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Biological Trace Element Research

, Volume 189, Issue 1, pp 118–133 | Cite as

Arsenic-Induced Neurotoxicity by Dysfunctioning Cholinergic and Dopaminergic System in Brain of Developing Rats

  • Lalit P. ChandravanshiEmail author
  • Richa Gupta
  • Rajendra K. Shukla
Article

Abstract

Chronic exposure to arsenic via drinking water throughout the globe is assumed to cause a developmental neurotoxicity. Here, we investigated the effect of perinatal arsenic exposure on the neurobehavioral and neurochemical changes in the corpus striatum, frontal cortex, and hippocampus that is critically involved in motor and cognition functions. In continuation of previous studies, this study demonstrates that perinatal exposures (GD6–PD21) to arsenic (2 or 4 mg/kg body weight, p.o.) cause hypo-activity in arsenic-exposed rats on PD22. The hypo-activity was found to be linked with a decrease in the mRNA and protein expression of the DA-D2 receptor. Further, a protein expression of tyrosine hydroxylase (TH), levels of dopamine, and its metabolites were also significantly impaired in corpus striatum. The arsenic-exposed groups showed spatial learning and memory significantly below the average in a dose-dependent manner for the controls. Here, we evaluated the declined expression of CHRM2 receptor gene and protein expression of ChAT, PKCβ-1 in the frontal cortex and hippocampus, which are critically involved in cognition functions including learning and memory. A trend of recovery was found in the cholinergic and dopaminergic system of the brain, but changes remained persisted even after the withdrawal of arsenic exposure on PD45. Taken together, our results indicate that perinatal arsenic exposure appears to be critical and vulnerable as the development of cholinergic and dopaminergic system continues during this period.

Keywords

Developmental neurotoxicity Arsenic DA-D2 receptor Spatial memory Locomotor activity etc. 

Notes

Acknowledgements:

The authors thank the Director of the CSIR–Indian Institute of Toxicology Research (CSIR-IITR), Lucknow for his support and keen interest in the present study. Financial support by the University Grants Commission, New Delhi for carrying out the study is gratefully acknowledged.

Compliance with Ethical Standards

Conflict of Interest

The authors state no conflict of interest.

