Impact of low-dose oral exposure to bisphenol A (BPA) on Juvenile and adult rat exploratory and anxiety behavior: A CLARITY-BPA Consortium Study

Toxicological Sciences

Volumn 148, Issue 2, 2015, Pages 341-354

  Rebuli, Meghan E ^a   Camacho, Luísa ^b   Adonay, Maria E ^a   Reif, David M ^a   Aylor, David L ^a   Patisaul, Heather B ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

anxiety; behavior; bisphenol A; BPA; brain; CLARITY; EDC; endocrine disruption; exploratory activity; plastic; sexually dimorphic

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ENDOCRINE DISRUPTOR; ETHINYLESTRADIOL; BENZHYDRYL DERIVATIVE; PHENOL DERIVATIVE;

ADULT; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIOR ASSESSMENT; BRAIN DEVELOPMENT; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; ELEVATED ZERO MAZE TEST; EXPLORATORY BEHAVIOR; EXPOSURE; FEMALE; JUVENILE ANIMAL; LACTATION; MALE; NONHUMAN; OPEN FIELD BEHAVIOR; PERINATAL PERIOD; PHENOTYPE; PREGNANCY; SEX DIFFERENCE; ADVERSE EFFECTS; AGE; ANIMAL; ANIMAL BEHAVIOR; CHEMICALLY INDUCED; DOSE RESPONSE; DRUG EFFECTS; GESTATIONAL AGE; MATERNAL EXPOSURE; MOTOR ACTIVITY; NEUROTOXICITY SYNDROMES; PRENATAL EXPOSURE; PSYCHOLOGY; RISK ASSESSMENT; SPRAGUE DAWLEY RAT;

AGE FACTORS; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BENZHYDRYL COMPOUNDS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCRINE DISRUPTORS; EXPLORATORY BEHAVIOR; FEMALE; GESTATIONAL AGE; LACTATION; MALE; MATERNAL EXPOSURE; MOTOR ACTIVITY; NEUROTOXICITY SYNDROMES; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS, SPRAGUE-DAWLEY; RISK ASSESSMENT; SEX FACTORS;

EID: 84952932385     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfv163     Document Type: Article

References (106)

1. Adewale, H. B., Todd, K. L., Mickens, J. A., and Patisaul, H. B. (2011). The impact of neonatal bisphenol-A exposure on sexually dimorphic hypothalamic nuclei in the female rat. Neurotoxicology 32, 38-49.
2. Albani, S.H., Andrawis, M. M., Abella, R. J., Fulghum, J.T., Vafamand, N., and Dumas, T. C. (2015). Behavior in the elevated plus maze is differentially affected by testing conditions in rats under and over threeweeks of age. Front. Behav. Neurosci. 9, 31.
3. Anderson, E. E. (1940). The sex hormones and emotional behavior: I. The effect of sexual receptivity upon timidity in the female rat. Pedagogical Semin. J. Genet. Psychol. 56, 149-158.
4. Anderson, O. S., Peterson, K. E., Sanchez, B. N., Zhang, Z., Mancuso, P., and Dolinoy, D. C. (2013). Perinatal bisphenol A exposure promotes hyperactivity, lean body composition, and hormonal responses across the murine life course. FASEB J. 27, 1784-1792.
5. Archer, J. (1975). Rodent sex differences in emotional and related behavior. Behav. Biol. 14, 451-479.
6. Bailey, K. R., and Crawley, J. N. (2009). Anxiety-related behaviors in mice. In Methods of Behavior Analysis in Neuroscience, 2nd ed. (J. J. Buccafusco, Ed.). CRC Press, Boca Raton, FL.
7. Bailey, M., and Silver, R. (2014). Sex differences in circadian timing systems: Implications for disease. Front. Neuroendocrinol. 35, 111-139.
8. Bell, R., Duke, A. A., Gilmore, P. E., Page, D., and Begue, L. (2014). Anxiolytic-like effects observed in rats exposed to the elevated zero-maze following treatment with 5-HT2/5-HT3/5-HT4 ligands. Sci. Rep. 4, 3881.
9. Beronius, A., Ruden, C., Hakansson, H., and Hanberg, A. (2010). Risk to all or none? A comparative analysis of controversies in the health risk assessment of Bisphenol A. Reprod. Toxicol. 29, 132-146.
