Sex-specific Enhanced Behavioral Toxicity Induced by Maternal Exposure to a Mixture of Low Dose Endocrine-Disrupting Chemicals
Open accessAbstract
Humans are increasingly and consistently exposed to a variety of endocrine disrupting chemicals (EDCs), chemicals that have been linked to neurobehavioral disorders such as ADHD and autism. Many of such EDCs have been shown to adversely influence brain mesocorticolimbic systems raising the potential for cumulative toxicity. As such, understanding the effects of developmental exposure to mixtures of EDCs is critical to public health protection. Consequently, this study compared the effects of a mixture of four EDCs to their effects alone to examine potential for enhanced toxicity, using behavioral domains and paradigms known to be mediated by mesocorticolimbic circuits (fixed interval (FI) schedule controlled behavior, novel object recognition memory and locomotor activity) in offspring of pregnant mice that had been exposed to vehicle or relatively low doses of four EDCs, atrazine (ATR - 10mg/kg), perfluorooctanoic acid (PFOA - 0.1mg/kg), bisphenol-A (BPA - 50 μg/kg), 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD - 0.25 μg/kg) alone or combined in a mixture (MIX), from gestational day 7 until weaning. EDC-treated males maintained significantly higher horizontal activity levels across three testing sessions, indicative of delayed habituation, whereas no effects were found in females. Statistically significant effects of MIX were seen in males, but not females, in the form of increased FI response rates, in contrast to reductions in response rate with ATR, BPA and TCDD, and reduced short term memory in the novel object recognition paradigm. MIX also reversed the typically lower neophobia levels of males compared to females. With respect to individual EDCs, TCDD produced notable increases in FI response rates in females, and PFOA significantly increased ambulatory locomotor activity in males. Collectively, these findings show the potential for enhanced behavioral effects of EDC mixtures in males and underscore the need for animal studies to fully investigate mixtures, including chemicals that converge on common physiological substrates to examine potential mechanisms of toxicity with full dose effect curves to assist in interpretations of relevant mechanisms.
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
Cites
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?
C57BL/6 mice gestationally exposed to 0.1 mg/kg/day PFOA from GD seven to weaning exhibited hyperactivity.
“The same hyperactivity was exhibited by C57BL/6 mice gestationally exposed to 0.1 mg/kg/day PFOA, from GD seven to weaning (Sobolewski et al., 2014).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Sobolewski et al., 2014
The Methods (Developmental Exposure; page unavailable) describe C57BL/6 mice exposed to 0.1 mg/kg PFOA from gestational day 7 until weaning. The Results (Behavioral Testing; page unavailable) report increased locomotor activity and decreased resting time in PFOA-exposed males, but say significant locomotor changes occurred only in males. The claim omits that sex-specific limitation. (LLM, conf=0.87)
Experimental — accuracy not yet measuredIn Sobolewski et al., a hyperactive phenotype was only observed in PFOA-exposed male mice.
“a hyperactive phenotype was only observed in PFOA-exposed male mice”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Sobolewski et al., 2014
The Discussion (page unavailable) describes significantly increased hyperactivity in PFOA-exposed males. But the Locomotor Behavior results (page unavailable) also report increased horizontal movement in ATR-, TCDD-, and mixture-exposed males. Thus the finding was male-specific, but increased activity was not exclusive to the PFOA group. (LLM, conf=0.87)
Experimental — accuracy not yet measuredIn Sobolewski et al., an increased FI response rate occurred only in TCDD-exposed female mice.
“an increased FI response rate occurred only in TCDD-exposed female mice (Sobolewski et al., 2014).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Sobolewski et al., 2014
The Results (Behavioral Testing; page unavailable) report increased FI response rates in TCDD-exposed females, while TCDD-exposed males had reduced rates. But MIX-exposed males also had increased FI response rates, so the increase did not occur only in TCDD-exposed females. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn Sobolewski et al., animals exposed individually to ATR, BPA, or TCDD experienced decreased response rates in the FI task, highlighting a potentially unique additive effect in mixture-exposed animals.