References

  1. 1.
    Agrawal S, Bhatnagar P, Flora SJ (2015) Changes in tissue oxidative stress, brain biogenic amines and acetylcholinesterase following co-exposure to lead, arsenic and mercury in rats. Food Chem Toxicol 86:208–216CrossRefGoogle Scholar
  2. 2.
    Ahmed S, Mahabbat-e Khoda S, Rekha RS, Gardner RM, Ameer SS, Moore S, Ekström EC, Vahter M, Raqib R (2011) Arsenic-associated oxidative stress, inflammation, and immune disruption in human placenta and cord blood. Environ Health Perspect 119:258–264CrossRefGoogle Scholar
  3. 3.
    Ali N, Hoque MA, Haque A, Salam KA, Karim MR, Rahman A, Islam K, Saud ZA, Khalek MA, Akhand AA, Hossain M, Mandal A, Karim MR, Miyataka H, Himeno S, Hossain K (2010) Association between arsenic exposure and plasma cholinesterase activity: a population based study in Bangladesh. Environ Health 10:9–36Google Scholar
  4. 4.
    Altman J, Sudarshan K (1975) Postnatal development of locomotion in the laboratory rat. Anim Behav 23:896–920CrossRefGoogle Scholar
  5. 5.
    Aung KH, Kyi-Tha-Thu C, Sano K, Nakamura K, Tanoue A, Nohara K, Kakeyama M, Tohyama C, Tsukahara S, Maekawa F (2016) Prenatal exposure to arsenic impairs behavioral flexibility and cortical structure in mice. Front Neurosci 10:137CrossRefGoogle Scholar
  6. 6.
    Ballentine R, Burford DD (1957) Determination of metals. Methods Enzymol 3:1002–1035CrossRefGoogle Scholar
  7. 7.
    Bardullas U, Limón-Pacheco JH, Giordano M, Carrizales L, Mendoza-Trejo MS, Rodríguez VM (2009) Chronic low-level arsenic exposure causes gender-specific alterations in locomotor activity, dopaminergic systems, and thioredoxin expression in mice. Toxicol Appl Pharmacol 239:169–177CrossRefGoogle Scholar
  8. 8.
    Bashir S, Sharma Y, Irshad M, Nag TC, Tiwari M, Kabra M, Dogra TD (2006) Arsenic induced apoptosis in rat liver following repeated 60 days exposure. Toxicology 217:63–70CrossRefGoogle Scholar
  9. 9.
    Brinkel J, Khan MH, Kraemer A (2009) Systematic review of arsenic exposure and its social and mental health effects with special reference to Bangladesh. Int J Environ Res Public Health 6:1609–1619CrossRefGoogle Scholar
  10. 10.
    Caldwell KE, Labrecque MT, Solomon BR, Ali A, Allan AM (2015) Prenatal arsenic exposure alters the programming of the glucocorticoid signaling system during embryonic development. Neurotoxicol Teratol 47:66–79CrossRefGoogle Scholar
  11. 11.
    Chandravanshi LP, Yadav RS, Shukla RK, Singh A, Sultana S, Pant AB, Parmar D, Khanna VK (2014a) Reversibility of changes in brain cholinergic receptors and acetylcholinesterase activity in rats following early life arsenic exposure. Int J Dev Neurosci 34:60–75CrossRefGoogle Scholar
  12. 12.
    Chandravanshi LP, Shukla RK, Sultana S, Pant AB, Khanna VK (2014b) Early life arsenic exposure and brain dopaminergic alterations in rats. Int J Dev Neurosci 38:91–104CrossRefGoogle Scholar
  13. 13.
    Chandravanshi LP, Gupta R, Shukla RK (2018 Mar 3) Developmental neurotoxicity of arsenic: involvement of oxidative stress and mitochondrial functions. Biol Trace Elem Res.  https://doi.org/10.1007/s12011-018-1286-1
  14. 14.
    Chen Y, Graziano JH, Parvez F, Liu M, Slavkovich V, Kalra T, Argos M, Islam T, Ahmed A, Rakibuz-Zaman M (2011) Arsenic exposure from drinking water andmortality from cardiovascular disease in Bangladesh: prospective cohort study. BMJ 342:d2431CrossRefGoogle Scholar
  15. 15.
