Anterior cingulate glutamate levels associate with functional activation and connectivity during sensory integration in schizophrenia: a multimodal

Humans Magnetic Resonance Imaging / methods Gyrus Cinguli Schizophrenia Glutamic Acid Proton Magnetic Resonance Spectroscopy / methods Magnetic Resonance Spectroscopy / methods Brain Mapping
functional connectivity functional magnetic resonance imaging glutamate magnetic resonance spectroscopy schizophrenia sensory integration

Journal

Psychological medicine
ISSN: 1469-8978
Titre abrégé: Psychol Med
Pays: England
ID NLM: 1254142

Informations de publication

Date de publication:
08 2023
Historique:
medline: 1 9 2023
pubmed: 7 7 2022
entrez: 6 7 2022
Statut: ppublish

Résumé

Glutamatergic dysfunction has been implicated in sensory integration deficits in schizophrenia, yet how glutamatergic function contributes to behavioural impairments and neural activities of sensory integration remains unknown. Fifty schizophrenia patients and 43 healthy controls completed behavioural assessments for sensory integration and underwent magnetic resonance spectroscopy (MRS) for measuring the anterior cingulate cortex (ACC) glutamate levels. The correlation between glutamate levels and behavioural sensory integration deficits was examined in each group. A subsample of 20 pairs of patients and controls further completed an audiovisual sensory integration functional magnetic resonance imaging (fMRI) task. Blood Oxygenation Level Dependent (BOLD) activation and task-dependent functional connectivity (FC) were assessed based on fMRI data. Full factorial analyses were performed to examine the Group-by-Glutamate Level interaction effects on fMRI measurements (group differences in correlation between glutamate levels and fMRI measurements) and the correlation between glutamate levels and fMRI measurements within each group. We found that schizophrenia patients exhibited impaired sensory integration which was positively correlated with ACC glutamate levels. Multimodal analyses showed significantly Group-by-Glutamate Level interaction effects on BOLD activation as well as task-dependent FC in a 'cortico-subcortical-cortical' network (including medial frontal gyrus, precuneus, ACC, middle cingulate gyrus, thalamus and caudate) with positive correlations in patients and negative in controls. Our findings indicate that ACC glutamate influences neural activities in a large-scale network during sensory integration, but the effects have opposite directionality between schizophrenia patients and healthy people. This implicates the crucial role of glutamatergic system in sensory integration processing in schizophrenia.

Sections du résumé

BACKGROUND
Glutamatergic dysfunction has been implicated in sensory integration deficits in schizophrenia, yet how glutamatergic function contributes to behavioural impairments and neural activities of sensory integration remains unknown.
METHODS
Fifty schizophrenia patients and 43 healthy controls completed behavioural assessments for sensory integration and underwent magnetic resonance spectroscopy (MRS) for measuring the anterior cingulate cortex (ACC) glutamate levels. The correlation between glutamate levels and behavioural sensory integration deficits was examined in each group. A subsample of 20 pairs of patients and controls further completed an audiovisual sensory integration functional magnetic resonance imaging (fMRI) task. Blood Oxygenation Level Dependent (BOLD) activation and task-dependent functional connectivity (FC) were assessed based on fMRI data. Full factorial analyses were performed to examine the Group-by-Glutamate Level interaction effects on fMRI measurements (group differences in correlation between glutamate levels and fMRI measurements) and the correlation between glutamate levels and fMRI measurements within each group.
RESULTS
We found that schizophrenia patients exhibited impaired sensory integration which was positively correlated with ACC glutamate levels. Multimodal analyses showed significantly Group-by-Glutamate Level interaction effects on BOLD activation as well as task-dependent FC in a 'cortico-subcortical-cortical' network (including medial frontal gyrus, precuneus, ACC, middle cingulate gyrus, thalamus and caudate) with positive correlations in patients and negative in controls.
CONCLUSIONS
Our findings indicate that ACC glutamate influences neural activities in a large-scale network during sensory integration, but the effects have opposite directionality between schizophrenia patients and healthy people. This implicates the crucial role of glutamatergic system in sensory integration processing in schizophrenia.

