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Current Environmental Health Reports

, Volume 4, Issue 2, pp 180–191 | Cite as

Cognitive Effects of Air Pollution Exposures and Potential Mechanistic Underpinnings

  • J. L. Allen
  • C. Klocke
  • K. Morris-Schaffer
  • K. Conrad
  • M. Sobolewski
  • D. A. Cory-SlechtaEmail author
Mechanisms of Toxicity (JR Richardson, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Mechanisms of Toxicity

Abstract

Purpose of Review

This review sought to address the potential for air pollutants to impair cognition and mechanisms by which that might occur.

Recent Findings

Air pollution has been associated with deficits in cognitive functions across a wide range of epidemiological studies, both with developmental and adult exposures. Studies in animal models are significantly more limited in number, with somewhat inconsistent findings to date for measures of learning, but show more consistent impairments for short-term memory. Potential contributory mechanisms include oxidative stress/inflammation, altered levels of dopamine and/or glutamate, and changes in synaptic plasticity/structure.

Summary

Epidemiological studies are consistent with adverse effects of air pollutants on cognition, but additional studies and better phenotypic characterization are needed for animal models, including more precise delineation of specific components of cognition that are affected, as well as definitions of critical exposure periods for such effects and the components of air pollution responsible. This would permit development of more circumscribed hypotheses as to potential behavioral and neurobiological mechanisms.

Keywords

Air pollution Learning Memory Attention Inflammation Glutamate 

Notes

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does contain studies with animal subjects performed by the authors.

References

Papers of particular interest, published recently, have been highlighted as: •Of importance