    Dhar P, Jaitley M, Kalaivani M, Mehra RD (2005) Preliminary morphological and histochemical changes in rat spinal cord neurons following arsenic ingestion. Neurotoxicology 26:309–320CrossRefGoogle Scholar
  16. 16.
    Duker AA, Carranza EJ, Hale M (2005) Arsenic geochemistry and health. Environ Int 31:631–641CrossRefGoogle Scholar
  17. 17.
    Dwivedi N, Flora SJ (2011) Concomitant exposure to arsenic and organophosphates on tissue oxidative stress in rats. Food Chem Toxicol 49:1152–1159CrossRefGoogle Scholar
  18. 18.
    Eisenegger C, Naef M, Linssen A, Clark L, Gandamaneni PK, Müller U, Robbins TW (2014) Role of dopamine D2 receptors in human reinforcement learning. Neuropsychopharmacology 39:2366–2375CrossRefGoogle Scholar
  19. 19.
    Ellman GL, Courtney KD, Andres VJ, Feather-Stone RM (1961) A new and rapid calorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95CrossRefGoogle Scholar
  20. 20.
    Fängström B, Moore S, Nermell B, Kuenstl L, Goessler W, Grandér M, Kabir I, Palm B, Arifeen SE, Vahter M (2008) Breast-feeding protects against arsenic exposure in Bangladeshi infants. Environ Health Perspect 116:963–969CrossRefGoogle Scholar
  21. 21.
    Farag AT, Goda NF, Shaaban NA, Mansee AH (2007) Effects of oral exposure of synthetic pyrethroid, cypermethrin on the behavior of F1-progeny in mice. Reprod Toxicol 23:560–567CrossRefGoogle Scholar
  22. 22.
    Girault JA, Greengard P (2004) The neurobiology of dopamine signaling. Arch Neurol 61:641–644CrossRefGoogle Scholar
  23. 23.
    Glowinski J, Iversen LL (1966) Regional studies of catecholamines in the rat brain. I. The disposition of [3H]norepinephrine, [3H]dopamine and [3H]dopa in various regions of the brain. J Neurochem 13:655–659CrossRefGoogle Scholar
  24. 24.
    Gong G, O'Bryant SE (2010) The arsenic exposure hypothesis for Alzheimer disease. Alzheimer Dis Assoc Disord 24:311–316CrossRefGoogle Scholar
  25. 25.
    Gonzalez-Cortes T, Recio-Vega R, Lantz RC, Chau BT (2017) DNA methylation of extracellular matrix remodeling genes in children exposed to arsenic. Toxicol Appl Pharmacol 329:140–147CrossRefGoogle Scholar
  26. 26.
    González-Horta C, Ballinas-Casarrubias L, Sánchez-Ramírez B, Ishida MC, Barrera-Hernández A, Gutiérrez-Torres D, Zacarias OL, Saunders RJ, Drobná Z, Mendez MA, García-Vargas G, Loomis D, Stýblo M, Del Razo LM (2015) A concurrent exposure to arsenic and fluoride from drinking water in Chihuahua, Mexico. Int J Environ Res Public Health 12:4587–4601CrossRefGoogle Scholar
  27. 27.
    Hirner AV, Rettenmeier AW (2010) Methylated metal(loid) species in humans. Met Ions Life Sci 7:465-521Google Scholar
  28. 28.
    Hughes MF, Beck BD, Chen Y, Lewis AS, Thomas DJ (2011) Arsenic exposure and toxicology: a historical perspective. Toxicol Sci 123:305–332CrossRefGoogle Scholar
  29. 29.
    Ishii K, Itoh Y, Iwasaki N, Shibata Y, Tamaoka A (2014) Detection of diphenylarsinic acid and its derivatives in human serum and cerebrospinal fluid. Clin Chim Acta 431:227–231CrossRefGoogle Scholar
  30. 30.
    Itoh T, Zhang YF, Murai S, Saito H, Nagahama H, Miyate H, Saito Y, Abe E (1990) The effect of arsenic trioxide on brain monoamine metabolism and locomotor activity of mice. Toxicol Lett 54:345–353CrossRefGoogle Scholar
  31. 31.
    Jin Y, Xi S, Li X, Lu C, Li G, Xu Y, Qu C, Niu Y, Sun G (2006) Arsenic speciation transported through the placenta from mother mice to their newborn pups. Environ Res 101:349–355CrossRefGoogle Scholar
  32. 32.