“animals exposed individually to three of the chemicals in the mixture (ATR, BPA, or TCDD) experienced decreased response rates in the FI task, highlighting a potentially unique additive effect in the mixture exposed animals (Sobolewski et al., 2014).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Sobolewski et al., 2014
The Results (Behavioral Testing; page unavailable) report decreased FI response rates in male offspring exposed individually to ATR, BPA, or TCDD, while mixture-exposed males showed increased rates. The Discussion calls the mixture response a unique alteration, but does not establish that it was additive. The claim also omits the male-specific qualification. (LLM, conf=0.87)
Experimental — accuracy not yet measuredIn Sobolewski et al., only male mice exposed to the chemical mixture exhibited increased response rates in a fixed interval schedule of reward task, indicative of increased impulsivity.
“increased response rates in a fixed interval (FI) schedule of reward task, indicative of increased impulsivity (Sobolewski et al., 2014).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Sobolewski et al., 2014
In Sobolewski et al., only male mice exposed to the chemical mixture exhibited significantly diminished short-term memory in a novel object recognition task.
“only male mice that were exposed to the chemical mixture exhibited significantly diminished short-term memory in a novel object recognition task”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Sobolewski et al., 2014
Developmental EDC exposure can lead to sex-specific changes in behavior.
“Developmental EDC exposure can also lead to sex-specific changes in behavior (Jacobsen et al., 2012; Kundakovic et al., 2013; Sobolewski et al., 2014; Williams et al., 2013).”
From The effects of prenatal PCBs on adult social behavior in rats (2015) · cites this paper as Sobolewski et al., 2014
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Endocrine-Disrupting Chemicals: An Endocrine Society Scientific Statement
Diamanti-Kandarakis, E., Bourguignon, J.-P., Giudice, L. C., Hauser, R., Prins, G. S., Soto, A. M., Zoeller, R. T., & Gore, A. C. (2009) · Endocrine Reviews · doi:10.1210/er.2009-0002 · Cited by 4,585 · see citing works
Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses
Vandenberg, L. N., Colborn, T., Hayes, T. B., Heindel, J. J., Jacobs, D. R., Lee, D.-H., Shioda, T., Soto, A. M., vom Saal, F. S., Welshons, W. V., et al. (2012) · Endocrine Reviews · doi:10.1210/er.2011-1050 · Cited by 3,209 · see citing works
The novel object recognition memory: neurobiology, test procedure, and its modifications
Antunes, M., & Biala, G. (2012) · Cognitive Processing · doi:10.1007/s10339-011-0430-z · Cited by 2,390 · see citing works
Roadmap to embryo implantation: clues from mouse models
Wang, H., & Dey, S. K. (2006) · Nature Reviews Genetics · doi:10.1038/nrg1808 · Cited by 1,302 · see citing works
Competitiveness, risk taking, and violence: the young male syndrome
WILSON, M. I., & Daly, M. (1985) · Ethology and Sociobiology · doi:10.1016/0162-3095(85)90041-x · Cited by 1,242 · see citing works
Saal, F. S. V., & Hughes, C. L. (2005) · Environmental Health Perspectives · doi:10.1289/ehp.7713 · Cited by 1,174 · see citing works
Endocrine disrupting chemicals and disease susceptibility
Schug, T. T., Janesick, A., Blumberg, B., & Heindel, J. J. (2011) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2011.08.007 · Cited by 1,093 · see citing works
The physiology of male sexual behavior
Meisel, R. (1994) · Medical Entomology and Zoology · Cited by 988 · see citing works
Endocrine-Disrupting Chemicals: Associated Disorders and Mechanisms of Action
Coster, S. D., & Larebeke, N. V. (2012) · Journal of Environmental and Public Health · doi:10.1155/2012/713696 · Cited by 622 · see citing works
Johansson, N., Fredriksson, A., & Eriksson, P. (2008) · NeuroToxicology · doi:10.1016/j.neuro.2007.10.008 · Cited by 463 · see citing works
Howdeshell, K. L., Wilson, V. S., Furr, J., Lambright, C. R., Rider, C. V., Blystone, C. R., Hotchkiss, A. K., & Gray, L. E. (2008) · Toxicological Sciences · doi:10.1093/toxsci/kfn077 · Cited by 441 · see citing works
Frye, C., Bo, E., Calamandrei, G., Calzà, L., Dessì‐Fulgheri, F., Fernández, M., Fusani, L., Kah, O., Kajta, M., Le Page, Y., et al. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02229.x · Cited by 431 · see citing works
