Superfund Research Program

Neurobehavioral Toxicity Core

Project Leader: Edward D. Levin
Grant Number: P42ES010356
Funding Period: 2011-2022

Project-Specific Links

Publications

2021

• Boyda J, Hawkey AB, Holloway Z, Trevisan R, Di Giulio RT, Levin ED. 2021. The organophosphate insecticide diazinon and aging: Neurobehavioral and mitochondrial effects in zebrafish exposed as embryos or during aging. Neurotoxicol Teratol 87:doi:10.1016/j.ntt.2021.107011 PMID:34224825 PMCID:PMC8440393
• Hawkey AB, Holloway Z, Levin ED. 2021. A behavioral test battery to assess larval and adult zebrafish after developmental neurotoxic exposure. Experimental Neurotoxicology Methods 172:353-380. doi:10.1007/978-1-0716-1637-6_16
• Holloway Z, Hawkey AB, Asrat H, Boinapally N, Levin ED. 2021. The use of tocofersolan as a rescue agent in larval zebrafish exposed to benzo[a]pyrene in early development. Neurotoxicology 86:78-84. doi:10.1016/j.neuro.2021.07.003 PMID:34273383
• Levin ED. 2021. Invited Perspective: Does developmental adaptation pose risks with changing toxicant exposures?. Environ Health Perspect 129(8):81302. doi:10.1289/ehp9560 PMID:34383604 PMCID:PMC8360002
• Pan WK, Weinhouse C, Ortiz EJ, Berky AJ, Fixsen E, Mallipudi A, Feingold BJ, Navio S, Rivera NA, Hsu-Kim H, Miranda JJ. 2021. CoNaMad-Cohorte de Nacimiento de Madre de Dios / Madre de Dios Birth Cohort to Study Effects of in-utero Trace Metals Exposure in the Southern Peruvian Amazon. Ann Glob Health 87:doi:10.5334/aogh.3152 PMID:34327116 PMCID:PMC8300581

2020

• Brenner RG, Oliveri A, Sinnott-Armstrong W, Levin ED. 2020. Effects of sub-chronic methylphenidate on risk-taking and sociability in zebrafish (Danio rerio). Naunyn Schmiedebergs Arch Pharmacol doi:10.1007/s00210-020-01835-z PMID:32025747 PMCID:PMC7716188
• Hawkey AB, Pippen E, White H, Kim J, Greengrove E, Kenou B, Holloway Z, Levin ED. 2020. Gestational and perinatal exposure to diazinon causes long-lasting neurobehavioral consequences in the Rat. Toxicology 429:doi:10.1016/j.tox.2019.152327 PMID:31704166 PMCID:PMC6925319
• Hollander JA, Cory-Slechta DA, Jacka FN, Szabo ST, Guilarte TR, Bilbo SD, Mattingly CJ, Moy SS, Haroon E, Hornig M, Levin ED, Pletnikov MV, Zehr JL, McAllister KA, Dzierlenga AL, Garton AE, Lawler C, Ladd-Acosta C. 2020. Beyond the looking glass: recent advances in understanding the impact of environmental exposures on neuropsychiatric disease. Neuropsychopharmacology 45:doi:10.1038/s41386-020-0648-5 PMID:32109936 PMCID:PMC7234981
• Holloway Z, Koburov R, Hawkey AB, Levin ED. 2020. Measuring attention in rats with a visual signal detection task: Signal intensity vs. signal duration. Pharmacol Biochem Behav 199:doi:10.1016/j.pbb.2020.173069 PMID:33144207 PMCID:PMC7726090
• Oliveri A, Glazer L, Mahapatra D, Kullman SW, Levin ED. 2020. Developmental exposure of zebrafish to vitamin D receptor acting drugs and environmental toxicants disrupts behavioral function. Neurotoxicol Teratol 81:10. doi:10.1016/j.ntt.2020.106902 PMID:32473203 PMCID:PMC7483728
• Oliveri A, Knuth M, Glazer L, Bailey JM, Kullman SW, Levin ED. 2020. Zebrafish show long-term behavioral impairments resulting from developmental vitamin D deficiency. Physiol Behav 224:113016. doi:10.1016/j.physbeh.2020.113016 PMID:32561170 PMCID:PMC7737556 (ahead of print)