10. Birnbaum, L. S., Bucher, J. R., Collman, G. W., Zeldin, D. C., Johnson, A. F., Schug, T. T., and Heindel, J. J. (2012). Consortium-based science: The NIEHS's multipronged, collaborative approach to assessing the health effects of bisphenol A. Environ. Health. Perspect. 120, 1640-1644.
11. Boctor, S. Y., and Ferguson, S. A. (2010). Altered adult locomotor activity in rats from phencyclidine treatment on postnatal days 7, 9 and 11, but not repeated ketamine treatment on postnatal day 7. Neurotoxicology 31, 42-54.
12. Braun, A. A., Skelton, M. R., Vorhees, C. V., and Williams, M. T. (2011a). Comparison of the elevated plus and elevated zero mazes in treated and untreated male Sprague-Dawley rats: Effects of anxiolytic and anxiogenic agents. Pharmacol. Biochem. Behav. 97, 406-415.
13. Braun, J. M., Kalkbrenner, A. E., Calafat, A. M., Yolton, K., Ye, X., Dietrich, K. N., and Lanphear, B. P. (2011b). Impact of earlylife bisphenol A exposure on behavior and executive function in children. Pediatrics 128, 873-882.
14. Bronstein, P. M., Neiman, H., Wolkoff, F. D., and Levine, M. J. (1974). The development of habituation in the rat. Anim. Learn. Behav. 2, 92-96.
15. Calafat, A. M., Ye, X., Wong, L. Y., Reidy, J. A., and Needham, L. L. (2008). Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ. Health. Perspect. 116, 39-44.
16. Camacho, L., Basavarajappa, M. S., Chang, C. W., Han, T., Kobets, T., Koturbash, I., Surratt, G., Lewis, S. M., Vanlandingham, M. M., Fuscoe, J. C., et al. (2015). Effects of oral exposure to bisphenol A on gene expression and global genomic DNA methylation in the prostate, female mammary gland, and uterus of NCTR Sprague-Dawley rats. Food Chem. Toxicol. 81, 92-103.
17. Cao, J., Rebuli, M. E., Rogers, J., Todd, K. L., Leyrer, S. M., Ferguson, S. A., and Patisaul, H. B. (2013). Prenatal bisphenol A exposure alters sex-specific estrogen receptor expression in the neonatal rat hypothalamus and amygdala. Toxicol. Sci. 133, 157-173.
18. Casas, M., Chevrier, C., Hond, E. D., Fernandez, M. F., Pierik, F., Philippat, C., Slama, R., Toft, G., Vandentorren, S., Wilhelm, M., et al. (2013). Exposure to brominated flame retardants, perfluorinated compounds, phthalates and phenols in European birth cohorts: ENRIECO evaluation, first human biomonitoring results, and recommendations. Int. J. Hyg. Environ. Health. 216, 230-242.
19. Chadman, K. K., Yang, M., and Crawley, J. N. (2009). Criteria for validating mouse models of psychiatric diseases. Am. J. Med. Genet. B Neuropsychiatr. Genet. 150B, 1-11.
20. Chapin, R. E., Adams, J., Boekelheide, K., Gray, L. E., Jr., Hayward, S. W., Lees, P. S., McIntyre, B. S., Portier, K. M., Schnorr, T. M., Selevan, S. G., et al. (2008). NTP-CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A. Birth Defects Res. B Dev. Reprod. Toxicol. 83, 157-395.
21. Churchwell, M. I., Camacho, L., Vanlandingham, M. N., Twaddle, N. C., Sepehr, E., Delclos, K. B., Fisher, J. W., and Doerge, D. R. (2014). Comparison of life-stage-dependent internal dosimetry for bisphenol A, ethinyl estradiol, a reference estrogen, and endogenous estradiol to test an estrogenic model of action in Sprague-Dawley rats. Toxicol. Sci. 139, 4-20.
22. Cohen, J., Cohen, P., Stephen, G. W., and Aiken, L. S. (2002). Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences, 3rd ed. Lawrence Erlbaum Associates, Inc 10 Industrial Avenue Mahwah, NJ 07430.