Mesocorticolimbic Glutamatergic Pathway
Yamaguchi, T., Wang, H.-L., Li, X., Ng, T. H., & Morales, M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1598-11.2011 · Cited by 332 · see citing works
Rubin, B. S., Lenkowski, J. R., Schaeberle, C. M., Vandenberg, L. N., Ronsheim, P. M., & Soto, A. M. (2006) · Endocrinology · doi:10.1210/en.2006-0189 · Cited by 311 · see citing works
Effects of developmental exposure to bisphenol A on brain and behavior in mice
Palanza, P., Gioiosa, L., Saal, F. S. V., & Parmigiani, S. (2008) · Environmental Research · doi:10.1016/j.envres.2008.07.023 · Cited by 276 · see citing works
Palanza, P. L., Howdeshell, K. L., Parmigiani, S., & vom Saal, F. S. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.02110s3415 · Cited by 268 · see citing works
Neurodevelopment and Endocrine Disruption
Colborn, T. (2003) · Environmental Health Perspectives · doi:10.1289/ehp.6601 · Cited by 268 · see citing works
Hoffman, K., Webster, T. F., Weisskopf, M. G., Weinberg, J., & Vieira, V. M. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.1001898 · Cited by 262 · see citing works
Cognitive Effects of Endocrine-Disrupting Chemicals in Animals
Schantz, S. L., & Widholm, J. J. (2001) · Environmental Health Perspectives · doi:10.1289/ehp.011091197 · Cited by 247 · see citing works
Long-term effects of environmental endocrine disruptors on reproductive physiology and behavior
Patisaul, H. B. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.010.2009 · Cited by 245 · see citing works
Stress produced by gavage administration in the rat.
Brown, A. P., Dinger, N., & LEVINE, B. S. (2000) · PubMed · Cited by 202 · see citing works
Evaluating the effects of endocrine disruptors on endocrine function during development.
Bigsby, R. M., Chapin, R. E., Daston, G. P., et al. (1999) · Environmental Health Perspectives · doi:10.1289/ehp.99107s4613 · Cited by 199 · see citing works
de Cock, M., Maas, Y. G. H., & van de Bor, M. (2012) · Acta Paediatrica · doi:10.1111/j.1651-2227.2012.02693.x · Cited by 198 · see citing works
Tian, Y., Baek, J., Lee, S., & Jang, C. (2010) · Synapse · doi:10.1002/syn.20746 · Cited by 197 · see citing works
Ennaceur, A., Michalíková, S., Bradford, A., & Ahmed, S. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.11.006 · Cited by 195 · see citing works
Sex Differences in the Behavioral Response to Spatial and Object Novelty in Adult C57BL/6 Mice.
Frick, K. M., & Gresack, J. E. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.6.1283 · Cited by 190 · see citing works
Gasiewicz, T. A., Geiger, L. E., Rucci, G., et al. (1983) · Drug Metabolism and Disposition · doi:10.1016/s0090-9556(25)08040-7 · Cited by 185 · see citing works
Gestational Exposure to Low Dose Bisphenol A Alters Social Behavior in Juvenile Mice
Wolstenholme, J. T., Taylor, J. A., Shetty, S. R. J., Edwards, M., Connelly, J. J., & Rissman, E. F. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025448 · Cited by 168 · cited 1× · see citing works
“…deficits occur after exposure to EDCs, e.g., BPA, ATR and TCDD, and have been associated with spatial and object memory deficits in developmentally exposed male mice (Belloni et al., 2011, Brouillette and Quirion, 2008, Lin et al., 2013b, Palanza, Gioiosa, 2008, Tian et al., 2010, Xu et al., 2011).”
BackgroundAllen, J. L., Liu, X., Weston, D., Prince, L., Oberdörster, G., Finkelstein, J. N., Johnston, C. J., & Cory-Slechta, D. A. (2014) · Toxicological Sciences · doi:10.1093/toxsci/kfu059 · Cited by 168 · see citing works
Self-citationGioiosa, L., Fissore, E., Ghirardelli, G., Parmigiani, S., & Palanza, P. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.05.006 · Cited by 160 · see citing works
Prenatal Exposure to PFOS or PFOA Alters Motor Function in Mice in a Sex-Related Manner
Onishchenko, N., Fischer, C., Ibrahim, W. N. W., Negri, S., Spulber, S., Cottica, D., & Ceccatelli, S. (2011) · Neurotoxicity research · doi:10.1007/s12640-010-9200-4 · Cited by 152 · see citing works
Performance and exposure indices of rats exposed to low concentrations of lead*1
Cory‐Slechta, D. A. (1985) · Toxicology and Applied Pharmacology · doi:10.1016/0041-008x(85)90292-3 · Cited by 141 · see citing works
Self-citationStudying Toxicants as Single Chemicals: Does this Strategy Adequately Identify Neurotoxic Risk?