2019

• Hawkey AB, Junaid S, Yao L, Spiera Z, White H, Cauley M, Levin ED. 2019. Gestational exposure to nicotine and/or benzo[a]pyrene causes long-lasting neurobehavioral consequences. Birth Defects Res 111(17):1248-1258. doi:10.1002/bdr2.1568 PMID:31368242 PMCID:PMC6983916
• Oliveri A, Levin ED. 2019. Dopamine D1 and D2 receptor antagonism during development alters later behavior in zebrafish. Behav Brain Res 356:250-256. doi:10.1016/j.bbr.2018.08.028 PMID:30172631 PMCID:PMC6192051
• Slotkin TA, Skavicus S, Ko A, Levin ED, Seidler FJ. 2019. Perinatal diazinon exposure compromises the development of acetylcholine and serotonin systems. Toxicology 424:10. doi:10.1016/j.tox.2019.152240 PMID:31251962 PMCID:PMC6689134
• Slotkin TA, Skavicus S, Ko A, Levin ED, Seidler FJ. 2019. The developmental neurotoxicity of tobacco smoke can be mimicked by a combination of nicotine and benzo[a]pyrene: effects on cholinergic and serotonergic systems. Toxicol Sci 168:280. doi:10.1093/toxsci/kfy304 PMID:30247698 PMCID:PMC6681680

2018

• Glazer L, Hawkey AB, Wells C, Drastal M, Odamah K, Behl M, Levin ED. 2018. Developmental exposure to low concentrations of organophosphate flame retardants causes life-long behavioral alterations in zebrafish. Toxicol Sci 165(2):487-498. doi:10.1093/toxsci/kfy173 PMID:29982741 PMCID:PMC6154272
• Glazer L, Wells C, Drastal M, Odamah K, Galat RE, Behl M, Levin ED. 2018. Developmental exposure to low concentrations of two brominated flame retardants, BDE-47 and BDE-99, causes life-long behavioral alterations in zebrafish. Neurotoxicology 66:221-232. doi:10.1016/j.neuro.2017.09.007 PMID:28935585 PMCID:PMC5858967
• Levin ED, Abreu-Villaca Y. 2018. Developmental neurotoxicity of nicotine and tobacco. Chapter 39 in: Handbook of Developmental Neurotoxicology, 2nd Edition. Elsevier Inc., pp.439-452.
• Massarsky A, Abdel A, Glazer L, Levin ED, Di Giulio RT. 2018. Neurobehavioral effects of 1,2-propanediol in zebrafish (Danio rerio). Neurotoxicology 65:111-124. doi:10.1016/j.neuro.2018.02.007 PMID:29432853
• Oliveri A, Ortiz E, Levin ED. 2018. Developmental exposure to an organophosphate flame retardant alters later behavioral responses to dopamine antagonism in zebrafish larvae. Neurotoxicol Teratol 67:25-30. doi:10.1016/j.ntt.2018.03.002 PMID:29559250 PMCID:PMC5970957
• Pitt JA, Trevisan R, Massarsky A, Kozal JS, Levin ED, Di Giulio RT. 2018. Maternal transfer of nanoplastics to offspring in zebrafish (Danio rerio): A case study with nanopolystyrene. Sci Total Environ 643:324-334. doi:10.1016/j.scitotenv.2018.06.186 PMID:29940444

2017

• Abreu-Villaca Y, Levin ED. 2017. Developmental neurotoxicity of succeeding generations of insecticides. Environ Int 99:55-77. doi:10.1016/j.envint.2016.11.019 PMID:27908457 PMCID:PMC5285268
• Levin ED. 2017. Neurodevelopmental Toxicity of Tobacco Smoke and Nicotine. Neurotoxicol Teratol 61:153. doi:10.1016/j.ntt.2017.04.004
• Macaulay LJ, Chernick M, Chen A, Hinton DE, Bailey JM, Kullman SW, Levin ED, Stapleton HM. 2017. Exposure to a PBDE/OH-BDE mixture alters juvenile zebrafish (Danio rerio) development. Environ Toxicol Chem 36(1):36-48. doi:10.1002/etc.3535 PMID:27329031
• Massarsky A, Abdel A, Glazer L, Levin ED, Di Giulio RT. 2017. Exposure to 1,2-propanediol impacts early development of zebrafish (Danio rerio) and induces hyperactivity. Zebrafish 14(3):216-222. doi:10.1089/zeb.2016.1400 PMID:28266909
• Slotkin TA, Skavicus S, Card JA, Di Giulio RT, Seidler FJ. 2017. In vitro models reveal differences in the developmental neurotoxicity of an environmental polycylic aromatic hydrocarbon mixture compared to benzo[a]pyrene: Neuronotypic PC12 Cells and embryonic neural stem cells. Toxicology 377:49-56. doi:10.1016/j.tox.2016.12.008 PMID:28049045 PMCID:PMC5250555

