Social Isolation-Induced Territorial Aggression in Male Offspring Is Enhanced by Exposure to Diesel Exhaust during Pregnancy
Open accessAbstract
Diesel exhaust particles are a major component of ambient particulate matter, and concern about the health effects of exposure to ambient particulate matter is growing. Previously, we found that in utero exposure to diesel exhaust affected locomotor activity and motor coordination, but there are also indications that such exposure may contribute to increased aggression in offspring. Therefore, the aim of the present study was to test the effects of prenatal diesel exhaust exposure on social isolation-induced territorial aggression. Pregnant mice were exposed to low concentrations of diesel exhaust (DE; mass concentration of 90 μg/m3: DE group: n = 15) or clean air (control group: n = 15) for 8 h/day during gestation. Basal locomotion of male offspring was measured at 10 weeks of age. Thereafter, male offspring were individually housed for 2 weeks and subsequently assessed for aggression using the resident-intruder test at 12 weeks of age, and blood and brain tissue were collected from the male offspring on the following day for measuring serum testosterone levels and neurochemical analysis. There were no significant differences in locomotion between control and DE-exposed mice. However, DE-exposed mice showed significantly greater social isolation-induced territorial aggressive behavior than control mice. Additionally, socially-isolated DE-exposed mice expressed significantly higher concentrations of serum testosterone levels than control mice. Neurochemical analysis revealed that dopamine levels in the prefrontal cortex and nucleus accumbens were higher in socially isolated DE-exposed mice. Serotonin levels in the nucleus accumbens, amygdala, and hypothalamus were also lower in the socially isolated DE-exposed mice than in control mice. Thus, even at low doses, prenatal exposure to DE increased aggression and serum testosterone levels, and caused neurochemical changes in male socially isolated mice. These results may have serious implications for pregnant women living in regions with high levels of traffic-related air pollution.
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Male offspring exposed to low-level diesel exhaust during the prenatal period had significantly greater social isolation-induced territorial aggressive behavior compared with controls, correlated with higher serum testosterone levels.
“Additionally, Yokota et al. [97] observed male offspring exposed to low level DE during the prenatal period had significantly greater social isolation-induced territorial aggressive behavior in comparison to control mice. This behavior correlated with higher serum testosterone levels in exposed males.”
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 [97]
The Abstract reports significantly greater social isolation-induced territorial aggression in male offspring prenatally exposed to low-level diesel exhaust. The Results also report approximately twofold higher serum testosterone in exposed residents, but the paper presents these as separate group comparisons, not a measured correlation between testosterone and aggressive behavior. (LLM, conf=0.85)
Experimental — accuracy not yet measuredIn several prenatal mouse exposure models, DE concentrations have ranged from 90 to 300 μg/m3 PM2.5.
“In several prenatal mouse exposure models, DE concentrations have ranged from 90 to 300 μg/m3 PM2.5 [97–100].”
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 [97]
In socially isolated DE-exposed mice, dopamine levels were higher in the prefrontal cortex and nucleus accumbens, whereas serotonin levels were lower in the nucleus accumbens, amygdala, and hypothalamus.
“Likewise, dopamine levels were higher in the prefrontal cortex and nucleus accumbens, a functional part of the reward system, whereas serotonin levels were lower in the nucleus accumbens, amygdala, and hypothalamus in socially isolated DE-exposed mice.”
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 [97]
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Johnson, N. M., Hoffmann, A. R., Behlen, J. C., Lau, C., Pendleton, D., Harvey, N., Shore, R., Li, Y., Chen, J., Tian, Y., et al. (2021) · Environmental Health and Preventive Medicine · doi:10.1186/s12199-021-00995-5 · Cited by 339 · see citing works
“[97] observed male offspring exposed to low level DE during the prenatal period had significantly greater social isolationinduced territorial aggressive behavior in comparison to control mice.”
BackgroundResultWoodward, N. C., Haghani, A., Johnson, R. G., Hsu, T. M., Saffari, A., Sioutas, C., Kanoski, S. E., Finch, C. E., & Morgan, T. E. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0317-1 · Cited by 118 · see citing works
- Authors
- Yokota, S., Oshio, S., Moriya, N., & Takeda, K.
- Affiliations
- Tokyo University of Science (JP)
- Ohu University (JP)
- Hyogo University of Health Sciences (JP)
- Corresponding author
- Yokota, Satoshi
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2016-02-26
- Volume
- 11
- Issue
- 2
- Pages
- e0149737
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4769130
- OpenAlex
- W2281806709
- Cited by
- 58
- References
- 3
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 8 · 2023: 9 · 2022: 6 · 2021: 9 · 2020: 2 · 2019: 7 · 2018: 4 · 2017: 6 · 2016: 1
- FWCI
- 3.77
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology
- Japan Society for the Promotion of Science
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Air Quality and Health Impacts
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Keywords
- diesel exhaust, prenatal exposure, social isolation, territorial aggression, male offspring, testosterone, dopamine, serotonin, neurochemistry, resident-intruder test, locomotor activity, traffic-related air pollution, gestation, mice
- MeSH terms
- Aggression, Animals, Vehicle Emissions, Body Weight, Dopamine, Female, Male, Mice, Inbred ICR, Motor Activity, Pregnancy, Prenatal Exposure Delayed Effects, Serotonin, Social Isolation, Testosterone
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