Cory‐Slechta, D. A. (2005) · NeuroToxicology · doi:10.1016/j.neuro.2004.12.007 · Cited by 131 · see citing works
Self-citationCoban, A., & Filipov, N. M. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04294.x · Cited by 128 · see citing works
Jašarević, E., Williams, S. A., Vandas, G. M., Ellersieck, M. R., Liao, C., Kannan, K., Roberts, R. M., Geary, D. C., & Rosenfeld, C. S. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.09.009 · Cited by 124 · see citing works
Petersen, S. L., & Barraclough, C. A. (1989) · Brain Research · doi:10.1016/0006-8993(89)90371-5 · Cited by 118 · see citing works
Adriani, W., Seta, D. D., Dessì‐Fulgheri, F., Farabollini, F., & Giovanni Laviola, A. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.5856 · Cited by 117 · see citing works
Aubele, T., Kaufman, R., Montalmant, F., & Kritzer, M. F. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.04.001 · Cited by 115 · see citing works
Kow, L., & Pfaff, D. W. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00189-7 · Cited by 108 · see citing works
Rider, C. V., Wilson, V. S., Howdeshell, K. L., Hotchkiss, A. K., Furr, J., Lambright, C. R., & Gray, L. E. (2009) · Toxicologic Pathology · doi:10.1177/0192623308329478 · Cited by 108 · see citing works
Patisaul, H. B., Sullivan, A. W., Radford, M. E., Walker, D. M., Adewale, H. B., Winnik, B., Coughlin, J. L., Buckley, B., & Gore, A. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043890 · Cited by 106 · see citing works
Suzuki, T., Mizuo, K., Nakazawa, H., Funae, Y., Fushiki, S., Fukushima, S., Shirai, T., & Narita, M. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00935-1 · Cited by 99 · see citing works
Spulber, S., Kilian, P., Wan Ibrahim, W. N., Onishchenko, N., Ulhaq, M., Norrgren, L., Negri, S., Di Tuccio, M., & Ceccatelli, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094227 · Cited by 98 · see citing works
Lin, Z., Dodd, C. A., & Filipov, N. M. (2013) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2013.06.002 · Cited by 96 · see citing works
Social Ecology of Children’s Vulnerability to Environmental Pollutants
Weiss, B., & Bellinger, D. C. (2006) · Environmental Health Perspectives · doi:10.1289/ehp.9101 · Cited by 96 · see citing works
Gioiosa, L., Parmigiani, S., Saal, F. S. V., & Palanza, P. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.02.016 · Cited by 88 · see citing works
Xu, X., Dong, T., Hong, X., Chen, L., & Xie, L. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.04.027 · Cited by 88 · see citing works
Bardullas, U., Giòrdano, M., & Rodríguez, V. M. (2010) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2010.09.001 · Cited by 84 · see citing works
Endo, T., Kakeyama, M., Uemura, Y., Haijima, A., Okuno, H., Bito, H., & Tohyama, C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050741 · Cited by 83 · see citing works
Fetal Exposure to Perfluorinated Compounds and Attention Deficit Hyperactivity Disorder in Childhood
Ode, A., Källén, K., Gustafsson, P., Rylander, L., Jönsson, B., Olofsson, P., Ivarsson, S. A., Lindh, C. H., & Rignell‐Hydbom, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0095891 · Cited by 82 · see citing works
Fenton, S., Reiner, J. L., Nakayama, S., Delinsky, A. D., Stanko, J., Hines, E., White, S., Lindstrom, A., Strynar, M., & Petropoulou, S.-S. E. (2009) · Reproductive Toxicology · doi:10.1016/j.reprotox.2009.02.012 · Cited by 80 · see citing works
Hays, L. E., Carpenter, C. D., & Petersen, S. L. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.02110s3369 · Cited by 80 · see citing works
Petersen, S. L., Cheuk, C., Hartman, R. D., & Barraclough, C. A. (1989) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1989.tb00116.x · Cited by 75 · see citing works
Gray, P., & Brooks, P. J. (1984) · Behavioral Neuroscience · doi:10.1037//0735-7044.98.4.703 · Cited by 75 · see citing works