2016

• Abreu-Villaca Y, Levin ED. 2016. Developmental neurobehavioral neurotoxicity of insecticides. In: Handbook of Development Neurotoxicology. Academic Press, San Diego, CA. pp.453-466.
• Bailey JM, Oliveri A, Karbhari N, Brooks RA, De La Rocha AJ, Janardhan S, Levin ED. 2016. Persistent behavioral effects following early life exposure to retinoic acid or valproic acid in zebrafish. Neurotoxicology 52:23-33. doi:10.1016/j.neuro.2015.10.001 PMID:26439099 PMCID:PMC4753107
• Brown DR, Bailey JM, Oliveri A, Levin ED, Di Giulio RT. 2016. Developmental exposure to a complex PAH mixture causes persistent behavioral effects in naive Fundulus heteroclitus (killifish) but not in a population of PAH-adapted killifish. Neurotoxicol Teratol 53:55-63. doi:10.1016/j.ntt.2015.10.007 PMID:26548404 PMCID:PMC4803068
• Petro A, Sexton HG, Miranda C, Rastogi A, Freedman JH, Levin ED. 2016. Persisting neurobehavioral effects of developmental copper exposure in wildtype and metallothionein 1 and 2 knockout mice. BMC Pharmacol Toxicol 17(1):55. doi:10.1186/s40360-016-0096-3 PMID:27802831 PMCID:PMC5090947
• Slotkin TA, Skavicus S, Card JA, Levin ED, Seidler FJ. 2016. Diverse neurotoxicants target the differentiation of embryonic neural stem cells into neuronal and glial phenotypes. Toxicology 372:42-51. doi:10.1016/j.tox.2016.10.015 PMID:27816694 PMCID:PMC5137195

2015

• Bailey JM, Crosby EB, Oliveri A, Levin ED. 2015. Neurobehavioral impairments caused by developmental imidacloprid exposure in zebrafish. Neurotoxicol Teratol 49:81-90. doi:10.1016/j.ntt.2015.04.006 PMID:25944383 PMCID:PMC4458463
• Bailey JM, Levin ED. 2015. Neurotoxicity of FireMaster 550® in zebrafish (Danio rerio): chronic developmental and acute adolescent exposures. Neurotoxicol Teratol 52(PtB):210-219. doi:10.1016/j.ntt.2015.07.001 PMID:26239867 PMCID:PMC4679535
• Bailey JM, Oliveri A, Levin ED. 2015. Pharmacological analyses of learning and memory in zebrafish (Danio rerio). Pharmacol Biochem Behav 139PtB:103-111. doi:10.1016/j.pbb.2015.03.006 PMID:25792292 PMCID:PMC4573775
• Bailey JM, Oliveri A, Zhang C, Fraizer JM, Mackinnon S, Cole GJ, Levin ED. 2015. Long-term behavioral impairment following acute embryonic ethanol exposure in zebrafish. Neurotoxicol Teratol 48:1-8. doi:10.1016/j.ntt.2015.01.005 PMID:25599606 PMCID:PMC4363207
• Levin ED. 2015. Learning about cognition risk with the radial-arm maze in the developmental neurotoxicology battery. Neurotoxicol Teratol 52(PtA):88-92. doi:10.1016/j.ntt.2015.05.007 PMID:26013674 PMCID:PMC4656139
• Macaulay LJ, Bailey JM, Levin ED, Stapleton HM. 2015. Persisting effects of a PBDE metabolite, 6-OH-BDE-47, on larval and juvenile zebrafish swimming behavior. Neurotoxicol Teratol 52(PtB):119-126. doi:10.1016/j.ntt.2015.05.002 PMID:25979796 PMCID:PMC4644107
• Massarsky A, Jayasundara N, Bailey JM, Oliveri A, Levin ED, Prasad GL, Di Giulio RT. 2015. Teratogenic, bioenergetic, and behavioral effects of exposure to total particulate matter on early development of zebrafish (Danio rerio) are not mimicked by nicotine. Neurotoxicol Teratol 51:77-88. doi:10.1016/j.ntt.2015.09.006 PMID:26391568 PMCID:PMC4821439
• Oliveri A, Bailey JM, Levin ED. 2015. Developmental exposure to organophosphate flame retardants causes behavioral effects in larval and adult zebrafish. Neurotoxicol Teratol 52(PtB):220-227. doi:10.1016/j.ntt.2015.08.008 PMID:26344674 PMCID:PMC4769864
• Slotkin TA, Skavicus S, Levin ED, Seidler FJ. 2015. Prenatal nicotine changes the response to postnatal chlorpyrifos: Interactions targeting serotonergic synaptic function and cognition. Brain Res Bull 111:84-96. doi:10.1016/j.brainresbull.2015.01.003 PMID:25592617 PMCID:PMC4324014

