Investigating brain–gut microbiota dynamics and inflammatory processes in an autistic-like rat model using MRI biomarkers during childhood and adolescence
•Reduced microbiota diversity emphasized the early interventions targeting gut dysbiosis in ASD.•Dysregulation in SCFA metabolism potentially impacts ASD-related behaviors.•Elevated astrocytic, microglial activation, and proinflammatory cytokines in ASD.•The potential of DTI metrics as imaging-based...
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| Published in | NeuroImage (Orlando, Fla.) Vol. 302; p. 120899 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
15.11.2024
Elsevier Limited Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1053-8119 1095-9572 1095-9572 |
| DOI | 10.1016/j.neuroimage.2024.120899 |
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| Abstract | •Reduced microbiota diversity emphasized the early interventions targeting gut dysbiosis in ASD.•Dysregulation in SCFA metabolism potentially impacts ASD-related behaviors.•Elevated astrocytic, microglial activation, and proinflammatory cytokines in ASD.•The potential of DTI metrics as imaging-based biomarkers for ASD.
Autism spectrum disorder (ASD) is characterized by social interaction deficits and repetitive behaviors. Recent research has linked that gut dysbiosis may contribute to ASD-like behaviors. However, the exact developmental time point at which gut microbiota alterations affect brain function and behavior in patients with ASD remains unclear. We hypothesized that ASD-related brain microstructural changes and gut dysbiosis induce metabolic dysregulation and proinflammatory responses, which collectively contribute to the social behavioral deficits observed in early childhood. We used an autistic-like rat model that was generated via prenatal valproic acid exposure. We analyzed brain microstructural changes using diffusion tensor imaging (DTI) and examined microbiota, blood, and fecal samples for inflammation biomarkers. The ASD model rats exhibited significant brain microstructural changes in the anterior cingulate cortex, hippocampus, striatum, and thalamus; reduced microbiota diversity (Prevotellaceae and Peptostreptococcaceae); and altered metabolic signatures. The shift in microbiota diversity and density observed at postnatal day (PND) 35, which is a critical developmental period, underscored the importance of early ASD interventions. We identified a unique metabolic signature in the ASD model, with elevated formate and reduced acetate and butyrate levels, indicating a dysregulation in short-chain fatty acid (SCFA) metabolism. Furthermore, increased astrocytic and microglial activation and elevated proinflammatory cytokines—interleukin-1 beta (IL-1β), interleukin-6 (IL-6), interferon-gamma (IFN-γ), and tumor necrosis factor-alpha (TNF-α)—were observed, indicating immune dysregulation. This study provided insights into the complex interplay between the brain and the gut, and indicated DTI metrics as potential imaging-based biomarkers in ASD, thus emphasizing the need for early childhood interventions. |
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| AbstractList | •Reduced microbiota diversity emphasized the early interventions targeting gut dysbiosis in ASD.•Dysregulation in SCFA metabolism potentially impacts ASD-related behaviors.•Elevated astrocytic, microglial activation, and proinflammatory cytokines in ASD.•The potential of DTI metrics as imaging-based biomarkers for ASD.
Autism spectrum disorder (ASD) is characterized by social interaction deficits and repetitive behaviors. Recent research has linked that gut dysbiosis may contribute to ASD-like behaviors. However, the exact developmental time point at which gut microbiota alterations affect brain function and behavior in patients with ASD remains unclear. We hypothesized that ASD-related brain microstructural changes and gut dysbiosis induce metabolic dysregulation and proinflammatory responses, which collectively contribute to the social behavioral deficits observed in early childhood. We used an autistic-like rat model that was generated via prenatal valproic acid exposure. We analyzed brain microstructural changes using diffusion tensor imaging (DTI) and examined microbiota, blood, and fecal samples for inflammation biomarkers. The ASD model rats exhibited significant brain microstructural changes in the anterior cingulate cortex, hippocampus, striatum, and thalamus; reduced microbiota diversity (Prevotellaceae and Peptostreptococcaceae); and altered metabolic signatures. The shift in microbiota diversity and density observed at postnatal day (PND) 35, which is a critical developmental period, underscored the importance of early ASD interventions. We identified a unique metabolic signature in the ASD model, with elevated formate and reduced acetate and butyrate levels, indicating a dysregulation in short-chain