Superfund Research Program

Cholinergic and Monoaminergic Mechanisms of Persistent Neurobehavioral Toxicity

Project Leader: Edward D. Levin
Co-Investigators: Theodore A. Slotkin (Duke University Medical Center), Frederic J. Seidler
Grant Number: P42ES010356
Funding Period: 2017-2022

Project-Specific Links

Publications

2022

• Hawkey AB, Pippen E, Kenou B, Holloway Z, Slotkin TA, Seidler FJ, Levin ED. 2022. Persistent neurobehavioral and neurochemical anomalies in middle-aged rats after maternal diazinon exposure. Toxicology 472:153189. doi:10.1016/j.tox.2022.153189 PMID:35452779

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
• Slotkin TA, Levin ED, Seidler FJ. 2021. Paternal cannabis exposure prior to mating, but not 9-tetrahydrocannabinol, elicits deficits in dopaminergic synaptic activity in the offspring. Toxicol Sci 184(2):doi:10.1093/toxsci/kfab117 PMID:34590702

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, Glazer L, Dean C, Wells C, Odamah K, Slotkin TA, Seidler FJ, Levin ED. 2020. Adult exposure to insecticides causes persistent behavioral and neurochemical alterations in zebrafish. Neurotoxicol Teratol 78:doi:10.1016/j.ntt.2019.106853 PMID:31911208 PMCID:PMC7061078
• 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
• 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
• Slotkin TA, Skavicus S, Seidler FJ. 2018. Developmental neurotoxicity resulting from pharmacotherapy of preterm labor, modeled In Vitro: Terbutaline and dexamethasone, separately and together. Toxicology 30033-30037. doi:10.1016/j.tox.2018.03.001 PMID:29524569 PMCID:PMC5903951

2017

• 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
• Slotkin TA, Skavicus S, Seidler FJ. 2017. Diazinon and parathion diverge in their effects on development of noradrenergic systems. Brain Res Bull 130:268-273. doi:10.1016/j.brainresbull.2017.02.004 PMID:28235599
• Slotkin TA, Skavicus S, Stapleton HM, Seidler FJ. 2017. Brominated and organophosphate flame retardants target different neurodevelopmental stages, characterized with embryonic neural stem cells and neuronotypic PC12 cells. Toxicology 390:32-42. doi:10.1016/j.tox.2017.08.009 PMID:28851516 PMCID:PMC5633518

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.