2014

• Levin ED, Cauley M, Johnson JE, Cooper EM, Stapleton HM, Ferguson PL, Seidler FJ, Slotkin TA. 2014. Prenatal dexamethasone augments the neurobehavioral teratology of chlorpyrifos: significance for maternal stress and preterm labor. Neurotoxicol Teratol 41:35-42. doi:10.1016/j.ntt.2013.10.004 PMID:24177596 PMCID:PMC3943881
• Slotkin TA, Card JA, Seidler FJ. 2014. Prenatal dexamethasone, as used in preterm labor, worsens the impact of postnatal chlorpyrifos exposure on serotonergic pathways. Brain Res Bull 100:44-54. doi:10.1016/j.brainresbull.2013.10.014 PMID:24280657 PMCID:PMC3891922

2013

• Bailey JM, Oliveri A, Levin ED. 2013. Zebrafish model systems for developmental neurobehavioral toxicology. Birth Defects Res C Embryo Today 99:14-23. doi:10.1002/bdrc.21027 PMID:23723169 PMCID:PMC4000730
• Levin ED, Landrigan PJ, Etzel R. 2013. Developmental Toxicology and Children's Environmental Health. In: The Oxford Textbook of Environmental Pediatrics: Environmental Influences on Health, Development and Disease. Oxford, New York, NY. pp.83-88.
• Slotkin TA, Card JA, Infante A, Seidler FJ. 2013. BDE99 (2,2',4,4',5-pentabromodiphenyl ether) suppresses differentiation into neurotransmitter phenotypes in PC12 cells. Neurotoxicol Teratol 37:13-17. doi:10.1016/j.ntt.2013.02.001 PMID:23422510 PMCID:PMC3669237
• Slotkin TA, Card JA, Infante A, Seidler FJ. 2013. Prenatal dexamethasone augments the sex-selective developmental neurotoxicity of chlorpyrifos: Implications for vulnerability after pharmacotherapy for preterm labor. Neurotoxicol Teratol 37:1-12. doi:10.1016/j.ntt.2013.02.002 PMID:23416428 PMCID:PMC3669256
• Slotkin TA, Card JA, Seidler FJ. 2013. Adverse benzo[a]pyrene effects on neurodifferentiation are altered by other neurotoxicant coexposures: Interactions with dexamethasone, chlorpyrifos, or nicotine in PC12 cells. Environ Health Perspect 121:825-831. doi:10.1289/ehp.1306528 PMID:23603068 PMCID:PMC3702011
• Slotkin TA, Cooper EM, Stapleton HM, Seidler FJ. 2013. Does thyroid disruption contribute to the developmental neurotoxicity of chlorpyrifos?. Environ Toxicol Pharmacol 36(2):284-287. doi:10.1016/j.etap.2013.04.003 PMID:23686008 PMCID:PMC3745805