fatty acid (SCFA) metabolism. Furthermore, increased astrocytic and microglial activation and elevated proinflammatory cytokines—interleukin-1 beta (IL-1β), interleukin-6 (IL-6), interferon-gamma (IFN-γ), and tumor necrosis factor-alpha (TNF-α)—were observed, indicating immune dysregulation. This study provided insights into the complex interplay between the brain and the gut, and indicated DTI metrics as potential imaging-based biomarkers in ASD, thus emphasizing the need for early childhood interventions. Autism spectrum disorder (ASD) is characterized by social interaction deficits and repetitive behaviors. Recent research has linked that gut dysbiosis may contribute to ASD-like behaviors. However, the exact developmental time point at which gut microbiota alterations affect brain function and behavior in patients with ASD remains unclear. We hypothesized that ASD-related brain microstructural changes and gut dysbiosis induce metabolic dysregulation and proinflammatory responses, which collectively contribute to the social behavioral deficits observed in early childhood. We used an autistic-like rat model that was generated via prenatal valproic acid exposure. We analyzed brain microstructural changes using diffusion tensor imaging (DTI) and examined microbiota, blood, and fecal samples for inflammation biomarkers. The ASD model rats exhibited significant brain microstructural changes in the anterior cingulate cortex, hippocampus, striatum, and thalamus; reduced microbiota diversity (Prevotellaceae and Peptostreptococcaceae); and altered metabolic signatures. The shift in microbiota diversity and density observed at postnatal day (PND) 35, which is a critical developmental period, underscored the importance of early ASD interventions. We identified a unique metabolic signature in the ASD model, with elevated formate and reduced acetate and butyrate levels, indicating a dysregulation in short-chain fatty acid (SCFA) metabolism. Furthermore, increased astrocytic and microglial activation and elevated proinflammatory cytokines-interleukin-1 beta (IL-1β), interleukin-6 (IL-6), interferon-gamma (IFN-γ), and tumor necrosis factor-alpha (TNF-α)-were observed, indicating immune dysregulation. This study provided insights into the complex interplay between the brain and the gut, and indicated DTI metrics as potential imaging-based biomarkers in ASD, thus emphasizing the need for early childhood interventions.Autism spectrum disorder (ASD) is characterized by social interaction deficits and repetitive behaviors. Recent research has linked that gut dysbiosis may contribute to ASD-like behaviors. However, the exact developmental time point at which gut microbiota alterations affect brain function and behavior in patients with ASD remains unclear. We hypothesized that ASD-related brain microstructural changes and gut dysbiosis induce metabolic dysregulation and proinflammatory responses, which collectively contribute to the social behavioral deficits observed in early childhood. We used an autistic-like rat model that was generated via prenatal valproic acid exposure. We analyzed brain microstructural changes using diffusion tensor imaging (DTI) and examined microbiota, blood, and fecal samples for inflammation biomarkers. The ASD model rats exhibited significant brain microstructural changes in the anterior cingulate cortex, hippocampus, striatum, and thalamus; reduced microbiota diversity (Prevotellaceae and Peptostreptococcaceae); and altered metabolic signatures. The shift in microbiota diversity and density observed at postnatal day (PND) 35, which is a critical developmental period, underscored the importance of early ASD interventions. We identified a unique metabolic signature in the ASD model, with elevated formate and reduced acetate and butyrate levels, indicating a dysregulation in short-chain fatty acid (SCFA) metabolism. Furthermore, increased astrocytic and microglial activation and elevated proinflammatory cytokines-interleukin-1 beta (IL-1β), interleukin-6 (IL-6), interferon-gamma (IFN-γ), and tumor necrosis factor-alpha (TNF-α)-were observed, indicating immune dysregulation. This study provided insights into the complex interplay between the brain and the gut, and indicated DTI metrics as potential imaging-based biomarkers in ASD, thus emphasizing the need for early childhood interventions. Autism spectrum disorder (ASD) is characterized by social interaction deficits and repetitive behaviors. Recent research has linked that gut dysbiosis may contribute to ASD-like behaviors. However, the exact developmental time point at which gut microbiota alterations affect brain function and behavior in patients with ASD remains unclear. We hypothesized that ASD-related brain microstructural changes and gut dysbiosis induce metabolic dysregulation and proinflammatory responses, which collectively contribute to the social behavioral