23. Cox, K. H., Gatewood, J. D., Howeth, C., and Rissman, E. F. (2010). Gestational exposure to bisphenol A and cross-fostering affect behaviors in juvenile mice. Horm. Behav. 58, 754-761.
24. Cryan, J. F., and Sweeney, F. F. (2011). The age of anxiety: Role of animal models of anxiolytic action in drug discovery. Br. J. Pharmacol. 164, 1129-1161.
25. Delclos, K. B., Camacho, L., Lewis, S. M., Vanlandingham, M. M., Latendresse, J. R., Olson, G. R., Davis, K. J., Patton, R. E., Gamboa da Costa, G., Woodling, K. A., et al. (2014). Toxicity evaluation of bisphenol A administered by gavage to Sprague Dawley rats from gestation day 6 through postnatal day 90. Toxicol. Sci. 139, 174-197.
26. Diaz-Veliz, G., Alarcon, T., Espinoza, C., Dussaubat, N., and Mora, S. (1997). Ketanserin and anxiety levels: Influence of gender, estrous cycle, ovariectomy and ovarian hormones in female rats. Pharmacol. Biochem. Behav. 58, 637-642.
27. Doerge, D. R., Vanlandingham, M., Twaddle, N. C., and Delclos, K. B. (2010). Lactational transfer of bisphenol A in Sprague-Dawley rats. Toxicol. Lett. 199, 372-376.
28. EFSA (2015). EFSA panel on food contact materials, enzymes, flavourings and processing acids (CEF). EFSA J. 13, 3978.
29. Ehrlich, S., Calafat, A. M., Humblet, O., Smith, T., and Hauser, R. (2014). Handling of thermal receipts as a source of exposure to bisphenol A. JAMA 311, 859-860.
30. EPA (1993). Bisphenol A, Integrated Risk Information System. Available at: http://www.epa.gov/ncea/iris/subst/0356.htm. Accessed March 18 2014.
31. FAO/WHO (2011). Toxicological and health aspects of bisphenol A: Report of Joint FAO/WHO Expert Meeting and Report of Stakeholder Meeting on Bisphenol A. In World Health Organization. http://whqlibdoc.who.int/publications/2011/97892141564274_eng.pdf
32. Farabollini, F., Porrini, S., Della Seta, D., Bianchi, F., and Dessi-Fulgheri, F. (2002). Effects of perinatal exposure to bisphenol A on sociosexual behavior of female and male rats. Environ. Health. Perspect. 110(Suppl. 3), 409-414.
33. Faul, F., Erdfelder, E., Buchner, A., and Lang, A. G. (2009). Statistical power analyses using G*Power 3.1: Tests for correlation and regression analyses. Behav. Res. Methods 41, 1149-1160.
34. FDA (2012). Bisphenol A (BPA): Use in food contact application. In (F. a. D. Administration, Ed.). http://www.fda.gov/downloads/Food/IngredientsPackagingLabeling/FoodAdditivesIngredients/UCM424011.pdf
35. Ferguson, S. A., and Berry, K. J. (2010). Chronic oral treatment with isotretinoin alters measures of activity but not anxiety in male and female rats. Neurotoxicol. Teratol. 32, 573-578.
36. Ferguson, S. A., and Boctor, S. Y. (2010). Cocaine responsiveness or anhedonia in rats treated with methylphenidate during adolescence. Neurotoxicol. Teratol. 32, 432-442.
37. Ferguson, S. A., Law, C. D., Jr., and Abshire, J. S. (2011). Developmental treatment with bisphenol A or ethinyl estradiol causes few alterations on early preweaning measures. Toxicol. Sci. 124, 149-160.
38. Ferguson, S. A., Law, C. D., and Abshire, J. S. (2012). Developmental treatment with bisphenol A causes few alterations on measures of postweaning activity and learning. Neurotoxicol. Teratol. 34, 598-606.
39. Ferguson, S. A., Law, C. D., and Kissling, G. E. (2014). Developmental treatment with ethinyl estradiol, but not bisphenol A, causes alterations in sexually dimorphic behaviors in male and female Sprague Dawley rats. Toxicol. Sci. 140, 374-392.
40. Frye, C. A., Petralia, S. M., and Rhodes, M. E. (2000). Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3alpha, 5alpha-THP. Pharmacol. Biochem. Behav. 67, 587-596.