Rossato, J. I., Radiske, A., Kohler, C. A., Gonzalez, C., Bevilaqua, L. R., Medina, J. H., & Cammarota, M. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.07.012 · Cited by 75 · see citing works
Early exposure to low doses of atrazine affects behavior in juvenile and adult CD1 mice
Belloni, V., Dessì-Fulgheri, F., Zaccaroni, M., Di Consiglio, E., De Angelis, G., Testai, E., Santochirico, M., Alleva, E., & Santucci, D. (2011) · Toxicology · doi:10.1016/j.tox.2010.07.002 · Cited by 74 · see citing works
Inflammation-like glial response in rat brain induced by prenatal PFOS exposure
Zeng, H., Zhang, L., Li, Y., Wang, Y., Xia, W., Lin, Y., Wei, J., & Xu, S. (2010) · NeuroToxicology · doi:10.1016/j.neuro.2010.10.001 · Cited by 71 · see citing works
Rodríguez, V. M., Limón-Pacheco, J. H., Mendoza-Trejo, M. S., et al. (2012) · NeuroToxicology · doi:10.1016/j.neuro.2012.10.012 · Cited by 64 · see citing works
Gray, P., & Brooks, P. J. (1984) · Behavioral Neuroscience · doi:10.1037/0735-7044.98.4.703 · Cited by 63 · see citing works
Developmental Immunotoxicity of Atrazine in Rodents
Rowe, A. M., Brundage, K. M., & Barnett, J. B. (2008) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/j.1742-7843.2007.00175.x · Cited by 61 · see citing works
Sy, H., Wu, S., Wang, W., Chen, C.-H., Huang, Y.-T., Liou, Y., Chiou, C., Pawlak, C. R., & Ho, Y. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.12.020 · Cited by 61 · see citing works
Cory‐Slechta, D. A., O’Mara, D. J., & Brockel, B. J. (1998) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)37655-4 · Cited by 59 · see citing works
Self-citationPerinatal TCDD exposure alters developmental neuroendocrine system
Ahmed, R. G. (2011) · Food and Chemical Toxicology · doi:10.1016/j.fct.2011.03.008 · Cited by 58 · see citing works
Cory‐Slechta, D. A., Stern, S., Weston, D., Allen, J. L., & Liu, S. M. (2010) · Toxicological Sciences · doi:10.1093/toxsci/kfq221 · Cited by 55 · see citing works
Self-citationThe Aryl Hydrocarbon Receptor Pathway and Sexual Differentiation of Neuroendocrine Functions
Petersen, S. L., Krishnan, S., & Hudgens, E. D. (2006) · Endocrinology · doi:10.1210/en.2005-1157 · Cited by 50 · see citing works
Hossain, M. M., & Filipov, N. M. (2008) · Toxicology · doi:10.1016/j.tox.2008.03.007 · Cited by 49 · see citing works
Harte, M., & O'Connor, W. T. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.08.045 · Cited by 47 · see citing works
Narita, M., Miyagawa, K., Mizuo, K., Yoshida, T., & Suzuki, T. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.04.014 · Cited by 45 · see citing works
Mizuo, K., Narita, M., Miyagawa, K., Narita, M., Okuno, E., & Suzuki, T. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2003.11.027 · Cited by 42 · see citing works
Vorderstrasse, B. A., Cundiff, J. A., & Lawrence, B. P. (2006) · Journal of Toxicology and Environmental Health · doi:10.1080/15287390500246985 · Cited by 42 · see citing works
Self-citationCory‐Slechta, D. A., Pazmino, R., & Bare, C. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00591-x · Cited by 39 · see citing works
Self-citationMizuo, K., Narita, M., Yoshida, T., Narita, M., & Suzuki, T. (2004) · Addiction Biology · doi:10.1080/13556210410001674059 · Cited by 34 · see citing works
Serum Dioxin and Cognitive Functioning among Veterans of Operation Ranch Hand
Barrett, D. H., Morris, R. D., Akhtar, F. Z., & Michalek, J. E. (2001) · NeuroToxicology · doi:10.1016/s0161-813x(01)00051-1 · Cited by 33 · see citing works
Cyrenne, D. M. (2012) · St Andrews Research Repository (St Andrews Research Repository) · Cited by 32 · see citing works
Male rats that differ in novelty exploration demonstrate distinct patterns of sexual behavior.
Cummings, J., Clinton, S. M., Perry, A. N., Akil, H., & Becker, J. B. (2013) · Behavioral Neuroscience · doi:10.1037/a0031528 · Cited by 29 · see citing works
Endocrine Disruption Overview: Are Males at Risk?
