Increased glutamate and glutamine levels and their relationship to astrocytes and dopaminergic transmissions in the brains of adults with autism

Increased excitatory neuronal tones have been implicated in autism, but its mechanism remains elusive. The amplified glutamate signals may arise from enhanced glutamatergic circuits, which can be affected by astrocyte activation and suppressive signaling of dopamine neurotransmission. We tested this...

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Published inScientific reports Vol. 13; no. 1; pp. 11655 - 10
Main Authors Oya, Masaki, Matsuoka, Kiwamu, Kubota, Manabu, Fujino, Junya, Tei, Shisei, Takahata, Keisuke, Tagai, Kenji, Yamamoto, Yasuharu, Shimada, Hitoshi, Seki, Chie, Itahashi, Takashi, Aoki, Yuta Y., Ohta, Haruhisa, Hashimoto, Ryu-ichiro, Sugihara, Genichi, Obata, Takayuki, Zhang, Ming-Rong, Suhara, Tetsuya, Nakamura, Motoaki, Kato, Nobumasa, Takado, Yuhei, Takahashi, Hidehiko, Higuchi, Makoto
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 19.07.2023
Nature Publishing Group
Nature Portfolio
Subjects
692/699/476/1373
692/700/1421/1628
692/700/1421/1846/2092
Adult
Astrocytes
Astrocytes - metabolism
Autism
Autistic Disorder - metabolism
Brain - diagnostic imaging
Brain - metabolism
Cortex (cingulate)
Dopamine
Dopamine - metabolism
Dopamine D1 receptors
Glutamatergic transmission
Glutamic Acid - metabolism
Glutamine
Glutamine - metabolism
Gyrus Cinguli - diagnostic imaging
Gyrus Cinguli - metabolism
Humanities and Social Sciences
Humans
Inositol
Magnetic resonance spectroscopy
Male
multidisciplinary
Neurotransmission
Positron emission tomography
Science
Science (multidisciplinary)
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Abstract Increased excitatory neuronal tones have been implicated in autism, but its mechanism remains elusive. The amplified glutamate signals may arise from enhanced glutamatergic circuits, which can be affected by astrocyte activation and suppressive signaling of dopamine neurotransmission. We tested this hypothesis using magnetic resonance spectroscopy and positron emission tomography scan with 11 C-SCH23390 for dopamine D1 receptors in the anterior cingulate cortex (ACC). We enrolled 18 male adults with high-functioning autism and 20 typically developed (TD) male subjects. The autism group showed elevated glutamate, glutamine, and myo-inositol (mI) levels compared with the TD group ( p  = 0.045, p  = 0.044, p  = 0.030, respectively) and a positive correlation between glutamine and mI levels in the ACC (r = 0.54, p  = 0.020). In autism and TD groups, ACC D1 receptor radioligand binding was negatively correlated with ACC glutamine levels (r =  − 0.55, p  = 0.022; r =  − 0.58, p  = 0.008, respectively). The enhanced glutamate-glutamine metabolism might be due to astroglial activation and the consequent reinforcement of glutamine synthesis in autistic brains. Glutamine synthesis could underly the physiological inhibitory control of dopaminergic D1 receptor signals. Our findings suggest a high neuron excitation-inhibition ratio with astrocytic activation in the etiology of autism.
AbstractList Increased excitatory neuronal tones have been implicated in autism, but its mechanism remains elusive. The amplified glutamate signals may arise from enhanced glutamatergic circuits, which can be affected by astrocyte activation and suppressive signaling of dopamine neurotransmission. We tested this hypothesis using magnetic resonance spectroscopy and positron emission tomography scan with 11 C-SCH23390 for dopamine D1 receptors in the anterior cingulate cortex (ACC). We enrolled 18 male adults with high-functioning autism and 20 typically developed (TD) male subjects. The autism group showed elevated glutamate, glutamine, and myo-inositol (mI) levels compared with the TD group ( p  = 0.045, p  = 0.044, p  = 0.030, respectively) and a positive correlation between glutamine and mI levels in the ACC (r = 0.54, p  = 0.020). In autism and TD groups, ACC D1 receptor radioligand binding was negatively correlated with ACC glutamine levels (r =  − 0.55, p  = 0.022; r =  − 0.58, p  = 0.008, respectively). The enhanced glutamate-glutamine metabolism might be due to astroglial activation and the consequent reinforcement of glutamine synthesis in autistic brains. Glutamine synthesis could underly the physiological inhibitory control of dopaminergic D1 receptor signals. Our findings suggest a high neuron excitation-inhibition ratio with astrocytic activation in the etiology of autism.