41. Gioiosa, L., Parmigiani, S., Vom Saal, F. S., and Palanza, P. (2013). The effects of bisphenol A on emotional behavior depend upon the timing of exposure, age and gender in mice. Horm. Behav. 63, 598-605.
42. Goma, M., and Tobena, A. (1978). Reliability of various measures obtained in open-field test. Psychol. Rep. 43, 1123-1128.
43. Goncalves, C. R., Cunha, R. W., Barros, D. M., and Martinez, P. E. (2010). Effects of prenatal and postnatal exposure to a low dose of bisphenol A on behavior and memory in rats. Environ. Toxicol. Pharmacol. 30, 195-201.
44. Gould, T. D., Kovacsics, D. T., and C. E. (2010). The open field test. In Mood and Anxiety Related Phenotypes in Mice (Todd D. Gould, Ed.). Humana Press, New York City, NY.
45. Harley, K. G., Gunier, R. B., Kogut, K., Johnson, C., Bradman, A., Calafat, A. M., and Eskenazi, B. (2013). Prenatal and early childhood bisphenol A concentrations and behavior in school-aged children. Environ. Res. 126, 43-50.
46. Haseman, J. K., Bailer, A. J., Kodell, R. L., Morris, R., and Portier, K. (2001). Statistical issues in the analysis of low-dose endocrine disruptor data. Toxicol. Sci. 61, 201-210.
47. Heindel, J. J., Newbold, R. R., Bucher, J. R., Camacho, L., Delclos, K. B., Lewis, S. M., Vanlandingham, M., Churchwell, M. I., Twaddle, N. C., McLellen, M., et al. (2015). NIEHS/FDA CLARITY-BPA research program update. Reprod. Toxicol. 58, 33-44.
48. Hogg, S. (1996). A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol. Biochem. Behav. 54, 21-30.
49. Jasarevic, E., Sieli, P. T., Twellman, E. E., Welsh, T. H., Jr., Schachtman, T. R., Roberts, R. M., Geary, D. C., and Rosenfeld, C. S. (2011). Disruption of adult expression of sexually selected traits by developmental exposure to bisphenol A. Proc. Natl. Acad. Sci. U S A 108, 11715-11720.
50. Jasarevic, E., Williams, S. A., Vandas, G. M., Ellersieck, M. R., Liao, C., Kannan, K., Roberts, R. M., Geary, D. C., and Rosenfeld, C. S. (2013). Sex and dose-dependent effects of developmental exposure to bisphenol A on anxiety and spatial learning in deer mice (Peromyscus maniculatus bairdii) offspring. Horm. Behav. 63, 180-189.
51. Jones, B. A., Shimell, J. J., and Watson, N. V. (2010). Pre-and postnatal bisphenol A treatment results in persistent deficits in the sexual behavior of male rats, but not female rats, in adulthood. Horm. Behav. 59, 246-251.
52. Jones, B. A., andWatson, N. V. (2012). Perinatal BPA exposure demasculinizesmales in measures of affect but has no effect on water maze learning in adulthood. Horm. Behav. 61, 605-610.
53. Kinch, C. D., Ibhazehiebo, K., Jeong, J. H., Habibi, H. R., and Kurrasch, D. M. (2015). Low-dose exposure to bisphenol A and replacement bisphenol S induces precocious hypothalamic neurogenesis in embryonic zebrafish. Proc. Natl. Acad. Sci. U S A 112, 1475-1480.
54. Kundakovic, M., Gudsnuk, K., Franks, B., Madrid, J., Miller, R. L., Perera, F. P., and Champagne, F. A. (2013). Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proc. Natl. Acad. Sci. U S A 110, 9956-9961.
55. Lakind, J. S., and Naiman, D. Q. (2011). Daily intake of bisphenol A and potential sources of exposure: 2005-2006 National Health and Nutrition Examination Survey. J. Expo. Sci. Environ. Epidemiol. 21, 272-279.
56. Laviola, G., Renna, G., Bignami, G., and Cuomo, V. (1988). Ontogenetic and pharmacological dissociation of various components of locomotor activity and habituation in the rat. Int. J. Dev. Neurosci. 6, 431-438.