  1. 1.
    Forouzanfar MH, Alexander L, Anderson HR, Bachman VF, Biryukov S, Brauer M, et al. Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks in 188 countries, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2015:2287–323. Doi: 10.1016/S0140-6736(15)00128-2.
  2. 2.
    Lelieveld J, Evans JS, Fnais M, Giannadaki D, Pozzer A. The contribution of outdoor air pollution sources to premature mortality on a global scale. Nature. 2015;525(7569):367–71. doi: 10.1038/nature15371.CrossRefPubMedGoogle Scholar
  3. 3.
    Kumar P, Morawska L, Birmili W, Paasonen P, Hu M, Kulmala M, et al. Ultrafine particles in cities. Environ Int. 2014;66:1–10. doi: 10.1016/j.envint.2014.01.013.CrossRefPubMedGoogle Scholar
  4. 4.
    Oberdorster G, Ferin J, Lehnert BE. Correlation between particle size, in vivo particle persistence, and lung injury. Environ Health Perspect. 1994;102(Suppl 5):173–9.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Brown DM, Wilson MR, MacNee W, Stone V, Donaldson K. Size-dependent proinflammatory effects of ultrafine polystyrene particles: a role for surface area and oxidative stress in the enhanced activity of ultrafines. Toxicol Appl Pharmacol. 2001;175(3):191–9. doi: 10.1006/taap.2001.9240.CrossRefPubMedGoogle Scholar
  6. 6.
    Elder A, Gelein R, Silva V, Feikert T, Opanashuk L, Carter J, et al. Translocation of inhaled ultrafine manganese oxide particles to the central nervous system. Environ Health Perspect. 2006;114(8):1172–8.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Lewis J, Bench G, Myers O, Tinner B, Staines W, Barr E, et al. Trigeminal uptake and clearance of inhaled manganese chloride in rats and mice. Neurotoxicology. 2005;26(1):113–23. doi: 10.1016/j.neuro.2004.06.005.CrossRefPubMedGoogle Scholar
  8. 8.
    Ruuskanen J, Tuch T, Brink T, Peters A, Khlystov A, Mirme A, et al. Concentrations of ultrafine, fine and PM2.5 particles in three European cities. Atmos Environ. 2001;35:3729–8.CrossRefGoogle Scholar
  9. 9.
    Pitz M, Kreyling WG, Holscher B, Cyrys J, Wichmann HE, Heinrich J. Change of the ambient particle size distribution in East Germany between 1993 and 1999. Atmos Environ. 2001;35(25):4357–66. doi: 10.1016/S1352-2310(01)00229-1.CrossRefGoogle Scholar
  10. 10.
    Martins LD, Martins JA, Freitas ED, Mazzoli CR, Goncalves FLT, Ynoue RY, et al. Potential health impact of ultrafine particles under clean and polluted urban atmospheric conditions: a model-based study. Air Quality Atmosphere and Health. 2010;3(1):29–39. doi: 10.1007/s11869-009-0048-9.CrossRefGoogle Scholar
  11. 11.
    Frank BP, Tang S, Lanni T, Grygas J, Rideout G, Meyer N, et al. The effect of fuel type and aftertreatment method on ultrafine particle emissions from a heavy-duty diesel engine. Aerosol Sci Technol. 2007;41(11):1029–39. doi: 10.1080/02786820701697531.CrossRefGoogle Scholar
  12. 12.
    Ristovski ZD, Jayaratne ER, Lim M, Ayoko GA, Morawska L. Influence of diesel fuel sulfur on nanoparticle emissions from city buses. Environmental Science & Technology. 2006;40(4):1314–20. doi: 10.1021/es050094i.CrossRefGoogle Scholar
  13. 13.
    Costa LG, Cole TB, Coburn J, Chang YC, Dao K, Roque PJ. Neurotoxicity of traffic-related air pollution. Neurotoxicology. 2015; doi: 10.1016/j.neuro.2015.11.008.PubMedCentralGoogle Scholar
  14. 14.
    Heusinkveld HJ, Wahle T, Campbell A, Westerink RH, Tran L, Johnston H, et al. Neurodegenerative and neurological disorders by small inhaled particles. Neurotoxicology. 2016;56:94–106. doi: 10.1016/j.neuro.2016.07.007.CrossRefPubMedGoogle Scholar
  15. 15.
    Power MC, Adar SD, Yanosky JD, Weuve J. Exposure to air pollution as a potential contributor to cognitive function, cognitive decline, brain imaging, and dementia: a systematic review of epidemiologic research. Neurotoxicology. 2016; doi: 10.1016/j.neuro.2016.06.004.PubMedGoogle Scholar
  16. 16.
