sex and dose-dependent effects of developmental exposure to bisphenol A on anxiety and spatial learning in deer mice (Peromyscus maniculatus bairdii) offspring","volume":"63","author":"Jasarevic","year":"2013","journal-title":"Horm. Behav."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/j.pnpbp.2012.06.016","article-title":"Effects of perinatal exposure to low dose of bisphenol A on anxiety like behavior and dopamine metabolites in brain","volume":"39","author":"Matsuda","year":"2012","journal-title":"Prog. Neuro-Psychopharmacol. Biol. Psychiatry"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"580","DOI":"10.1016\/j.yhbeh.2008.01.008","article-title":"Neonatal exposure to endocrine active compounds or an ERbeta agonist increases adult anxiety and aggression in gonadally intact male rats","volume":"53","author":"Patisaul","year":"2008","journal-title":"Horm. Behav."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1016\/j.yhbeh.2012.08.005","article-title":"Gestational and lactational exposure to bisphenol-A affects anxiety- and depression-like behaviors in mice","volume":"62","author":"Xu","year":"2012","journal-title":"Horm. Behav."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.yhbeh.2015.11.007","article-title":"Two-hit exposure to polychlorinated biphenyls at gestational and juvenile life stages: 1. Sexually dimorphic effects on social and anxiety-like behaviors","volume":"78","author":"Bell","year":"2016","journal-title":"Horm. Behav."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.yhbeh.2016.10.011","article-title":"Anxiety-like behaviors in adulthood are altered in male but not female rats exposed to low dosages of polychlorinated biphenyls in utero","volume":"87","author":"Gillette","year":"2017","journal-title":"Horm. Behav."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Quinnies, K.M., Harris, E.P., Snyder, R.W., Sumner, S.S., and Rissman, E.F. (2017). Direct and transgenerational effects of low doses of perinatal di-(2-ethylhexyl) phthalate (DEHP) on social behaviors in mice. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0171977"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"692","DOI":"10.1016\/j.yhbeh.2013.01.006","article-title":"Antiandrogenic effect of perinatal exposure to the endocrine disruptor di-(2-ethylhexyl) phthalate increases anxiety-like behavior in male rats during sexual maturation","volume":"63","author":"Carbone","year":"2013","journal-title":"Horm. Behav."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1289\/ehp.1307063","article-title":"Prenatal phthalate exposuRes and neurobehavioral development scoRes in boys and girls at 6\u201310 years of age","volume":"122","author":"Kobrosly","year":"2014","journal-title":"Environ. Health Perspect."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"105892","DOI":"10.1016\/j.envint.2020.105892","article-title":"Similar names, different results: Consistency of the associations between prenatal exposure to phthalates and parent-ratings of behavior problems in preschool children","volume":"142","author":"Martin","year":"2020","journal-title":"Environ. Int."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"261","DOI":"10.9758\/cpn.2020.18.2.261","article-title":"Associations between Exposure to Bisphenol A and Behavioral and Cognitive Function in Children with Attention-deficit\/Hyperactivity Disorder: A Case-control Study","volume":"18","author":"Yoo","year":"2020","journal-title":"Clin. Psychopharmacol. Neurosci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/j.envres.2016.07.028","article-title":"Bisphenol A exposure and symptoms of anxiety and depression among inner city children at 10\u201312 years of age","volume":"151","author":"Perera","year":"2016","journal-title":"Environ. Res."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Vermeir, G., Covaci, A., Van Larebeke, N., Schoeters, G., Nelen, V., Koppen, G., and Viaene, M. (2021). Neurobehavioural and cognitive effects of prenatal exposure to organochlorine compounds in three year old children. BMC Pediatr., 21.","DOI":"10.1186\/s12887-021-02533-2"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1466","DOI":"10.1126\/science.1108190","article-title":"Epigenetic transgenerational actions of endocrine disruptors and male fertility","volume":"308","author":"Anway","year":"2005","journal-title":"Science"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1106","DOI":"10.1080\/15592294.2018.1543506","article-title":"Passing experiences on to future generations: Endocrine disruptors and transgenerational inheritance of epimutations in brain and sperm","volume":"13","author":"Gillette","year":"2018","journal-title":"Epigenetics"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"eabd1159","DOI":"10.1126\/sciadv.abd1159","article-title":"Gestational low-dose BPA exposure impacts suprachiasmatic nucleus neurogenesis and circadian activity with transgenerational effects","volume":"7","author":"Nesan","year":"2021","journal-title":"Sci. Adv."