57. Leranth, C., Hajszan, T., Szigeti-Buck, K., Bober, J., and MacLusky, N. J. (2008a). Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proc. Natl. Acad. Sci. U S A 105, 14187-14191.
58. Leranth, C., Szigeti-Buck, K., Maclusky, N. J., and Hajszan, T. (2008b). Bisphenol A prevents the synaptogenic response to testosterone in the brain of adult male rats. Endocrinology 149, 988-994.
59. Levine, M., and Ensom, M. H. (2001). Post hoc power analysis: An idea whose time has passed? Pharmacotherapy 21, 405-409.
60. Lewis, S. M., Lee, F. W., Ali, A. A., Allaben, W. T., Weis, C. C., and Leakey, J. E. (2010). Modifying a displacement pump for oral gavage dosing of solution and suspension preparations to adult and neonatal mice. Lab. Anim. (NY) 39, 149-154.
61. Li, D., Zhou, Z., Qing, D., He, Y., Wu, T., Miao, M., Wang, J., Weng, X., Ferber, J. R., Herrinton, L. J., et al. (2010). Occupational exposure to bisphenol-A (BPA) and the risk of self-reported male sexual dysfunction. Hum. Reprod. 25, 519-527.
62. Luo, G., Wei, R., Niu, R., Wang, C., and Wang, J. (2013). Pubertal exposure to bisphenol A increases anxiety-like behavior and decreases acetylcholinesterase activity of hippocampus in adult male mice. Food Chem. Toxicol. 60, 177-180.
63. Markham, J. A., and Koenig, J. I. (2011). Prenatal stress: Role in psychotic and depressive diseases. Psychopharmacology (Berl) 214, 89-106.
64. Masur, J., Schutz, M. T., and Boerngen, R. (1980). Gender differences in open-field behavior as a function of age. Dev. Psychobiol. 13, 107-110.
65. Matsuda, S., Matsuzawa, D., Ishii, D., Tomizawa, H., Sutoh, C., Nakazawa, K., Amano, K., Sajiki, J., and Shimizu, E. (2012). Effects of perinatal exposure to low dose of bisphenol A on anxiety like behavior and dopamine metabolites in brain. Prog. Neuropsychopharmacol. Biol. Psychiatry. 39, 273-279.
66. Mileva, G., Baker, S. L., Konkle, A. T., and Bielajew, C. (2014). Bisphenol-A: Epigenetic reprogramming and effects on reproduction and behavior. Int. J. Environ. Res. Public Health 11, 7537-7561.
67. Mora, S., Dussaubat, N., and Diaz-Veliz, G. (1996). Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 21, 609-620.
68. Nakagami, A., Negishi, T., Kawasaki, K., Imai, N., Nishida, Y., Ihara, T., Kuroda, Y., Yoshikawa, Y., and Koyama, T. (2009). Alterations in male infant behaviors towards its mother by prenatal exposure to bisphenol A in cynomolgus monkeys (Macaca fascicularis) during early suckling period. Psychoneuroendocrinology 34, 1189-1197.
69. Nakamura, K., Itoh, K., Dai, H., Han, L., Wang, X., Kato, S., Sugimoto, T., and Fushiki, S. (2012). Prenatal and lactational exposure to low-doses of bisphenol A alters adult mice behavior. Brain. Dev. 34, 57-63.
70. NTP (2008). NTP-CERHR monograph on the potential human reproductive and developmental effects of bisphenol A. In (Vol. 08-5994). NIH. http://ntp.niehs.nih.gov/ntp/ohat/bisphenol/bisphenol.pdf.
71. Padilla, E., Barrett, D., Shumake, J., and Gonzalez-Lima, F. (2009). Strain, sex, and open-field behavior: Factors underlying the genetic susceptibility to helplessness. Behav. Brain. Res. 201, 257-264.
72. Palanza, P., Gioiosa, L., vom Saal, F. S., and Parmigiani, S. (2008). Effects of developmental exposure to bisphenol A on brain and behavior in mice. Environ. Res. 108, 150-157.
73. Patisaul, H. B., and Bateman, H. L. (2008). Neonatal exposure to endocrine active compounds or an ERbeta agonist increases adult anxiety and aggression in gonadally intact male rats. Horm. Behav. 53, 580-588.