    Xu X, Ha SU, Basnet R. A review of epidemiological research on adverse neurological effects of exposure to ambient air pollution. Front Public Health. 2016;4:157. doi: 10.3389/fpubh.2016.00157.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    • Block ML, Calderon-Garciduenas L. Air pollution: mechanisms of neuroinflammation and CNS disease. Trends Neurosci. 2009;32(9):506–16. doi: 10.1016/j.tins.2009.05.009. Review of potential peripheral and CNS mechanisms of air pollution-induced neurotoxicity CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Clifford A, Lang L, Chen R, Anstey KJ, Seaton A. Exposure to air pollution and cognitive functioning across the life course—a systematic literature review. Environ Res. 2016;147:383–98. doi: 10.1016/j.envres.2016.01.018.CrossRefPubMedGoogle Scholar
  19. 19.
    Guxens M, Sunyer J. A review of epidemiological studies on neuropsychological effects of air pollution. Swiss Med Wkly. 2012;141:w13322. doi: 10.4414/smw.2011.13322.PubMedGoogle Scholar
  20. 20.
    Peters R, Peters J, Booth A, Mudway I. Is air pollution associated with increased risk of cognitive decline? A systematic review. Age Ageing. 2015;44(5):755–60. doi: 10.1093/ageing/afv087.CrossRefPubMedGoogle Scholar
  21. 21.
    Suades-Gonzalez E, Gascon M, Guxens M, Sunyer J. Air pollution and neuropsychological development: a review of the latest evidence. Endocrinology. 2015:en20151403. doi: 10.1210/en.2015-1403.
  22. 22.
    Woodward N, Finch CE, Morgan TE. Traffic-related air pollution and brain development. AIMS Environ Sci. 2015;2(2):353–73. doi: 10.3934/environsci.2015.2.353.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Ranft U, Schikowski T, Sugiri D, Krutmann J, Kramer U. Long-term exposure to traffic-related particulate matter impairs cognitive function in the elderly. Environ Res. 2009;109(8):1004–11. doi: 10.1016/j.envres.2009.08.003.CrossRefPubMedGoogle Scholar
  24. 24.
    Schikowski T, Vossoughi M, Vierkotter A, Schulte T, Teichert T, Sugiri D, et al. Association of air pollution with cognitive functions and its modification by APOE gene variants in elderly women. Environ Res. 2015;142:10–6. doi: 10.1016/j.envres.2015.06.009.CrossRefPubMedGoogle Scholar
  25. 25.
    Tzivian L, Dlugaj M, Winkler A, Weinmayr G, Hennig F, Fuks KB, et al. Long-term air pollution and traffic noise exposures and mild cognitive impairment in older adults: a cross-sectional analysis of the Heinz Nixdorf Recall Study. Environ Health Perspect. 2016;124(9):1361–8. doi: 10.1289/ehp.1509824.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Colicino E, Wilson A, Frisardi MC, Prada D, Power MC, Hoxha M, et al. Telomere length, long-term black carbon exposure, and cognitive function in a cohort of older men: the VA Normative Aging Study. Environ Health Perspect. 2016; doi: 10.1289/EHP241.Google Scholar
  27. 27.
    Best EA, Juarez-Colunga E, James K, LeBlanc WG, Serdar B. Biomarkers of exposure to polycyclic aromatic hydrocarbons and cognitive function among elderly in the United States (National Health and Nutrition Examination Survey: 2001–2002). PLoS One. 2016;11(2):e0147632. doi: 10.1371/journal.pone.0147632.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Ailshire JA, Clarke P. Fine particulate matter air pollution and cognitive function among U.S. older adults. J Gerontol B Psychol Sci Soc Sci. 2015;70(2):322–8. doi: 10.1093/geronb/gbu064.CrossRefPubMedGoogle Scholar
  29. 29.
    Gatto NM, Henderson VW, Hodis HN, St John JA, Lurmann F, Chen JC, et al. Components of air pollution and cognitive function in middle-aged and older adults in Los Angeles. Neurotoxicology. 2014;40:1–7. doi: 10.1016/j.neuro.2013.09.004.CrossRefPubMedGoogle Scholar
  30. 30.