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"3077","DOI":"10.1210\/EN.2015-1326","article-title":"Transgenerational Effects of Di-(2-Ethylhexyl) Phthalate (DEHP) on Stress Hormones and Behavior","volume":"156","author":"Quinnies","year":"2015","journal-title":"Endocrinology"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"3828","DOI":"10.1210\/en.2012-1195","article-title":"Gestational exposure to bisphenol A produces transgenerational changes in behaviors and gene expression","volume":"153","author":"Wolstenholme","year":"2012","journal-title":"Endocrinology"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1016\/j.yhbeh.2013.09.007","article-title":"Transgenerational effects of prenatal bisphenol A on social recognition","volume":"64","author":"Wolstenholme","year":"2013","journal-title":"Horm. Behav."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"097005","DOI":"10.1289\/EHP3550","article-title":"Effects of the endocrine-disrupting chemicals, vinclozolin and polychlorinated biphenyls, on physiological and sociosexual phenotypes in F2 generation Sprague-Dawley rats","volume":"126","author":"Krishnan","year":"2018","journal-title":"Environ. Health Perspect."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1016\/j.yhbeh.2018.12.009","article-title":"Maternal care modulates transgenerational effects of endocrine-disrupting chemicals on offspring pup vocalizations and adult behaviors","volume":"107","author":"Krishnan","year":"2019","journal-title":"Horm. Behav."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"9143","DOI":"10.1073\/pnas.1118514109","article-title":"Epigenetic transgenerational inheritance of altered stress responses","volume":"109","author":"Crews","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"5942","DOI":"10.1073\/pnas.0610410104","article-title":"Transgenerational epigenetic imprints on mate preference","volume":"104","author":"Crews","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"112063","DOI":"10.1016\/j.envres.2021.112063","article-title":"A cross-species comparative approach to assessing multi- and transgenerational effects of endocrine disrupting chemicals","volume":"204","author":"Robaire","year":"2021","journal-title":"Environ. Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"112674","DOI":"10.1016\/j.physbeh.2019.112674","article-title":"Endocrine-disrupting chemicals alter the neuromolecular phenotype in F2 generation adult male rats","volume":"211","author":"Krishnan","year":"2019","journal-title":"Physiol. Behav."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"690","DOI":"10.1093\/biolre\/ioab066","article-title":"Transgenerational effects of polychlorinated biphenyls: 2. Hypothalamic gene expression in rats \u2020","volume":"105","author":"Gore","year":"2021","journal-title":"Biol. Reprod."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/s12940-018-0362-5","article-title":"Transgenerational effects of polychlorinated biphenyls: 1. Development and physiology across 3 generations of rats","volume":"17","author":"Mennigen","year":"2018","journal-title":"Environ. Health"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1016\/j.yhbeh.2006.12.004","article-title":"The effects of prenatal PCBs on adult female paced mating reproductive behaviors in rats","volume":"51","author":"Steinberg","year":"2007","journal-title":"Horm. Behav."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1210\/en.2010-1103","article-title":"Endocrine disruption of brain sexual differentiation by developmental PCB exposure","volume":"152","author":"Dickerson","year":"2011","journal-title":"Endocrinology"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1289\/ehp.10432","article-title":"Polychlorinated biphenyl exposure and neuropsychological status among older residents of upper Hudson River communities","volume":"116","author":"Fitzgerald","year":"2008","journal-title":"Environ. Health Perspect."