Increased excitatory neuronal tones have been implicated in autism, but its mechanism remains elusive. The amplified glutamate signals may arise from enhanced glutamatergic circuits, which can be affected by astrocyte activation and suppressive signaling of dopamine neurotransmission. We tested this hypothesis using magnetic resonance spectroscopy and positron emission tomography scan with C-SCH23390 for dopamine D1 receptors in the anterior cingulate cortex (ACC). We enrolled 18 male adults with high-functioning autism and 20 typically developed (TD) male subjects. The autism group showed elevated glutamate, glutamine, and myo-inositol (mI) levels compared with the TD group (p = 0.045, p = 0.044, p = 0.030, respectively) and a positive correlation between glutamine and mI levels in the ACC (r = 0.54, p = 0.020). In autism and TD groups, ACC D1 receptor radioligand binding was negatively correlated with ACC glutamine levels (r =  - 0.55, p = 0.022; r =  - 0.58, p = 0.008, respectively). The enhanced glutamate-glutamine metabolism might be due to astroglial activation and the consequent reinforcement of glutamine synthesis in autistic brains. Glutamine synthesis could underly the physiological inhibitory control of dopaminergic D1 receptor signals. Our findings suggest a high neuron excitation-inhibition ratio with astrocytic activation in the etiology of autism.
Increased excitatory neuronal tones have been implicated in autism, but its mechanism remains elusive. The amplified glutamate signals may arise from enhanced glutamatergic circuits, which can be affected by astrocyte activation and suppressive signaling of dopamine neurotransmission. We tested this hypothesis using magnetic resonance spectroscopy and positron emission tomography scan with 11C-SCH23390 for dopamine D1 receptors in the anterior cingulate cortex (ACC). We enrolled 18 male adults with high-functioning autism and 20 typically developed (TD) male subjects. The autism group showed elevated glutamate, glutamine, and myo-inositol (mI) levels compared with the TD group (p = 0.045, p = 0.044, p = 0.030, respectively) and a positive correlation between glutamine and mI levels in the ACC (r = 0.54, p = 0.020). In autism and TD groups, ACC D1 receptor radioligand binding was negatively correlated with ACC glutamine levels (r =  − 0.55, p = 0.022; r =  − 0.58, p = 0.008, respectively). The enhanced glutamate-glutamine metabolism might be due to astroglial activation and the consequent reinforcement of glutamine synthesis in autistic brains. Glutamine synthesis could underly the physiological inhibitory control of dopaminergic D1 receptor signals. Our findings suggest a high neuron excitation-inhibition ratio with astrocytic activation in the etiology of autism.
Increased excitatory neuronal tones have been implicated in autism, but its mechanism remains elusive. The amplified glutamate signals may arise from enhanced glutamatergic circuits, which can be affected by astrocyte activation and suppressive signaling of dopamine neurotransmission. We tested this hypothesis using magnetic resonance spectroscopy and positron emission tomography scan with 11C-SCH23390 for dopamine D1 receptors in the anterior cingulate cortex (ACC). We enrolled 18 male adults with high-functioning autism and 20 typically developed (TD) male subjects. The autism group showed elevated glutamate, glutamine, and myo-inositol (mI) levels compared with the TD group (p = 0.045, p = 0.044, p = 0.030, respectively) and a positive correlation between glutamine and mI levels in the ACC (r = 0.54, p = 0.020). In autism and TD groups, ACC D1 receptor radioligand binding was negatively correlated with ACC glutamine levels (r =  - 0.55, p = 0.022; r =  - 0.58, p = 0.008, respectively). The enhanced glutamate-glutamine metabolism might be due to astroglial activation and the consequent reinforcement of glutamine synthesis in autistic brains. Glutamine synthesis could underly the physiological inhibitory control of dopaminergic D1 receptor signals. Our findings suggest a high neuron excitation-inhibition ratio with astrocytic activation in the etiology of autism.Increased excitatory neuronal tones have been implicated in autism, but its mechanism remains elusive. The amplified glutamate signals may arise from enhanced glutamatergic circuits, which can be affected by astrocyte activation and suppressive signaling of dopamine neurotransmission. We tested this hypothesis using magnetic resonance spectroscopy and positron emission tomography scan with 11C-SCH23390 for dopamine D1 receptors in the anterior cingulate cortex (ACC). We enrolled 18 male adults with high-functioning autism and 20 typically developed (TD) male subjects. The autism group showed elevated glutamate, glutamine, and myo-inositol (mI) levels compared with the TD group (p = 0.045, p = 0.044, p = 0.030, respectively) and a positive correlation between glutamine and mI levels in the ACC (r = 0.54, p = 0.020). In autism and TD groups, ACC D1 receptor radioligand binding was negatively correlated with ACC glutamine levels (r =  - 0.55, p = 0.022; r =  - 0.58, p = 0.008, respectively). The enhanced glutamate-glutamine metabolism might be due to astroglial activation and the consequent reinforcement of glutamine synthesis in autistic brains. Glutamine synthesis could underly the physiological inhibitory control of dopaminergic D1 receptor signals. Our findings suggest a high neuron excitation-inhibition ratio with astrocytic activation in the etiology of autism.