    • Weuve J, Puett RC, Schwartz J, Yanosky JD, Laden F, Grodstein F. Exposure to particulate air pollution and cognitive decline in older women. Arch Intern Med. 2012;172(3):219–27. doi: 10.1001/archinternmed.2011.683. Epidemiological study across 7-14 years showing that a 10 ug/m 3 increase in long-term PM exposure is the cognitive aging equivalent of approximately 2 years CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Tonne C, Elbaz A, Beevers S, Singh-Manoux A. Traffic-related air pollution in relation to cognitive function in older adults. Epidemiology. 2014;25(5):674–81. doi: 10.1097/EDE.0000000000000144.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Wellenius GA, Boyle LD, Coull BA, Milberg WP, Gryparis A, Schwartz J, et al. Residential proximity to nearest major roadway and cognitive function in community-dwelling seniors: results from the MOBILIZE Boston Study. J Am Geriatr Soc. 2012;60(11):2075–80. doi: 10.1111/j.1532-5415.2012.04195.x.PubMedPubMedCentralGoogle Scholar
  33. 33.
    Harris MH, Gold DR, Rifas-Shiman SL, Melly SJ, Zanobetti A, Coull BA, et al. Prenatal and childhood traffic-related pollution exposure and childhood cognition in the project viva cohort (Massachusetts, USA). Environ Health Perspect. 2015;123(10):1072–8. doi: 10.1289/ehp.1408803.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Harris MH, Gold DR, Rifas-Shiman SL, Melly SJ, Zanobetti A, Coull BA, et al. Prenatal and childhood traffic-related air pollution exposure and childhood executive function and behavior. Neurotoxicol Teratol. 2016; doi: 10.1016/j.ntt.2016.06.008.PubMedGoogle Scholar
  35. 35.
    Wang S, Zhang J, Zeng X, Zeng Y, Wang S, Chen S. Association of traffic-related air pollution with childrenʼs neurobehavioral functions in Quanzhou. China Environ Health Perspect. 2009;117(10):1612–8. doi: 10.1289/ehp.0800023.CrossRefPubMedGoogle Scholar
  36. 36.
    Suglia SF, Gryparis A, Wright RO, Schwartz J, Wright RJ. Association of black carbon with cognition among children in a prospective birth cohort study. Am J Epidemiol. 2008;167(3):280–6. doi: 10.1093/aje/kwm308.CrossRefPubMedGoogle Scholar
  37. 37.
    van Kempen E, Fischer P, Janssen N, Houthuijs D, van Kamp I, Stansfeld S, et al. Neurobehavioral effects of exposure to traffic-related air pollution and transportation noise in primary school children. Environ Res. 2012;115:18–25. doi: 10.1016/j.envres.2012.03.002.CrossRefPubMedGoogle Scholar
  38. 38.
    Guxens M, Garcia-Esteban R, Giorgis-Allemand L, Forns J, Badaloni C, Ballester F, et al. Air pollution during pregnancy and childhood cognitive and psychomotor development: six European birth cohorts. Epidemiology. 2014;25(5):636–47. doi: 10.1097/EDE.0000000000000133.CrossRefPubMedGoogle Scholar
  39. 39.
    Jedrychowski WA, Perera FP, Camann D, Spengler J, Butscher M, Mroz E, et al. Prenatal exposure to polycyclic aromatic hydrocarbons and cognitive dysfunction in children. Environ Sci Pollut Res Int. 2015;22(5):3631–9. doi: 10.1007/s11356-014-3627-8.CrossRefPubMedGoogle Scholar
  40. 40.
    Kicinski M, Vermeir G, Van Larebeke N, Den Hond E, Schoeters G, Bruckers L, et al. Neurobehavioral performance in adolescents is inversely associated with traffic exposure. Environ Int. 2015;75:136–43. doi: 10.1016/j.envint.2014.10.028.CrossRefPubMedGoogle Scholar
  41. 41.
    Siddique S, Banerjee M, Ray MR, Lahiri T. Attention-deficit hyperactivity disorder in children chronically exposed to high level of vehicular pollution. Eur J Pediatr. 2011;170(7):923–9. doi: 10.1007/s00431-010-1379-0.CrossRefPubMedGoogle Scholar
  42. 42.
    Newman NC, Ryan P, Lemasters G, Levin L, Bernstein D, Hershey GK, et al. Traffic-related air pollution exposure in the first year of life and behavioral scores at 7 years of age. Environ Health Perspect. 2013;121(6):731–6. doi: 10.1289/ehp.1205555.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Gong T, Almqvist C, Bolte S, Lichtenstein P, Anckarsater H, Lind T, et al. Exposure to air pollution from traffic and neurodevelopmental disorders in Swedish twins. Twin Res Hum Genet. 2014;17(6):553–62. doi: 10.1017/thg.2014.58.CrossRefPubMedGoogle Scholar
  44. 44.
