Developmental Exposure to Concentrated Ambient Ultrafine Particulate Matter Air Pollution in Mice Results in Persistent and Sex-Dependent Behavioral Neurotoxicity and Glial Activation
Open accessAbstract
The brain appears to be a target of air pollution. This study aimed to further ascertain behavioral and neurobiological mechanisms of our previously observed preference for immediate reward (Allen, J. L., Conrad, K., Oberdorster, G., Johnston, C. J., Sleezer, B., and Cory-Slechta, D. A. (2013). Developmental exposure to concentrated ambient particles and preference for immediate reward in mice. Environ. Health Perspect. 121, 32-38), a phenotype consistent with impulsivity, in mice developmentally exposed to inhaled ultrafine particles. It examined the impact of postnatal and/or adult concentrated ambient ultrafine particles (CAPS) or filtered air on another behavior thought to reflect impulsivity, Fixed interval (FI) schedule-controlled performance, and extended the assessment to learning/memory (novel object recognition (NOR)), and locomotor activity to assist in understanding behavioral mechanisms of action. In addition, levels of brain monoamines and amino acids, and markers of glial presence and activation (GFAP, IBA-1) were assessed in mesocorticolimbic brain regions mediating these cognitive functions. This design produced four treatment groups/sex of postnatal/adult exposure: Air/Air, Air/CAPS, CAPS/Air, and CAPS/CAPS. FI performance was adversely influenced by CAPS/Air in males, but by Air/CAPS in females, effects that appeared to reflect corresponding changes in brain mesocorticolimbic dopamine/glutamate systems that mediate FI performance. Both sexes showed impaired short-term memory on the NOR. Mechanistically, cortical and hippocampal changes in amino acids raised the potential for excitotoxicity, and persistent glial activation was seen in frontal cortex and corpus callosum of both sexes. Collectively, neurodevelopment and/or adulthood CAPS can produce enduring and sex-dependent neurotoxicity. Although mechanisms of these effects remain to be fully elucidated, findings suggest that neurodevelopment and/or adulthood air pollution exposure may represent a significant underexplored risk factor for central nervous system diseases/disorders and thus a significant public health threat even beyond current appreciation.
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Following early postnatal ultrafine PM exposure, both sexes showed impaired learning and short-term memory outcomes and persistent glial activation in the frontal cortex and corpus callosum.
“Following exposure, both sexes showed impaired learning and short-term memory outcomes and persistent glial activation in the frontal cortex and corpus callosum [56].”
From Air pollution and children’s health—a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter (2021) · cites this paper as [56]
The Abstract reports impaired short-term memory in both sexes, and the Discussion reports persistent glial activation in the cortex and corpus callosum. However, the Glial Activation results distinguish exposure timing and sex: postnatal exposure increased cortical markers in both sexes, while the female corpus callosum finding was only a trend associated with adult exposure. The claim overstates what early postnatal exposure produced across both sexes and regions. (LLM, conf=0.87)
Experimental — accuracy not yet measuredChanges in dopamine and glutamate systems known to mediate fixed interval performance coincided with phenotypic changes after PM exposure.
“Changes in dopamine and glutamate systems known to mediate FI performance coincided with phenotypic changes.”
From Air pollution and children’s health—a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter (2021) · cites this paper as [56]
Phenotypes related to impulsivity measured using fixed interval schedule-controlled performance tests vary based on sex and timing of exposure.
“Additional phenotypes related to impulsivity measured using fixed interval (FI) schedule-controlled performance tests reveal varied results based on sex and timing of exposure [56].”
From Air pollution and children’s health—a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter (2021) · cites this paper as [56]
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Percentages, sums and reported differences re-computed from the paper’s own numbers.
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“Following exposure, both sexes showed impaired learning and short-term memory outcomes and persistent glial activation in the frontal cortex and corpus callosum [56].”
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Self-citationHyperactivity disorder in children related to traffic-based air pollution during pregnancy
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- Authors
- Allen, J. L., Liu, X., Weston, D., Prince, L., Oberdörster, G., Finkelstein, J. N., Johnston, C. J., & Cory-Slechta, D. A.
- Affiliations
- University of Rochester Medicine (US)
- Venue
- Toxicological Sciences
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-04-01
- Volume
- 140
- Issue
- 1
- Pages
- 160-178
- ISSN
- 1096-0929 (ISSN-L)
- 1096-6080
- PMC
- PMC4081635
- OpenAlex
- W2132989726
- Cited by
- 168
- References
- 7
- Citations by year
- 2026: 11 · 2025: 12 · 2024: 14 · 2023: 13 · 2022: 22 · 2021: 12 · 2020: 21 · 2019: 21 · 2018: 12 · 2017: 10 · 2016: 11 · 2015: 6 · 2014: 3
- FWCI
- 6.58
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Toxicological Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Environmental Health Sciences (K12ES019852, P30 ES0 1247, R21ES019105, P30ES001247, T32ES007026, P30ES005022)
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Air Quality and Health Impacts
- Life Sciences › Immunology and Microbiology › Immunology › Immunotoxicology and immune responses
- Social Sciences › Sociology and Political Science › Environmental Justice and Health Disparities
- Keywords
- ultrafine particles, air pollution neurotoxicity, early life exposure, sex differences, impulsivity, novel object recognition, learning and memory, glial activation, excitotoxicity, brain amino acids, monoamines, glial fibrillary acidic protein, Iba1, hippocampus, frontal cortex, corpus callosum, mice
- MeSH terms
- Air Pollutants, Animals, Animals, Newborn, Behavior, Animal, Brain, Corticosterone, Female, Male, Mice, Inbred C57BL, Motor Activity, Neuroglia, Pattern Recognition, Visual, Sex Characteristics, Neurotransmitter Agents, Neurotoxicity Syndromes, Particulate Matter
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