    Kamkwalala AR, Newhouse PA (2017) Beyond acetylcholinesterase inhibitors: novel cholinergic treatments for Alzheimer's disease. Curr Alzheimer Res 14:377–392Google Scholar
  33. 33.
    Kapaj S, Peterson H, Liber K, Bhattacharya P (2006) Human health effects from chronic arsenic poisoning—a review. J Environ Sci Health A Tox Hazard Subst Environ Eng 41:2399–2428CrossRefGoogle Scholar
  34. 34.
    Kim C, Speisky MB, Kharouba SN (1987) Rapid and sensitive method for measuring norepinephrine, dopamine, 5-hydroxytryptamine and their major metabolites in rat brain by high-performance liquid chromatography. Differential effect of probenecid, haloperidol and yohimbine on the concentrations of biogenic amines and metabolites in various regions of rat brain. J Chromatogr 386:25–35CrossRefGoogle Scholar
  35. 35.
    Kim M, Seo S, Sung K, Kim K (2014) Arsenic exposure in drinking water alters the dopamine system in the brains of C57BL/6 mice. Biol Trace Elem Res 162(1–3):175–180CrossRefGoogle Scholar
  36. 36.
    Kordas K, Ardoino G, Coffman DL, Queirolo EI, Ciccariello D, Mañay N, Ettinger AS (2015) Patterns of exposure to multiple metals and associations with neurodevelopment of preschool children from Montevideo, Uruguay. J Environ Public Health 2015:493471CrossRefGoogle Scholar
  37. 37.
    Kozul-Horvath CD, Zandbergen F, Jackson BP, Enelow RI, Hamilton JW (2012) Effects of low-dose drinking water arsenic on mouse fetal and postnatal growth and development. PLoS One 7:e38249CrossRefGoogle Scholar
  38. 38.
    Krinke G (2000) In: Bullock G, Bunton TE (eds) The laboratory rat: a volume in handbook of experimental animals, chapter 12 developmental neurotoxicity. Academic Press, San Diego, p 75Google Scholar
  39. 39.
    Lazarini CA, Lima RY, Guedes AP, Bernardi MM (2004) Prenatal exposure to dichlorvos: physical and behavioral effects on rat offspring. Neurotoxicol Teratol 26:607–614CrossRefGoogle Scholar
  40. 40.
    Liu J, Waalkes MP (2018) Liver is a target of arsenic carcinogenesis. Toxicol Sci 105:24–32CrossRefGoogle Scholar
  41. 41.
    Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  42. 42.
    Luo JH, Qiu ZQ, Shu WQ, Zhang YY, Zhang L, Chen JA (2009) Effects of arsenic exposure from drinking water on spatial memory, ultra-structures and NMDAR gene expression of hippocampus in rats. Toxicol Lett 184:121–125CrossRefGoogle Scholar
  43. 43.
    Luo JH, Qiu ZQ, Zhang L, Shu WQ (2012) Arsenite exposure altered the expression of NMDA receptor and postsynaptic signaling proteins in rat hippocampus. Toxicol Lett 211:39–44CrossRefGoogle Scholar
  44. 44.
    Martinez-Finley EJ, Ali AM, Allan AM (2009) Learning deficits in C57BL/6J mice following perinatal arsenic exposure: consequence of lower corticosterone receptor levels? Pharmacol Biochem Behav 94:271–277CrossRefGoogle Scholar
  45. 45.
    Maurice T, Su T-P, Parish W, Nabeshima T, Privat A (1994) PRE-084, a sigma selective PCP derivative, attenuates MK-801-induced impairment of learning in mice. Pharmacol Biochem Behav 49:859–869CrossRefGoogle Scholar
  46. 46.
    Mazumdar M (2017) Does arsenic increase the risk of neural tube defects among a highly exposed population? A new case–control study in Bangladesh. Birth Defects Res 109:92–98CrossRefGoogle Scholar
  47. 47.
    Mejía JJ, Díaz-Barriga F, Calderón J, Ríos C, Jiménez-Capdeville ME (1997) Effects of lead-arsenic combined exposure on central monoaminergic systems. Neurotoxicol Teratol 19:489–497CrossRefGoogle Scholar
  48. 48.