    Sunyer J, Esnaola M, Alvarez-Pedrerol M, Forns J, Rivas I, Lopez-Vicente M, et al. Association between traffic-related air pollution in schools and cognitive development in primary school children: a prospective cohort study. PLoS Med. 2015;12(3):e1001792. doi: 10.1371/journal.pmed.1001792.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    • Basagana X, Esnaola M, Rivas I, Amato F, Alvarez-Pedrerol M, Forns J, et al. Neurodevelopmental deceleration by urban fine particles from different emission sources: a longitudinal observational study. Environ Health Perspect. 2016:124(5). doi: 10.1289/EHP209. Epidemiological study reporting that even an increase of an interquartile range in indoor traffic-related PM 2.5 was associated with reductions in cognitive growth, working memory and inattentiveness that ranged from 11–30%.
  46. 46.
    Kim E, Park H, Hong YC, Ha M, Kim Y, Kim BN, et al. Prenatal exposure to PM(1)(0) and NO(2) and childrenʼs neurodevelopment from birth to 24 months of age: mothers and Childrenʼs Environmental Health (MOCEH) study. Sci Total Environ. 2014;481:439–45. doi: 10.1016/j.scitotenv.2014.01.107.CrossRefPubMedGoogle Scholar
  47. 47.
    Hougaard KS, Jensen KA, Nordly P, Taxvig C, Vogel U, Saber AT, et al. Effects of prenatal exposure to diesel exhaust particles on postnatal development, behavior, genotoxicity and inflammation in mice. Part Fibre Toxicol. 2008;5:3. doi: 10.1186/1743-8977-5-3.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Yokota S, Sato A, Umezawa M, Oshio S, Takeda K. In utero exposure of mice to diesel exhaust particles affects spatial learning and memory with reduced N-methyl-D-aspartate receptor expression in the hippocampus of male offspring. Neurotoxicology. 2015;50:108–15. doi: 10.1016/j.neuro.2015.08.009.CrossRefPubMedGoogle Scholar
  49. 49.
    Win-Shwe TT, Yamamoto S, Fujitani Y, Hirano S, Fujimaki H. Nanoparticle-rich diesel exhaust affects hippocampal-dependent spatial learning and NMDA receptor subunit expression in female mice. Nanotoxicology. 2012;6(5):543–53. doi: 10.3109/17435390.2011.590904.CrossRefPubMedGoogle Scholar
  50. 50.
    Win-Shwe TT, Fujimaki H, Fujitani Y, Hirano S. Novel object recognition ability in female mice following exposure to nanoparticle-rich diesel exhaust. Toxicol Appl Pharmacol. 2012;262(3):355–62. doi: 10.1016/j.taap.2012.05.015.CrossRefPubMedGoogle Scholar
  51. 51.
    Win-Shwe TT, Fujitani Y, Kyi-Tha-Thu C, Furuyama A, Michikawa T, Tsukahara S, et al. Effects of diesel engine exhaust origin secondary organic aerosols on novel object recognition ability and maternal behavior in BALB/c mice. Int J Environ Res Public Health. 2014;11(11):11286–307. doi: 10.3390/ijerph111111286.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Fonken LK, Xu X, Weil ZM, Chen G, Sun Q, Rajagopalan S, et al. Air pollution impairs cognition, provokes depressive-like behaviors and alters hippocampal cytokine expression and morphology. Mol Psychiatry. 2011;16(10):987–95. 73 doi: 10.1038/mp.2011.76.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Allen JL, Liu X, Weston D, Prince L, Oberdorster G, Finkelstein JN, et al. Developmental exposure to concentrated ambient ultrafine particulate matter air pollution in mice results in persistent and sex-dependent behavioral neurotoxicity and glial activation. Toxicol Sci. 2014;140(1):160–78. doi: 10.1093/toxsci/kfu059.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Allen JL, Conrad K, Oberdorster G, Johnston CJ, Sleezer B, Cory-Slechta DA. Developmental exposure to concentrated ambient particles and preference for immediate reward in mice. Environ Health Perspect. 2013;121(1):32–8. doi: 10.1289/ehp.1205505.CrossRefPubMedGoogle Scholar
  55. 55.
    Zanchi AC, Fagundes LS, Barbosa Jr F, Bernardi R, Rhoden CR, Saldiva PH, et al. Pre and post-natal exposure to ambient level of air pollution impairs memory of rats: the role of oxidative stress. Inhal Toxicol. 2010;22(11):910–8. doi: 10.3109/08958378.2010.494313.CrossRefPubMedGoogle Scholar
  56. 56.
    Dong J, Shang Y, Inthavong K, Tu J, Chen R, Bai R, et al. From the cover: comparative numerical modeling of inhaled nanoparticle deposition in human and rat nasal cavities. Toxicol Sci. 2016;152(2):284–96. doi: 10.1093/toxsci/kfw087.CrossRefPubMedGoogle Scholar