Identifiants

DOI: 10.1017/S0033291722001817 PMID: 35791929
pubmed: 35791929
doi: 10.1017/S0033291722001817
pii: S0033291722001817
doi:

Substances chimiques

Glutamic Acid 3KX376GY7L

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4904-4914

Auteurs

Xin-Lu Cai (XL)

Neuropsychology and Applied Cognitive Neuroscience Laboratory, CAS Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.
Sino-Danish College, University of Chinese Academy of Sciences, Beijing, China.
Sino-Danish Centre for Education and Research, Beijing, China.

Cheng-Cheng Pu (CC)

Peking University Sixth Hospital, Peking University Institute of Mental Health, Beijing, China.
NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Beijing, China.

Shu-Zhe Zhou (SZ)

Peking University Sixth Hospital, Peking University Institute of Mental Health, Beijing, China.
NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Beijing, China.

Yi Wang (Y)

Neuropsychology and Applied Cognitive Neuroscience Laboratory, CAS Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.
Department of Psychology, University of Chinese Academy of Sciences, Beijing, China.

Jia Huang (J)

Neuropsychology and Applied Cognitive Neuroscience Laboratory, CAS Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.
Department of Psychology, University of Chinese Academy of Sciences, Beijing, China.

Simon S Y Lui (SSY)

Department of Psychiatry, School of Clinical Medicine, The University of Hong Kong, Hong Kong Special Administrative Region, China.

Arne Møller (A)

Sino-Danish College, University of Chinese Academy of Sciences, Beijing, China.
Sino-Danish Centre for Education and Research, Beijing, China.
Centre of Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmark.
Department of Nuclear Medicine and PET Centre, Aarhus University Hospital, Aarhus, Denmark.

Eric F C Cheung (EFC)

Castle Peak Hospital, Hong Kong Special Administrative Region, China.

Kristoffer H Madsen (KH)

Sino-Danish Centre for Education and Research, Beijing, China.
Danish Research Centre for Magnetic Resonance, Centre for Functional and Diagnostic Imaging and Research, Copenhagen University Hospital, Amager and Hvidovre, Denmark.
Department of Applied Mathematics and Computer Science, Technical University of Denmark, Kongens Lyngby, Denmark.

Rong Xue (R)

Sino-Danish College, University of Chinese Academy of Sciences, Beijing, China.
Sino-Danish Centre for Education and Research, Beijing, China.
State Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China.
Beijing Institute for Brain Disorders, Beijing, China.

Xin Yu (X)

Peking University Sixth Hospital, Peking University Institute of Mental Health, Beijing, China.
NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital), Beijing, China.

Raymond C K Chan (RCK)

Neuropsychology and Applied Cognitive Neuroscience Laboratory, CAS Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.
Sino-Danish College, University of Chinese Academy of Sciences, Beijing, China.
Sino-Danish Centre for Education and Research, Beijing, China.
Department of Psychology, University of Chinese Academy of Sciences, Beijing, China.
Department of Diagnostic Radiology, the University of Hong Kong, Hong Kong Special Administrative Region, China.
ORCID: 0000-0002-3414-450X

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Anterior cingulate glutamate levels associate...
questionsmedicales.fr › Diagnostic › Techniques et procédures diagnostiques › Imagerie diagnostique › Tomographie › Imagerie par résonance magnétique › Anterior cingulate glutamate levels associate...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Prosencéphale › Télencéphale › Cerveau › Cortex cérébral › Lobe limbique › Gyrus du cingulum › Anterior cingulate glutamate levels associate...
questionsmedicales.fr › Troubles mentaux › Schizophrénie et troubles avec traits psychotiques › Schizophrénie › Anterior cingulate glutamate levels associate...
questionsmedicales.fr › Acides aminés, peptides et protéines › Acides aminés › Acides aminés excitateurs › Acide glutamique › Anterior cingulate glutamate levels associate...
questionsmedicales.fr › Techniques d'investigation › Techniques de chimie analytique › Analyse spectrale › Spectroscopie par résonance magnétique › Spectroscopie par résonance magnétique du proton › Anterior cingulate glutamate levels associate...
questionsmedicales.fr › Techniques d'investigation › Techniques de chimie analytique › Analyse spectrale › Spectroscopie par résonance magnétique › Anterior cingulate glutamate levels associate...
questionsmedicales.fr › Techniques d'investigation › Neuroimagerie › Neuroimagerie fonctionnelle › Cartographie cérébrale › Anterior cingulate glutamate levels associate...