74. Patisaul, H. B., Blum, A., Luskin, J. R., and Wilson, M. E. (2005). Dietary soy supplements produce opposite effects on anxiety in intact male and female rats in the elevated plus-maze. Behav. Neurosci. 119, 587-594.
75. Patisaul, H. B., Fortino, A. E., and Polston, E. K. (2007). Differential disruption of nuclear volume and neuronal phenotype in the preoptic area by neonatal exposure to genistein and bisphenol-A. Neurotoxicology 28, 1-12.
76. Patisaul, H. B., Fortino, A. E., and Polston, E. K. (2006). Neonatal genistein or bisphenol-A exposure alters sexual differentiation of the AVPV. Neurotoxicol. Teratol. 28, 111-118.
77. Patisaul, H. B., and Polston, E. K. (2008). Influence of endocrine active compounds on the developing rodent brain. Brain Res. Rev. 57, 352-362.
78. Patisaul, H. B., Sullivan, A. W., Radford, M. E., Walker, D. M., Adewale, H. B., Winnik, B., Coughlin, J. L., Buckley, B., and Gore, A. C. (2012). Anxiogenic effects of developmental bisphenol A exposure are associated with gene expression changes in the juvenile rat amygdala and mitigated by soy. PLoS One 7, e43890.
79. Pellow, S., Chopin, P., File, S. E., and Briley, M. (1985). Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 14, 149-167.
80. Perera, F., Vishnevetsky, J., Herbstman, J. B., Calafat, A. M., Xiong, W., Rauh, V., and Wang, S. (2012). Prenatal bisphenol A exposure and child behavior in an inner-city cohort. Environ. Health. Perspect. 120, 1190-1194.
81. Team R. (2014). R: A Language and Environment for Statistical Computing. Vienna, Austria http://cran.r-project.org/doc/manuals/fullrefman.pdf.
82. Rebuli, M. E., Cao, J., Sluzas, E., Delclos, K. B., Camacho, L., Lewis, S. M., Vanlandingham, M. M., and Patisaul, H. B. (2014). Investigation of the effects of subchronic low dose oral exposure to bisphenol A (BPA) and ethinyl estradiol (EE) on estrogen receptor expression in the juvenile and adult female rat hypothalamus. Toxicol. Sci. 140, 190-203.
83. Rochester, J. R. (2013). Bisphenol A and human health: A review of the literature. Reprod. Toxicol. 42, 132-155.
84. Rosenfeld, C. S. (2012). Effects of maternal diet and exposure to bisphenol A on sexually dimorphic responses in conceptuses and offspring. Reprod. Domest. Anim. 47(Suppl. 4), 23-30.
85. Russo, S. J., Murrough, J. W., Han, M. H., Charney, D. S., and Nestler, E. J. (2012). Neurobiology of resilience. Nat. Neurosci. 15, 1475-1484.
86. Schug, T. T., Heindel, J. J., Camacho, L., Delclos, K. B., Howard, P., Johnson, A. F., Aungst, J., Keefe, D., Newbold, R., Walker, N. J., et al. (2013). A new approach to synergize academic and guideline-compliant research: The CLARITY-BPA research program. Reprod. Toxicol. 40, 35-40.
87. Shepherd, J. K., Grewal, S. S., Fletcher, A., Bill, D. J., and Dourish, C. T. (1994). Behavioural and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacology (Berl) 116, 56-64.
88. Silver, R., and Kriegsfeld, L. J. (2014). Circadian rhythms have broad implications for understanding brain and behavior. Eur. J. Neurosci. 39, 1866-1880.
89. Simpson, J., Ryan, C., Curley, A., Mulcaire, J., and Kelly, J. P. (2012). Sex differences in baseline and drug-induced behavioural responses in classical behavioural tests. Prog. Neuropsychopharmacol. Biol. Psychiatry 37, 227-236.
90. Slob, A. K., Huizer, T., and Van der Werff ten Bosch, J. J. (1986). Ontogeny of sex differences in open-field ambulation in the rat. Physiol. Behav. 37, 313-315.