  57. 57.
    Garcia GJ, Schroeter JD, Kimbell JS. Olfactory deposition of inhaled nanoparticles in humans. Inhal Toxicol. 2015;27(8):394–403. doi: 10.3109/08958378.2015.1066904.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Pedata P, Stoeger T, Zimmermann R, Peters A, Oberdorster G, D’Anna A. Are we forgetting the smallest, sub 10 nm combustion generated particles? Part Fibre Toxicol. 2017.Google Scholar
  59. 59.
    Ronkko T, Virtanen A, Kannosto J, Keskinen J, Lappi M, Pirjola L. Nucleation mode particles with a nonvolatile core in the exhaust of a heavy duty diesel vehicle. Environ Sci Technol. 2007;41:6384–9.CrossRefPubMedGoogle Scholar
  60. 60.
    Win-Shwe TT, Yamamoto S, Fujitani Y, Hirano S, Fujimaki H. Spatial learning and memory function-related gene expression in the hippocampus of mouse exposed to nanoparticle-rich diesel exhaust. Neurotoxicology. 2008;29(6):940–7. doi: 10.1016/j.neuro.2008.09.007.CrossRefPubMedGoogle Scholar
  61. 61.
    Costa LG, Cole TB, Coburn J, Chang YC, Dao K, Roque P. Neurotoxicants are in the air: convergence of human, animal, and in vitro studies on the effects of air pollution on the brain. Biomed Res Int. 2014;2014:736385. doi: 10.1155/2014/736385.PubMedPubMedCentralGoogle Scholar
  62. 62.
    Karadottir R, Attwell D. Neurotransmitter receptors in the life and death of oligodendrocytes. Neuroscience. 2007;145(4):1426–38. doi: 10.1016/j.neuroscience.2006.08.070.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Volpe JJ, Kinney HC, Jensen FE, Rosenberg PA. The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int J Dev Neurosci. 2011;29(4):423–40. doi: 10.1016/j.ijdevneu.2011.02.012.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Biber K, Neumann H, Inoue K, Boddeke HW. Neuronal ‘Onʼ and ‘Offʼ signals control microglia. Trends Neurosci. 2007;30(11):596–602. doi: 10.1016/j.tins.2007.08.007.CrossRefPubMedGoogle Scholar
  65. 65.
    Kaur C, Ling EA. Periventricular white matter damage in the hypoxic neonatal brain: role of microglial cells. Prog Neurobiol. 2009;87(4):264–80. doi: 10.1016/j.pneurobio.2009.01.003.CrossRefPubMedGoogle Scholar
  66. 66.
    Matute C, Alberdi E, Domercq M, Sanchez-Gomez MV, Perez-Samartin A, Rodriguez-Antiguedad A, et al. Excitotoxic damage to white matter. J Anat. 2007;210(6):693–702. doi: 10.1111/j.1469-7580.2007.00733.x.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Schmitz T, Krabbe G, Weikert G, Scheuer T, Matheus F, Wang Y, et al. Minocycline protects the immature white matter against hyperoxia. Exp Neurol. 2014;254:153–65. doi: 10.1016/j.expneurol.2014.01.017.CrossRefPubMedGoogle Scholar
  68. 68.
    Schwarz JM, Bilbo SD. Sex, glia, and development: interactions in health and disease. Horm Behav. 2012;62(3):243–53. doi: 10.1016/j.yhbeh.2012.02.018.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Tay TL, Savage J, Hui CW, Bisht K, Tremblay ME. Microglia across the lifespan: from origin to function in brain development, plasticity and cognition. J Physiol. 2016; doi: 10.1113/JP272134.PubMedGoogle Scholar
  70. 70.
    Skaper SD, Facci L, Giusti P. Neuroinflammation, microglia and mast cells in the pathophysiology of neurocognitive disorders: a review. CNS Neurol Disord Drug Targets. 2014;13(10):1654–66.CrossRefPubMedGoogle Scholar
  71. 71.
    Voytek B, Knight RT. Dynamic network communication as a unifying neural basis for cognition, development, aging, and disease. Biol Psychiatry. 2015;77(12):1089–97. doi: 10.1016/j.biopsych.2015.04.016.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Pavlova MA, Krageloh-Mann I. Limitations on the developing preterm brain: impact of periventricular white matter lesions on brain connectivity and cognition. Brain. 2013;136(Pt 4):998–1011. doi: 10.1093/brain/aws334.CrossRefPubMedGoogle Scholar
  73. 73.