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/S0031-9384(03)00227-0","article-title":"Characterization of 50-kHz ultrasonic vocalizations in male and female rats","volume":"80","author":"McGinnis","year":"2003","journal-title":"Physiol. Behav."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1017\/S1461145709990113","article-title":"Influence of acute caffeine on 50-kHz ultrasonic vocalizations in male adult rats and relevance to caffeine-mediated psychopharmacological effects","volume":"13","author":"Simola","year":"2010","journal-title":"Int. J. Neuropsychopharmacol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Wang, H., Liang, S., Burgdorf, J., Wess, J., and Yeomans, J. (2008). Ultrasonic vocalizations induced by sex and amphetamine in M2, M4, M5 muscarinic and D2 dopamine receptor knockout mice. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0001893"},{"key":"ref_43","unstructured":"R Core Team (2021). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing."},{"key":"ref_44","unstructured":"Kassambara, R. (2021, November 13). Rstatix: Pipe-Friendly Framework for Basic Statistical Tests. Available online: https:\/\/CRAN.R-project.org\/package=rstatix."},{"key":"ref_45","unstructured":"Lenth, R. (2021, November 13). Emmeans: Estimated Marginal Means, AKA least-Square Means. Available online: https:\/\/CRAN.R-project.org\/package=emmeans."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v067.i01","article-title":"Fitting Linear Mixed-Effects Models Using Lme4","volume":"67","author":"Bates","year":"2015","journal-title":"J. Stat. Softw."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v082.i13","article-title":"LmerTest Package: Tests in Linear Mixed Effects Models","volume":"82","author":"Kuznetsova","year":"2017","journal-title":"J. Stat. Softw."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Elkin, L.A., Kay, M., Higgins, J.J., and Wobbrock, J.O. (2021, January 10\u201314). An Aligned Rank Transform Procedure for Multifactor Contrast Tests. Proceedings of the ACM Symposium on User Interface Software and Technology (UIST 2021), Virtual Event.","DOI":"10.1145\/3472749.3474784"},{"key":"ref_49","unstructured":"Kay, M., Elkin, L., Higgins, J.J., and Wobbrock, J.O. (2021, November 13). ARTool: Aligned Rank Transform for Nonparametric Factorial ANOVAs. R package version 0.11.1. Available online: https:\/\/github.com\/mjskay\/ARTool."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Wobbrock, J.O., Findlater, L., Gergle, D., and Higgins, J.J. (2011, January 7\u201312). The Aligned Rank Transform for Nonparametric Factorial Analyses Using Only Anova Procedures. Proceedings of the ACM Conference on Human Factors in Computing Systems (CHI 2011), Vancouver, BC, USA.","DOI":"10.1145\/1978942.1978963"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/bs.apha.2021.03.006","article-title":"Epigenetics, estrogenic endocrine-disrupting chemicals (EDCs), and the brain","volume":"92","author":"Streifer","year":"2021","journal-title":"Adv. Pharmacol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1210\/me.2013-1270","article-title":"Dynamic postnatal developmental and sex-specific neuroendocrine effects of prenatal polychlorinated biphenyls in rats","volume":"28","author":"Walker","year":"2014","journal-title":"Mol. Endocrinol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1620\/tjem.206.327","article-title":"Endocrine disruptive effects of polychlorinated biphenyls on the thyroid gland in female rats","volume":"206","author":"Kilic","year":"2005","journal-title":"Tohoku J. Exp. Med."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.toxlet.2004.04.009","article-title":"Suppression of aromatase activity in vitro by PCBs 28 and 105 and Aroclor 1221","volume":"152","author":"Woodhouse","year":"2004","journal-title":"Toxicol. Lett."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1126\/science.1063443","article-title":"Epigenetic reprogramming in mammalian development","volume":"293","author":"Reik","year":"2001","journal-title":"Science"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1007\/s11154-007-9048-y","article-title":"Estrogenic environmental endocrine-disrupting chemical effects on reproductive neuroendocrine function and dysfunction across the life cycle","volume":"8","author":"Dickerson","year":"2007","journal-title":"Rev. Endocr. Metab. Disord."