    Milton AH, Hussain S, Akter S, Rahman M, Mouly TA, Mitchell K (2017) A review of the effects of chronic arsenic exposure on adverse pregnancy outcomes. Int J Environ Res Public Health 6Google Scholar
  49. 49.
    Minichilli F, Bianchi F, Ronchi AM, Gorini F, Bustaffa E (2018) Urinary arsenic in human samples from areas characterized by natural or anthropogenic pollution in Italy. Int J Environ Res Public Health 15Google Scholar
  50. 50.
    Miyauchi M, Kishida I, Suda A, Shiraishi Y, Hattori S, Fujibayashi M, Taguri M, Ishii C, Ishii N, Moritani T, Hirayasu Y (2016) Association of the cholinergic muscarinic M2 receptor with autonomic nervous system activity in patients with schizophrenia on high-dose antipsychotics. Neuropsychobiology 74:60–67CrossRefGoogle Scholar
  51. 51.
    Moreno Ávila CL, Limón-Pacheco JH, Giordano M, Rodríguez VM (2016) Chronic exposure to arsenic in drinking water causes alterations in locomotor activity and decreases striatal mRNA for the D2 dopamine receptor in CD1 male mice. J Toxicol 2016:4763434CrossRefGoogle Scholar
  52. 52.
    Mufson EJ, Counts SE, Perez SE, Ginsberg SD (2008) Cholinergic system during the progression of Alzheimer's disease: therapeutic implications. Expert Rev Neurother 8:1703–1718CrossRefGoogle Scholar
  53. 53.
    Mukherjee B, Bindhani B, Saha H, Sinha D, Ray MR (2014) Platelet hyperactivity, neurobehavioral symptoms and depression among Indian women chronically exposed to low level of arsenic. Neurotoxicology 45:159–167CrossRefGoogle Scholar
  54. 54.
    Paratcha G, Furman M, Bevilaqua L, Cammarota M, Vianna M, de Stein ML, Izquierdo I, Medina JH (2000) Involvement of hippocampal PKCbeta1 isoform in the early phase of memory formation of an inhibitory avoidance learning. Brain Res 855:199–205CrossRefGoogle Scholar
  55. 55.
    Parvez F, Wasserman GA, Factor-Litvak P, Liu X, Slavkovich V, Siddique AB, Sultana R, Sultana R, Islam T, Levy D, Mey JL, Van Geen A, Khan K, Kline J, Ahsan H, Graziano JH (2011) Arsenic exposure and motor function among children in Bangladesh. Environ Health Perspect 119:1665–1670Google Scholar
  56. 56.
    Patlolla AK, Tchounwou PB (2005) Serum acetyl cholinesterase as a biomarker of arsenic induced neurotoxicity in Sprague-Dawley rats. Int J Environ Res Public Health 2:80–83CrossRefGoogle Scholar
  57. 57.
    Prakash C, Soni M, Kumar V (2016) Mitochondrial oxidative stress and dysfunction in arsenic neurotoxicity: a review. J Appl Toxicol 36(2):179–188CrossRefGoogle Scholar
  58. 58.
    Rahman A, Persson LÅ, Nermell B, El Arifeen S, Ekström EC, Smith AH, Vahter M (2010) Arsenic exposure and risk of spontaneous abortion, stillbirth, and infant mortality. Epidemiology 21:797–804CrossRefGoogle Scholar
  59. 59.
    Rahman A, Kumarathasan P, Gomes J (2016) Infant and mother related outcomes from exposure to metals with endocrine disrupting properties during pregnancy. Sci Total Environ 569-570:1022–1031CrossRefGoogle Scholar
  60. 60.
    Rahman A, Granberg C, Persson LA (2017) Early life arsenic exposure, infant and child growth, and morbidity: a systematic review. Arch Toxicol 91:3459–3467CrossRefGoogle Scholar
  61. 61.
    Rodrigues EG, Bellinger DC, Valeri L, Hasan MO, Quamruzzaman Q, Golam M, Kile ML, Christiani DC, Wright RO, Mazumdar M (2016) Neurodevelopmental outcomes among 2- to 3-year-old children in Bangladesh with elevated blood lead and exposure to arsenic and manganese in drinking water. Environ Health 15:44CrossRefGoogle Scholar
  62. 62.