Colborn, T. L. (2004) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-8995-6_12 · Cited by 28 · see citing works
Evans, S. B., & Cory‐Slechta, D. A. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00108-4 · Cited by 27 · see citing works
Self-citationWeston, H. I., Sobolewski, M., Allen, J. L., Weston, D. D., Conrad, K., Pelkowski, S. D., Watson, G. E., Zaręba, G., & Cory‐Slechta, D. A. (2014) · NeuroToxicology · doi:10.1016/j.neuro.2014.01.009 · Cited by 26 · see citing works
Self-citationEffects of suppressing gonadal hormones on response to novel objects in adolescent rats
Cyrenne, D. M., & Brown, G. R. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.08.015 · Cited by 26 · see citing works
Sequeira‐Cordero, A., Mora-Gallegos, A., Cuenca-Berger, P., & Trías, J. F. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.046 · Cited by 20 · see citing works
Brouillette, J. (2008) · NeuroToxicology · doi:10.1016/j.neuro.2007.12.005 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Starnes, H. M., Rock, K. D., Jackson, T. W., & Belcher, S. M. (2022) · Frontiers in Toxicology · doi:10.3389/ftox.2022.881584 · Cited by 166 · see citing works
“In this study, C57BL/6 mice were exposed to a mixture of these four chemicals, or each individually, from GD 7 to PND 1, and the neurodevelopment of their offspring was assessed in a behavioral battery (Sobolewski et al., 2014).”
BackgroundMethodInfluentialThe effects of prenatal PCBs on adult social behavior in rats
Reilly, M. P., Weeks, C. D., Topper, V. Y., Thompson, L. M., Crews, D., & Gore, A. C. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.06.002 · Cited by 65 · see citing works
“Developmental EDC exposure can also lead to sex-specific changes in behavior (Jacobsen et al., 2012; Kundakovic et al., 2013; Sobolewski et al., 2014; Williams et al., 2013).”
Liu, D., Yan, S., Liu, Y., Chen, Q., & Ren, S. (2024) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2024.115939 · Cited by 44 · see citing works
Gestational Exposure to Perfluorooctanoic Acid (PFOA): Alterations in Motor Related Behaviors
Goulding, D. R., White, S. S., McBride, S. J., Fenton, S. E., & Harry, G. J. (2017) · NeuroToxicology · doi:10.1016/j.neuro.2016.11.008 · Cited by 42 · see citing works
- Authors
- Sobolewski, M., Conrad, K., Allen, J. L., Weston, H., Martin, K., Lawrence, B. P., & Cory-Slechta, D. A.
- Affiliations
- University of Rochester Medicine (US)
- Corresponding author
- Sobolewski, Marissa
- Venue
- NeuroToxicology
- Publisher
- Elsevier BV
- Published
- 2014-12
- Volume
- 45
- Pages
- 121-130
- ISSN
- 0161-813X (ISSN-L)
- PMC
- PMC4387783
- OpenAlex
- W1987842240
- Cited by
- 91
- References
- 81
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 6 · 2023: 9 · 2022: 6 · 2021: 7 · 2020: 7 · 2019: 5 · 2018: 10 · 2017: 12 · 2016: 9 · 2015: 4
- FWCI
- 5.48
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- NeuroToxicology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Medical Center, University of Rochester
- National Institute of Environmental Health Sciences (R01ES023260, R01ES017250, P30ES001247, T32ES007026)
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Pesticide Exposure and Toxicity
- Keywords
- endocrine disruptors, chemical mixtures, developmental neurotoxicity, sex differences, mesocorticolimbic system, novel object recognition memory, locomotor activity, neophobia, atrazine, perfluorooctanoic acid, bisphenol A, 2,3,7,8-tetrachlorodibenzo-p-dioxin, maternal exposure, attention deficit hyperactivity disorder, autism spectrum disorder
- MeSH terms
- Bisphenol A Compounds, Animals, Atrazine, Behavior, Animal, Benzhydryl Compounds, Caprylates, Dioxins, Drug Combinations, Female, Fluorocarbons, Male, Mice, Inbred C57BL, Motor Activity, Phenols, Pregnancy, Prenatal Exposure Delayed Effects, Reinforcement Schedule, Sex Factors, Recognition, Psychology, Mice, Endocrine Disruptors
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