    Gerlofs-Nijland ME, van Berlo D, Cassee FR, Schins RP, Wang K, Campbell A. Effect of prolonged exposure to diesel engine exhaust on proinflammatory markers in different regions of the rat brain. Part Fibre Toxicol. 2010;7:12. doi: 10.1186/1743-8977-7-12.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Levesque S, Taetzsch T, Lull ME, Kodavanti U, Stadler K, Wagner A, et al. Diesel exhaust activates and primes microglia: air pollution, neuroinflammation, and regulation of dopaminergic neurotoxicity. Environ Health Perspect. 2011;119(8):1149–55. doi: 10.1289/ehp.1002986.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Roque PJ, Dao K, Costa LG. Microglia mediate diesel exhaust particle-induced cerebellar neuronal toxicity through neuroinflammatory mechanisms. Neurotoxicology. 2016;56:204–14. doi: 10.1016/j.neuro.2016.08.006.CrossRefPubMedGoogle Scholar
  76. 76.
    Allen JL, Liu X, Pelkowski S, Palmer B, Conrad K, Oberdorster G, et al. Early postnatal exposure to ultrafine particulate matter air pollution: persistent ventriculomegaly, neurochemical disruption, and glial activation preferentially in male mice. Environ Health Perspect. 2014;122(9):939–45. doi: 10.1289/ehp.1307984.PubMedPubMedCentralGoogle Scholar
  77. 77.
    • Allen JL, Oberdorster G, Morris-Schaffer K, Wong C, Klocke C, Sobolewski M, et al. Developmental neurotoxicity of inhaled ambient ultrafine particle air pollution: parallels with neuropathological and behavioral features of autism and other neurodevelopmental disorders. Neurotoxicology. 2015; doi: 10.1016/j.neuro.2015.12.014. Mouse model of human third trimester equivalent exposure to ultrafine particles demonstratingneuropathological, neurochemical and behavioral consequences that parallel those seen in many human neurodevelopmental disorders. Google Scholar
  78. 78.
    Guo L, Li B, Miao JJ, Yun Y, Li GK, Sang N. Seasonal variation in air particulate matter (PM10) exposure-induced ischemia-like injuries in the rat brain. Chem Res Toxicol. 2015;28(3):431–9. doi: 10.1021/tx500392n.CrossRefPubMedGoogle Scholar
  79. 79.
    Cheng H, Saffari A, Sioutas C, Forman HJ, Morgan TE, Finch CE. Nano-scale particulate matter from urban traffic rapidly induces oxidative stress and inflammation in olfactory epithelium with concomitant effects on brain. Environ Health Perspect. 2016; doi: 10.1289/EHP134.Google Scholar
  80. 80.
    Chen JC, Wang X, Wellenius GA, Serre ML, Driscoll I, Casanova R, et al. Ambient air pollution and neurotoxicity on brain structure: evidence from Womenʼs Health Initiative Memory Study. Ann Neurol. 2015; doi: 10.1002/ana.24460.Google Scholar
  81. 81.
    Pujol J, Martinez-Vilavella G, Macia D, Fenoll R, Alvarez-Pedrerol M, Rivas I, et al. Traffic pollution exposure is associated with altered brain connectivity in school children. NeuroImage. 2016;129:175–84. doi: 10.1016/j.neuroimage.2016.01.036.CrossRefPubMedGoogle Scholar
  82. 82.
    Peterson D, Mahajan R, Crocetti D, Mejia A, Mostofsky S. Left-hemispheric microstructural abnormalities in children with high-functioning autism spectrum disorder. Autism Res. 2015;8(1):61–72. doi: 10.1002/aur.1413.CrossRefPubMedGoogle Scholar
  83. 83.
    Cepeda C, Andre VM, Jocoy EL, Levine MS. NMDA and dopamine: diverse mechanisms applied to interacting receptor systems. In: Van Dongen AM, editor. Biology of the NMDA receptor. Boca Raton: Frontiers in Neuroscience; 2009.Google Scholar
  84. 84.
    Wang M, Wong AH, Liu F. Interactions between NMDA and dopamine receptors: a potential therapeutic target. Brain Res. 2012;1476:154–63. doi: 10.1016/j.brainres.2012.03.029.CrossRefPubMedGoogle Scholar
  85. 85.
    Win-Shwe TT, Kyi-Tha-Thu C, Moe Y, Fujitani Y, Tsukahara S, Hirano S. Exposure of BALB/c mice to diesel engine exhaust origin secondary organic aerosol (DE-SOA) during the developmental stages impairs the social behavior in adult life of the males. Front Neurosci. 2015;9:524. doi: 10.3389/fnins.2015.00524.PubMedGoogle Scholar
  86. 86.
    Win-Shwe TT, Fujimaki H, Fujitani Y, Hirano S. Novel object recognition ability in female mice following exposure to nanoparticle-rich diesel exhaust. Toxicol Appl Pharmacol. 2012;262(3):355–62. doi: 10.1016/j.taap.2012.05.015.CrossRefPubMedGoogle Scholar