    Rodríguez VM, Dufour L, Carrizales L, Díaz-Barriga F, Jiménez-Capdeville ME (1998) Effects of oral exposure to mining waste on in vivo dopamine release from rat striatum. Environ Health Perspect 106:487–491Google Scholar
  63. 63.
    Rodríguez VM, Limón-Pacheco JH, Carrizales L, Mendoza-Trejo MS, Giordano M (2010) Chronic exposure to low levels of inorganic arsenic causes alterations in locomotor activity and in the expression of dopaminergic and antioxidant systems in the albino rat. Neurotoxicol Teratol 32:640–647CrossRefGoogle Scholar
  64. 64.
    Roghani M, Joghataie MT, Jalali MR, Baluchnejadmojarad T (2006) Time course of changes in passive avoidance and Y-maze performance in male diabetic rats. Iran Biomed J J10:99–104Google Scholar
  65. 65.
    Rosado JL, Ronquillo D, Kordas K, Rojas O, Alatorre J, Lopez P, Garcia-Vargas G, Del Carmen CM, Cebrian ME, Stoltzfus RJ (2007) Arsenic exposure and cognitive performance in Mexican schoolchildren. Environ Health Perspect 115:1371–1375CrossRefGoogle Scholar
  66. 66.
    Rudge CV, Röllin HB, Nogueira CM, Thomassen Y, Rudge MC, Odland JØ (2009) The placenta as a barrier for toxic and essential elements in paired maternal and cord blood samples of South African delivering women. J Environ Monit 11:1322–1330CrossRefGoogle Scholar
  67. 67.
    Sanders AP, Desrosiers TA, Warren JL, Herring AH, Enright D, Olshan AF, Meyer RE, Fry RC (2014) Association between arsenic, cadmium, manganese, and lead levels in private wells and birth defects prevalence in North Carolina: a semi-ecologic study. BMC Public Health 14:955CrossRefGoogle Scholar
  68. 68.
    Shih YH, Islam T, Hore SK, Sarwar G, Shahriar MH, Yunus M, Graziano JH, Harjes J, Baron JA, Parvez F, Ahsan H, Argos M (2017) Associations between prenatal arsenic exposure with adverse pregnancy outcome and child mortality. Environ Res 158:456–461CrossRefGoogle Scholar
  69. 69.
    Shohamy D, Adcock RA (2010) Dopamine and adaptive memory. Trends Cogn Sci 14:464–472CrossRefGoogle Scholar
  70. 70.
    Smeester L, Fry RC (2018) Long-term health effects and underlying biological mechanisms of developmental exposure to arsenic. Curr Environ Health Rep 1:134–144CrossRefGoogle Scholar
  71. 71.
    Soni I, Syed F, Bhatnagar P, Mathur R (2011) Perinatal toxicity of cyfluthrin in mice: developmental and behavioral effects. Hum Exp Toxicol 30:1096–1105CrossRefGoogle Scholar
  72. 72.
    Srivastava P, Yadav RS, Chandravanshi LP, Shukla RK, Dhuriya YK, Chauhan LK, Dwivedi HN, Pant AB, Khanna VK (2014) Unraveling the mechanism of neuroprotection of curcumin in arsenic induced cholinergic dysfunctions in rats. Toxicol Appl Pharmacol 279:428–440CrossRefGoogle Scholar
  73. 73.
    Terry AV Jr, Stone JD, Buccafusco JJ, Sickles DW, Sood A, Prendergast MA (2003) Repeated exposure to subthreshhold doses of chlorpyrifos in rats: hippocampal damage, impaired axonal transport and deficits in spatial learning. J Pharmacol Exp Ther 305:375–384CrossRefGoogle Scholar
  74. 74.
    Tolins M, Ruchirawat M, Landrigan P (2014) The developmental neurotoxicity of arsenic: cognitive and behavioral consequences of early life exposure. Ann Glob Health 80:303–314CrossRefGoogle Scholar
  75. 75.
    Tota S, Kamat PK, Awasthi H, Singh N, Raghubir R, Nath C, Hanif K (2009) Candesartan improves memory decline in mice: involvement of AT1 receptors in memory deficit induced by intracerebral streptozotocin. Behav Brain Res 199:235–240CrossRefGoogle Scholar
  76. 76.