deficits observed in early childhood. We used an autistic-like rat model that was generated via prenatal valproic acid exposure. We analyzed brain microstructural changes using diffusion tensor imaging (DTI) and examined microbiota, blood, and fecal samples for inflammation biomarkers. The ASD model rats exhibited significant brain microstructural changes in the anterior cingulate cortex, hippocampus, striatum, and thalamus; reduced microbiota diversity (Prevotellaceae and Peptostreptococcaceae); and altered metabolic signatures. The shift in microbiota diversity and density observed at postnatal day (PND) 35, which is a critical developmental period, underscored the importance of early ASD interventions. We identified a unique metabolic signature in the ASD model, with elevated formate and reduced acetate and butyrate levels, indicating a dysregulation in short-chain fatty acid (SCFA) metabolism. Furthermore, increased astrocytic and microglial activation and elevated proinflammatory cytokines-interleukin-1 beta (IL-1β), interleukin-6 (IL-6), interferon-gamma (IFN-γ), and tumor necrosis factor-alpha (TNF-α)-were observed, indicating immune dysregulation. This study provided insights into the complex interplay between the brain and the gut, and indicated DTI metrics as potential imaging-based biomarkers in ASD, thus emphasizing the need for early childhood interventions. |
| ArticleNumber | 120899 |
| Author | Tseng, Hsin-Yi Li, Ssu-Ju Chang, Ching-Wen Palanivelu, Lalitha Liang, Yao-Wen Lo, Yu-Chun Chang, Chih-Ju Chen, You-Yin |
| Author_xml | – sequence: 1 givenname: Lalitha orcidid: 0000-0002-1998-6127 surname: Palanivelu fullname: Palanivelu, Lalitha organization: International Ph.D. Program in Medicine, College of Medicine, Taipei Medical University, 7F., No. 250, Wuxing St., Xinyi Dist., Taipei city 110, Taiwan – sequence: 2 givenname: You-Yin orcidid: 0000-0003-4869-3857 surname: Chen fullname: Chen, You-Yin organization: Department of Biomedical Engineering, National Yang Ming Chiao Tung University, No.155, Sec.2, Linong St., Taipei 11221, Taiwan – sequence: 3 givenname: Chih-Ju surname: Chang fullname: Chang, Chih-Ju organization: Department of Neurosurgery, Cathay General Hospital, No. 280, Sec. 4, Renai Rd., Taipei 10629, Taiwan – sequence: 4 givenname: Yao-Wen surname: Liang fullname: Liang, Yao-Wen organization: Department of Biomedical Engineering, National Yang Ming Chiao Tung University, No.155, Sec.2, Linong St., Taipei 11221, Taiwan – sequence: 5 givenname: Hsin-Yi surname: Tseng fullname: Tseng, Hsin-Yi organization: Ph.D. Program in Medical Neuroscience, College of Medical Science and Technology, Taipei Medical University and National Health Research Institutes, 12F., Education and Research Building, Shuang-Ho Campus, No. 301, Yuantong Rd., New Taipei City 23564, Taiwan – sequence: 6 givenname: Ssu-Ju surname: Li fullname: Li, Ssu-Ju organization: Department of Biomedical Engineering, National Yang Ming Chiao Tung University, No.155, Sec.2, Linong St., Taipei 11221, Taiwan – sequence: 7 givenname: Ching-Wen surname: Chang fullname: Chang, Ching-Wen organization: Department of Biomedical Engineering, National Yang Ming Chiao Tung University, No.155, Sec.2, Linong St., Taipei 11221, Taiwan – sequence: 8 givenname: Yu-Chun surname: Lo fullname: Lo, Yu-Chun email: aricalo@tmu.edu.tw organization: Ph.D. Program in Medical Neuroscience, College of Medical Science and Technology, Taipei Medical University. 12F., Education and Research Building, Shuang-Ho Campus, No. 301, Yuantong Rd., New Taipei City 23564, Taiwan |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/39461606$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Acetic acid Adolescence Animals Anisotropy Autism Autism spectrum disorder Autism Spectrum Disorder - diagnostic imaging Autism Spectrum Disorder - immunology Autism Spectrum Disorder - metabolism Autism Spectrum Disorder - microbiology Behavior Biomarkers Biomarkers - metabolism Brain - diagnostic imaging Brain - metabolism Brain research Brain-Gut Axis - physiology Childhood Children Chromatography Cortex (cingulate) Cytokines Developmental stages Diffusion tensor imaging Diffusion Tensor Imaging - methods Disease Models, Animal Dysbacteriosis Fatty acids Feces Female Gastrointestinal Microbiome Gut microbiota Immune system Inflammation Inflammation - diagnostic imaging Inflammation - metabolism Interleukin 1 Interleukin 6 Intestinal microflora Magnetic resonance imaging Magnetic Resonance Imaging - methods Male Mass spectrometry Metabolites Microbiome dysbiosis Microbiota Neostriatum Neurodevelopmental disorders Neuroimaging Neuroinflammation Pregnancy Prenatal experience Prenatal exposure Rats Rats, Sprague-Dawley Scientific imaging Social behavior Tumor necrosis factor-α Valproic acid Valproic Acid - pharmacology γ-Interferon |
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