  87. 87.
    Cory-Slechta DA, Virgolini MB, Rossi-George A, Weston D, Thiruchelvam M. Experimental manipulations blunt time-induced changes in brain monoamine levels and completely reverse stress, but not Pb+/− stress-related modifications to these trajectories. Behav Brain Res. 2009;205(1):76–87.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Cory-Slechta DA, Merchant-Borna K, Allen J, Liu S, Weston D, Conrad K. Variations in the nature of behavioral experience can differentially alter the consequences of developmental exposures to lead, prenatal stress and the combination. Toxicol Sci. 2013;131:194–205. doi: 10.1093/toxsci/kfs260.CrossRefPubMedGoogle Scholar
  89. 89.
    Yokota S, Mizuo K, Moriya N, Oshio S, Sugawara I, Takeda K. Effect of prenatal exposure to diesel exhaust on dopaminergic system in mice. Neurosci Lett. 2009;449(1):38–41. doi: 10.1016/j.neulet.2008.09.085.CrossRefPubMedGoogle Scholar
  90. 90.
    Yokota S, Moriya N, Iwata M, Umezawa M, Oshio S, Takeda K. Exposure to diesel exhaust during fetal period affects behavior and neurotransmitters in male offspring mice. J Toxicol Sci. 2013;38(1):13–23.CrossRefPubMedGoogle Scholar
  91. 91.
    Yokota S, Oshio S, Moriya N, Takeda K. Social isolation-induced territorial aggression in male offspring is enhanced by exposure to diesel exhaust during pregnancy. PLoS One. 2016;11(2):e0149737. doi: 10.1371/journal.pone.0149737.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Suzuki T, Oshio S, Iwata M, Saburi H, Odagiri T, Udagawa T, et al. In utero exposure to a low concentration of diesel exhaust affects spontaneous locomotor activity and monoaminergic system in male mice. Part Fibre Toxicol. 2010;7:7. doi: 10.1186/1743-8977-7-7.CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Allen JL, Liu X, Weston D, Conrad K, Oberdorster G, Cory-Slechta DA. Consequences of developmental exposure to concentrated ambient ultrafine particle air pollution combined with the adult paraquat and maneb model of the Parkinsonʼs disease phenotype in male mice. Neurotoxicology. 2014;41:80–8. doi: 10.1016/j.neuro.2014.01.004.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Morgan TE, Davis DA, Iwata N, Tanner JA, Snyder D, Ning Z, et al. Glutamatergic neurons in rodent models respond to nanoscale particulate urban air pollutants in vivo and in vitro. Environ Health Perspect. 2011;119(7):1003–9. doi: 10.1289/ehp.1002973.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Halassa MM, Fellin T, Haydon PG. The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol Med. 2007;13(2):54–63. doi: 10.1016/j.molmed.2006.12.005.CrossRefPubMedGoogle Scholar
  96. 96.
    Davis DA, Bortolato M, Godar SC, Sander TK, Iwata N, Pakbin P, et al. Prenatal exposure to urban air nanoparticles in mice causes altered neuronal differentiation and depression-like responses. PLoS One. 2013;8(5):e64128. doi: 10.1371/journal.pone.0064128.CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Cheng H, Davis DA, Hasheminassab S, Sioutas C, Morgan TE, Finch CE. Urban traffic-derived nanoparticulate matter reduces neurite outgrowth via TNFalpha in vitro. J Neuroinflammation. 2016;13:19. doi: 10.1186/s12974-016-0480-3.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Cory-Slechta DA. Behavioral measures of neurotoxicity. Neurotoxicology. 1989;10:271–95.PubMedGoogle Scholar
  99. 99.
    Cory-Slechta D, Weiss B. Assessment of behavioral toxicity. In: Hayes AW, Kruger CL, editors. Principles and methods of toxicology. 6th ed. New York: CRC Press Taylor and Francis; 2014. p. 1831–90.Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • J. L. Allen
    • 1
  • C. Klocke
    • 1
  • K. Morris-Schaffer
    • 1
  • K. Conrad
    • 1
  • M. Sobolewski
    • 1
  • D. A. Cory-Slechta
    • 2
    Email author
  1. 1.Department of Environmental MedicineUniversity of Rochester Medical CenterRochesterUSA
  2. 2.Box EHSCUniversity of Rochester Medical CenterRochesterUSA

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