    Tseng HP, Wang YH, Wu MM, The HW, Chiou HY, Chen CJ (2006) Association between chronic exposure to arsenic and slow nerve conduction velocity among adolescents in Taiwan. J Health Popul Nutr 24:182–189Google Scholar
  77. 77.
    Tyler CR, Allan AM (2013) Adult hippocampal neurogenesis and mRNA expression are altered by perinatal arsenic exposure in mice and restored by brief exposure to enrichment. PLoS One 8:e73720CrossRefGoogle Scholar
  78. 78.
    Vahter M (2009) Effects of arsenic on maternal and fetal health. Annu Rev Nutr 29:381–399CrossRefGoogle Scholar
  79. 79.
    Valeri L, Mazumdar MM, Bobb JF, Claus Henn B, Rodrigues E, Sharif OIA, Kile ML, Quamruzzaman Q, Afroz S, Golam M, Amarasiriwardena C, Bellinger DC, Christiani DC, Coull BA, Wright RO (2017) The joint effect of prenatal exposure to metal mixtures on neurodevelopmental outcomes at 20–40 months of age: evidence from rural Bangladesh. Environ Health Perspect 125:067015CrossRefGoogle Scholar
  80. 80.
    Vathana T, Nijhuis TH, Friedrich PF, Bishop AT, Shin AY (2014) An experimental study to determine and correlate choline acetyltransferase assay with functional muscle testing after nerve injury. J Neurosurg 120:1125–1130CrossRefGoogle Scholar
  81. 81.
    von Ehrenstein OS, Poddar S, Yuan Y, Mazumder DG, Eskenazi B, Basu A, Hira-Smith M, Ghosh N, Lahiri S, Haque R, Ghosh A, Kalman D, Das S, Smith AH (2007) Children's intellectual function in relation to arsenic exposure. Epidemiology 1:44–51CrossRefGoogle Scholar
  82. 82.
    Vorhees CV, Brunner RL, Butcher RE (1979) Psychotropic drugs as behavioral teratogens. Science 205:1220–1225CrossRefGoogle Scholar
  83. 83.
    Wang X, Li W, Li S, Yan J, Wilson JX, Huang G (2017) Maternal folic acid supplementation during pregnancy improves neurobehavioral development in rat offspring. Mol Neurobiol 55:2676–2684.  https://doi.org/10.1007/s12035-017-0534-2 CrossRefGoogle Scholar
  84. 84.
    WHO (2008) “Guidelines for drinking-water quality, recommendations,” in Incorporating 1st and 2nd Addenda. Vol. 1, 3rd Edn (Geneva: World Health Organization), 306–308bGoogle Scholar
  85. 85.
    Willhite CC, Ferm VH (1984) Prenatal and developmental toxicology of arsenicals. Adv Exp Med Biol 177:205–228CrossRefGoogle Scholar
  86. 86.
    Wu J, Song TB, Li YJ, He KS, Ge L, Wang LR (2007) Prenatal restraint stress impairs learning and memory and hippocampal PKCbeta1 expression and translocation in offspring rats. Brain Res 1141:205–213CrossRefGoogle Scholar
  87. 87.
    Yadav RS, Chandravanshi LP, Shukla RK, Sankhwar ML, Ansari RW, Shukla PK, Pant AB, Khanna VK (2011) Neuroprotective efficacy of curcumin in arsenic induced cholinergic dysfunctions in rats. Neurotoxicology 32:760–768CrossRefGoogle Scholar
  88. 88.
    Zhang J, Liu X, Zhao L, Hu S, Li S, Piao F (2013) Subchronic exposure to arsenic disturbed the biogenic amine neurotransmitter level and the mRNA expression of synthetase in mice brains. Neuroscience 241:52–58CrossRefGoogle Scholar
  89. 89.
    Zhao F, Liao Y, Tang H, Piao J, Wang G, Jin Y (2017) Effects of developmental arsenite exposure on hippocampal synapses in mouse offspring. Metallomics 9:1394–1412CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Division of Forensic Science, School of Basic and Applied SciencesGalgotias UniversityGreater NoidaIndia
  2. 2.Developmental Toxicology DivisionCSIR–Indian Institute of Toxicology ResearchLucknowIndia
  3. 3.Department of BiochemistryAll India Institute of Medical SciencesBhopalIndia

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