Exposure to polystyrene microplastics reduces sociality and brain oxytocin levels through the gut-brain axis in mice

The rising global prevalence of microplastics (MPs) has highlighted their diverse toxicological effects. The oxytocin (OT) system in mammals, deeply intertwined with social behaviors, is recognized to be vulnerable to environmental stressors. We hypothesized that MP exposure might disrupt this syste...

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Veröffentlicht in:The Science of the total environment 2024-10, Vol.945, p.174026, Article 174026
Hauptverfasser: Wang, Limin, Li, Shuxin, Hao, Yaotong, Liu, Xu, Liu, Yaqing, Zuo, Lirong, Tai, Fadao, Yin, Liyun, Young, Larry J., Li, Dongming
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container_start_page 174026
container_title The Science of the total environment
container_volume 945
creator Wang, Limin
Li, Shuxin
Hao, Yaotong
Liu, Xu
Liu, Yaqing
Zuo, Lirong
Tai, Fadao
Yin, Liyun
Young, Larry J.
Li, Dongming
description The rising global prevalence of microplastics (MPs) has highlighted their diverse toxicological effects. The oxytocin (OT) system in mammals, deeply intertwined with social behaviors, is recognized to be vulnerable to environmental stressors. We hypothesized that MP exposure might disrupt this system, a topic not extensively studied. We investigated the effects of MPs on behavioral neuroendocrinology via the gut-brain axis by exposing adolescent male C57BL/6 mice to varied sizes (5 μm and 50 μm) and concentrations (100 μg/L and 1000 μg/L) of polystyrene MPs over 10 weeks. The results demonstrated that exposure to 50 μm MPs significantly reduced colonic mucin production and induced substantial alterations in gut microbiota. Notably, the 50 μm-100 μg/L group showed a significant reduction in OT content within the medial prefrontal cortex and associated deficits in sociality, along with damage to the blood-brain barrier. Importantly, blocking the vagal pathway ameliorated these behavioral impairments, emphasizing the pivotal role of the gut-brain axis in mediating neurobehavioral outcomes. Our findings confirm the toxicity of MPs on sociality and the corresponding neuroendocrine systems, shedding light on the potential hazards and adverse effects of environmental MPs exposure on social behavior and neuroendocrine frameworks in social mammals, including humans. [Display omitted] •Chronic intake of PS-MPs induced social disorder in adult mice.•Chronic intake of PS-MPs decreased the OT levels of mPFC in adult mice.•Chronic intake of PS-MPs decreased mucin layers and led to gut microbiota dysbiosis.•The impairment of social interaction and brain OT levels is via the gut-brain axis.
doi_str_mv 10.1016/j.scitotenv.2024.174026
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The oxytocin (OT) system in mammals, deeply intertwined with social behaviors, is recognized to be vulnerable to environmental stressors. We hypothesized that MP exposure might disrupt this system, a topic not extensively studied. We investigated the effects of MPs on behavioral neuroendocrinology via the gut-brain axis by exposing adolescent male C57BL/6 mice to varied sizes (5 μm and 50 μm) and concentrations (100 μg/L and 1000 μg/L) of polystyrene MPs over 10 weeks. The results demonstrated that exposure to 50 μm MPs significantly reduced colonic mucin production and induced substantial alterations in gut microbiota. Notably, the 50 μm-100 μg/L group showed a significant reduction in OT content within the medial prefrontal cortex and associated deficits in sociality, along with damage to the blood-brain barrier. Importantly, blocking the vagal pathway ameliorated these behavioral impairments, emphasizing the pivotal role of the gut-brain axis in mediating neurobehavioral outcomes. Our findings confirm the toxicity of MPs on sociality and the corresponding neuroendocrine systems, shedding light on the potential hazards and adverse effects of environmental MPs exposure on social behavior and neuroendocrine frameworks in social mammals, including humans. [Display omitted] •Chronic intake of PS-MPs induced social disorder in adult mice.•Chronic intake of PS-MPs decreased the OT levels of mPFC in adult mice.•Chronic intake of PS-MPs decreased mucin layers and led to gut microbiota dysbiosis.•The impairment of social interaction and brain OT levels is via the gut-brain axis.</description><identifier>ISSN: 0048-9697</identifier><identifier>ISSN: 1879-1026</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2024.174026</identifier><identifier>PMID: 38885706</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Gut microbiota ; Microplastics ; Neurobehavioral toxicity ; Oxytocin ; Vagus nerve</subject><ispartof>The Science of the total environment, 2024-10, Vol.945, p.174026, Article 174026</ispartof><rights>2024 Elsevier B.V.</rights><rights>Copyright © 2024 Elsevier B.V. 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The oxytocin (OT) system in mammals, deeply intertwined with social behaviors, is recognized to be vulnerable to environmental stressors. We hypothesized that MP exposure might disrupt this system, a topic not extensively studied. We investigated the effects of MPs on behavioral neuroendocrinology via the gut-brain axis by exposing adolescent male C57BL/6 mice to varied sizes (5 μm and 50 μm) and concentrations (100 μg/L and 1000 μg/L) of polystyrene MPs over 10 weeks. The results demonstrated that exposure to 50 μm MPs significantly reduced colonic mucin production and induced substantial alterations in gut microbiota. Notably, the 50 μm-100 μg/L group showed a significant reduction in OT content within the medial prefrontal cortex and associated deficits in sociality, along with damage to the blood-brain barrier. Importantly, blocking the vagal pathway ameliorated these behavioral impairments, emphasizing the pivotal role of the gut-brain axis in mediating neurobehavioral outcomes. Our findings confirm the toxicity of MPs on sociality and the corresponding neuroendocrine systems, shedding light on the potential hazards and adverse effects of environmental MPs exposure on social behavior and neuroendocrine frameworks in social mammals, including humans. 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subjects Gut microbiota
Microplastics
Neurobehavioral toxicity
Oxytocin
Vagus nerve
title Exposure to polystyrene microplastics reduces sociality and brain oxytocin levels through the gut-brain axis in mice
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