Abstract Increased excitatory neuronal tones have been implicated in autism, but its mechanism remains elusive. The amplified glutamate signals may arise from enhanced glutamatergic circuits, which can be affected by astrocyte activation and suppressive signaling of dopamine neurotransmission. We tested this hypothesis using magnetic resonance spectroscopy and positron emission tomography scan with 11C-SCH23390 for dopamine D1 receptors in the anterior cingulate cortex (ACC). We enrolled 18 male adults with high-functioning autism and 20 typically developed (TD) male subjects. The autism group showed elevated glutamate, glutamine, and myo-inositol (mI) levels compared with the TD group (p = 0.045, p = 0.044, p = 0.030, respectively) and a positive correlation between glutamine and mI levels in the ACC (r = 0.54, p = 0.020). In autism and TD groups, ACC D1 receptor radioligand binding was negatively correlated with ACC glutamine levels (r =  − 0.55, p = 0.022; r =  − 0.58, p = 0.008, respectively). The enhanced glutamate-glutamine metabolism might be due to astroglial activation and the consequent reinforcement of glutamine synthesis in autistic brains. Glutamine synthesis could underly the physiological inhibitory control of dopaminergic D1 receptor signals. Our findings suggest a high neuron excitation-inhibition ratio with astrocytic activation in the etiology of autism.
ArticleNumber 11655
Author Sugihara, Genichi
Aoki, Yuta Y.
Matsuoka, Kiwamu
Shimada, Hitoshi
Higuchi, Makoto
Hashimoto, Ryu-ichiro
Takado, Yuhei
Oya, Masaki
Tei, Shisei
Suhara, Tetsuya
Kubota, Manabu
Itahashi, Takashi
Zhang, Ming-Rong
Seki, Chie
Obata, Takayuki
Tagai, Kenji
Yamamoto, Yasuharu
Kato, Nobumasa
Nakamura, Motoaki
Takahashi, Hidehiko
Takahata, Keisuke
Fujino, Junya
Ohta, Haruhisa
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  givenname: Kiwamu
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– sequence: 3
  givenname: Manabu
  surname: Kubota
  fullname: Kubota, Manabu
  organization: Department of Functional Brain Imaging, Institute for Quantum Medical Science, National Institutes for Quantum Science and Technology (QST), Department of Psychiatry, Graduate School of Medicine, Kyoto University, Medical Institute of Developmental Disabilities Research, Showa University
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  surname: Tei
  fullname: Tei, Shisei
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/37468523$$D View this record in MEDLINE/PubMed
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Snippet Increased excitatory neuronal tones have been implicated in autism, but its mechanism remains elusive. The amplified glutamate signals may arise from enhanced...
Abstract Increased excitatory neuronal tones have been implicated in autism, but its mechanism remains elusive. The amplified glutamate signals may arise from...
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SubjectTerms 692/699/476/1373
692/700/1421/1628
692/700/1421/1846/2092
Adult
Astrocytes
Astrocytes - metabolism
Autism
Autistic Disorder - metabolism
Brain - diagnostic imaging
Brain - metabolism
Cortex (cingulate)
Dopamine
Dopamine - metabolism
Dopamine D1 receptors
Glutamatergic transmission
Glutamic Acid - metabolism
Glutamine
Glutamine - metabolism
Gyrus Cinguli - diagnostic imaging
Gyrus Cinguli - metabolism
Humanities and Social Sciences
Humans
Inositol
Magnetic resonance spectroscopy
Male
multidisciplinary
Neurotransmission
Positron emission tomography
Science
Science (multidisciplinary)
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Title Increased glutamate and glutamine levels and their relationship to astrocytes and dopaminergic transmissions in the brains of adults with autism
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Volume 13
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