91. Sullivan, A. W., Beach, E. C., Stetzik, L. A., Perry, A., D'Addezio, A. S., Cushing, B. S., and Patisaul, H. B. (2014). A novel model for neuroendocrine toxicology: Neurobehavioral effects of BPA exposure in a prosocial species, the prairie vole (Microtus ochrogaster). Endocrinology 155, 3867-3881.
92. Thigpen, J. E., Setchell, K. D., Kissling, G. E., Locklear, J., Caviness, G. F., Whiteside, T., Belcher, S. M., Brown, N. M., Collins, B. J., Lih, F. B., et al. (2013). The estrogenic content of rodent diets, bedding, cages, and water bottles and its effect on bisphenol A studies. J. Am. Assoc. Lab. Anim. Sci. 52, 130-141.
93. Thigpen, J. E., Setchell, K. D., Padilla-Banks, E., Haseman, J. K., Saunders, H. E., Caviness, G. F., Kissling, G. E., Grant, M. G., and Forsythe, D. B. (2007). Variations in phytoestrogen content between different mill dates of the same diet produces significant differences in the time of vaginal opening in CD-1 mice and F344 rats but not in CD Sprague-Dawley rats. Environ. Health. Perspect. 115, 1717-1726.
94. Tian, Y. H., Baek, J. H., Lee, S. Y., and Jang, C. G. (2010). Prenatal and postnatal exposure to bisphenol A induces anxiolytic behaviors and cognitive deficits in mice. Synapse 64, 432-439.
95. Valles, F. P. (1976). Age factors in sex differences in open-field activity of rats. Anim. Learn. Behav. 4, 457-460.
96. Viberg, H., Fredriksson, A., Buratovic, S., and Eriksson, P. (2011). Dose-dependent behavioral disturbances after a single neonatal Bisphenol A dose. Toxicology 290, 187-194.
97. vom Saal, F. S., Akingbemi, B. T., Belcher, S. M., Birnbaum, L. S., Crain, D. A., Eriksen, M., Farabollini, F., Guillette, L. J., Jr., Hauser, R., Heindel, J. J., et al. (2007). Chapel Hill bisphenol A expert panel consensus statement: Integration of mechanisms, effects in animals and potential to impact human health at current levels of exposure. Reprod. Toxicol. 24, 131-138.
98. von Goetz, N., Wormuth, M., Scheringer, M., and Hungerbuhler, K. (2010). Bisphenol A: How the most relevant exposure sources contribute to total consumer exposure. Risk. Anal. 30, 473-487.
99. Wagenmakers, E. J., Verhagen, J., Ly, A., Bakker, M., Lee, M. D., Matzke, D., Rouder, J. N., and Morey, R. D. (2014). A power fallacy. Behav. Res. Methods.
100. Walf, A. A., and Frye, C. A. (2007). The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat. Protoc. 2, 322-328.
101. Weiss, S. M., Wadsworth, G., Fletcher, A., and Dourish, C. T. (1998). Utility of ethological analysis to overcome locomotor confounds in elevated maze models of anxiety. Neurosci. Biobehav. Rev. 23, 265-271.
102. Wolstenholme, J. T., Goldsby, J. A., and Rissman, E. F. (2013). Transgenerational effects of prenatal bisphenol A on social recognition. Horm. Behav. 64, 833-839.
103. Wolstenholme, J. T., Rissman, E. F., and Connelly, J. J. (2011a). The role of Bisphenol A in shaping the brain, epigenome and behavior. Horm. Behav. 59, 296-305.
104. Wolstenholme, J. T., Taylor, J. A., Shetty, S. R., Edwards, M., Connelly, J. J., and Rissman, E. F. (2011b). Gestational exposure to low dose bisphenol A alters social behavior in juvenile mice. PLoS One 6, e25448.
105. Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R., Ueda, M., Block, G. D., Sakaki, Y., Menaker, M., and Tei, H. (2000). Resetting central and peripheral circadian oscillators in transgenic rats. Science 288, 682-685.
106. Yeo, M., Berglund, K., Hanna, M., Guo, J. U., Kittur, J., Torres, M. D., Abramowitz, J., Busciglio, J., Gao, Y., Birnbaumer, L., et al. (2013). Bisphenol A delays the perinatal chloride shift in cortical neurons by epigenetic effects on the Kcc2 promoter. Proc. Natl. Acad. Sci. U S A 110, 4315-4320.