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.taap.2009.04.023","article-title":"Chronic treatment with polychlorinated biphenyls (PCB) during pregnancy and lactation in the rat. Part 2: Effects on reproductive parameters, on sex behavior, on memory retention and on hypothalamic expression of aromatase and 5alpha-reductases in the offspring","volume":"239","author":"Colciago","year":"2009","journal-title":"Toxicol. Appl. Pharmacol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/j.neuro.2008.12.008","article-title":"Female sexual behavior, estrous cycle and gene expression in sexually dimorphic brain regions after pre- and postnatal exposure to endocrine active UV filters","volume":"30","author":"Faass","year":"2009","journal-title":"Neurotoxicology"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.yhbeh.2008.08.009","article-title":"Estrogen treatment during development alters adult partner preference and reproductive behavior in female laboratory rats","volume":"55","author":"Henley","year":"2009","journal-title":"Horm. Behav."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/j.physbeh.2008.07.016","article-title":"Exposure to PCB 77 affects partner preference but not sexual behavior in the female rat","volume":"95","author":"Cummings","year":"2008","journal-title":"Physiol. Behav."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Hull, E.M., Meisel, R.L., and Sachs, B.D. (2002). Male Sexual Behavior. Hormones, Brain and Behavior, Elsevier.","DOI":"10.1016\/B978-012532104-4\/50003-2"},{"key":"ref_62","first-page":"28","article-title":"Types and functions of ultrasonic vocalizations in laboratory rats and mice","volume":"46","author":"Portfors","year":"2007","journal-title":"J. Am. Assoc. Lab. Anim. Sci."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1111\/j.1749-6632.1986.tb27996.x","article-title":"The role of ultrasonic vocalizations in the regulation of reproduction in rats","volume":"474","author":"Barfield","year":"1986","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/0031-9384(89)90123-6","article-title":"Playback of female rat ultrasonic vocalizations during sexual behavior","volume":"45","author":"White","year":"1989","journal-title":"Physiol. Behav."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/j.bbr.2008.08.037","article-title":"Repeated intravenous amphetamine exposure: Rapid and persistent sensitization of 50-kHz ultrasonic trill calls in rats","volume":"197","author":"Ahrens","year":"2009","journal-title":"Behav. Brain Res."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1016\/j.physbeh.2007.11.031","article-title":"Effects of experience and context on 50-kHz vocalizations in rats","volume":"93","author":"Houx","year":"2008","journal-title":"Physiol. Behav."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1002\/dev.21998","article-title":"Sex differences in the acoustic featuRes. of social play-induced 50-kHz ultrasonic vocalizations: A detailed spectrographic analysis in wild-type Sprague\u2013Dawley and Cacna1c haploinsufficient rats","volume":"63","author":"Kisko","year":"2021","journal-title":"Dev. Psychobiol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1006\/hbeh.1997.1367","article-title":"Inhibition of male sexual behavior by intracranial implants of the protein synthesis inhibitor anisomycin into the medial preoptic area of the rat","volume":"31","author":"McGinnis","year":"1997","journal-title":"Horm. Behav."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"722456","DOI":"10.3389\/fnbeh.2021.722456","article-title":"Anticipatory 50-kHz Precontact Ultrasonic Vocalizations and Sexual Motivation: Characteristic Pattern of Ultrasound Subtypes in an Individual Analyzed Profile","volume":"15","author":"Rolf","year":"2021","journal-title":"Front. Behav. Neurosci."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Brudzynski, S.M. (2021). Biological Functions of Rat Ultrasonic Vocalizations, Arousal Mechanisms, and Call Initiation. Brain Sci., 11.","DOI":"10.3390\/brainsci11050605"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1016\/0031-9384(92)90116-J","article-title":"Variations in scent marking and ultrasonic vocalizations by Long-Evans rats across the estrous cycle","volume":"51","author":"Matochik","year":"1992","journal-title":"Physiol. Behav."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"27001","DOI":"10.1289\/EHP4977","article-title":"Lineage- and Sex-Dependent Behavioral and Biochemical Transgenerational Consequences of Developmental Exposure to Lead, Prenatal Stress, and Combined Lead and Prenatal Stress in Mice","volume":"128","author":"Sobolewski","year":"2020","journal-title":"Environ. 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