In vivo assessment of GABAergic inhibition and glutamate facilitation in treatment-resistant schizophrenia: a TMS study integrating clinical, cognitive, and neurophysiological evaluations

Abstract Treatment-resistant schizophrenia (TRS) affects approximately one-third of individuals with schizophrenia, posing significant challenges for clinical management. Clozapine treatment is often delayed, underscoring the urgent need for an early potential signature of TRS. To date, specific alt...

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Main Authors: Annarita Barone, Gianmaria Senerchia, Giuseppe De Simone, Marco Manzo, Mariateresa Ciccarelli, Stefano Tozza, Valentina Virginia Iuzzolino, Myriam Spisto, Raffaele Dubbioso, Felice Iasevoli, Rosa Iodice, Andrea de Bartolomeis
Format: Article
Language:English
Published: Nature Portfolio 2025-06-01
Series:Schizophrenia
Online Access:https://doi.org/10.1038/s41537-025-00634-w
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author Annarita Barone
Gianmaria Senerchia
Giuseppe De Simone
Marco Manzo
Mariateresa Ciccarelli
Stefano Tozza
Valentina Virginia Iuzzolino
Myriam Spisto
Raffaele Dubbioso
Felice Iasevoli
Rosa Iodice
Andrea de Bartolomeis
author_facet Annarita Barone
Gianmaria Senerchia
Giuseppe De Simone
Marco Manzo
Mariateresa Ciccarelli
Stefano Tozza
Valentina Virginia Iuzzolino
Myriam Spisto
Raffaele Dubbioso
Felice Iasevoli
Rosa Iodice
Andrea de Bartolomeis
author_sort Annarita Barone
collection DOAJ
description Abstract Treatment-resistant schizophrenia (TRS) affects approximately one-third of individuals with schizophrenia, posing significant challenges for clinical management. Clozapine treatment is often delayed, underscoring the urgent need for an early potential signature of TRS. To date, specific alterations in cortical excitability and plasticity underlying TRS remain unexplored. We evaluated cortical excitability and plasticity in 30 patients with schizophrenia (15 TRS, 15 non-TRS) and 21 controls using transcranial magnetic stimulation (TMS). Measures included motor thresholds and protocols probing GABAergic inhibition and glutamatergic facilitatory activity, the excitation index (EI) in the primary motor cortex (M1), and long-term potentiation (LTP)-like plasticity using intermittent theta burst stimulation (iTBS). Clinical severity and cognitive performance were evaluated using the Positive and Negative Syndrome Scale (PANSS) and the Brief Assessment of Cognition in Schizophrenia (BACS). TRS patients exhibited significantly higher active motor thresholds (p = 0.015) and impaired short-interval intracortical inhibition (SICI) (p = 0.001) vs healthy controls, reflecting GABAergic dysfunction. EI was elevated in TRS vs non-TRS patients (p = 0.034) and controls (p = 0.002), indicating pronounced cortical hyperexcitability. Both TRS (p = 0.008) and non-TRS patients (p = 0.033) showed reduced plasticity following iTBS compared to controls, with no TRS vs non-TRS difference. SICI deficits significantly correlated with negative (r = 0.524, p adj = 0.03) and autistic (r = 0.517, p adj = 0.03) symptom severity as assessed by the PANSS negative score and Positive and Negative Syndrome Scale Autism Severity Score (PAUSS). Our findings point to a neurophysiological continuum in schizophrenia, with TRS patients demonstrating the most pronounced cortical hyperexcitability and impaired plasticity, and non-TRS patients showing intermediate deficits.
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spelling doaj-art-07ff23483c4740d7b7d3fb37d1d3030c2025-08-20T03:47:14ZengNature PortfolioSchizophrenia2754-69932025-06-0111111010.1038/s41537-025-00634-wIn vivo assessment of GABAergic inhibition and glutamate facilitation in treatment-resistant schizophrenia: a TMS study integrating clinical, cognitive, and neurophysiological evaluationsAnnarita Barone0Gianmaria Senerchia1Giuseppe De Simone2Marco Manzo3Mariateresa Ciccarelli4Stefano Tozza5Valentina Virginia Iuzzolino6Myriam Spisto7Raffaele Dubbioso8Felice Iasevoli9Rosa Iodice10Andrea de Bartolomeis11Section of Psychiatry, Laboratory of Molecular and Translational Psychiatry, Unit of Treatment-Resistant Psychiatric Disorders, Department of Neuroscience, Reproductive Sciences and Dentistry, University of Naples “Federico II”Neurology Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, University of Naples “Federico II”Section of Psychiatry, Laboratory of Molecular and Translational Psychiatry, Unit of Treatment-Resistant Psychiatric Disorders, Department of Neuroscience, Reproductive Sciences and Dentistry, University of Naples “Federico II”Section of Psychiatry, Laboratory of Molecular and Translational Psychiatry, Unit of Treatment-Resistant Psychiatric Disorders, Department of Neuroscience, Reproductive Sciences and Dentistry, University of Naples “Federico II”Section of Psychiatry, Laboratory of Molecular and Translational Psychiatry, Unit of Treatment-Resistant Psychiatric Disorders, Department of Neuroscience, Reproductive Sciences and Dentistry, University of Naples “Federico II”Neurology Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, University of Naples “Federico II”Neurology Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, University of Naples “Federico II”Neurology Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, University of Naples “Federico II”Neurology Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, University of Naples “Federico II”Section of Psychiatry, Laboratory of Molecular and Translational Psychiatry, Unit of Treatment-Resistant Psychiatric Disorders, Department of Neuroscience, Reproductive Sciences and Dentistry, University of Naples “Federico II”Neurology Unit, Department of Neuroscience, Reproductive Sciences and Dentistry, University of Naples “Federico II”Section of Psychiatry, Laboratory of Molecular and Translational Psychiatry, Unit of Treatment-Resistant Psychiatric Disorders, Department of Neuroscience, Reproductive Sciences and Dentistry, University of Naples “Federico II”Abstract Treatment-resistant schizophrenia (TRS) affects approximately one-third of individuals with schizophrenia, posing significant challenges for clinical management. Clozapine treatment is often delayed, underscoring the urgent need for an early potential signature of TRS. To date, specific alterations in cortical excitability and plasticity underlying TRS remain unexplored. We evaluated cortical excitability and plasticity in 30 patients with schizophrenia (15 TRS, 15 non-TRS) and 21 controls using transcranial magnetic stimulation (TMS). Measures included motor thresholds and protocols probing GABAergic inhibition and glutamatergic facilitatory activity, the excitation index (EI) in the primary motor cortex (M1), and long-term potentiation (LTP)-like plasticity using intermittent theta burst stimulation (iTBS). Clinical severity and cognitive performance were evaluated using the Positive and Negative Syndrome Scale (PANSS) and the Brief Assessment of Cognition in Schizophrenia (BACS). TRS patients exhibited significantly higher active motor thresholds (p = 0.015) and impaired short-interval intracortical inhibition (SICI) (p = 0.001) vs healthy controls, reflecting GABAergic dysfunction. EI was elevated in TRS vs non-TRS patients (p = 0.034) and controls (p = 0.002), indicating pronounced cortical hyperexcitability. Both TRS (p = 0.008) and non-TRS patients (p = 0.033) showed reduced plasticity following iTBS compared to controls, with no TRS vs non-TRS difference. SICI deficits significantly correlated with negative (r = 0.524, p adj = 0.03) and autistic (r = 0.517, p adj = 0.03) symptom severity as assessed by the PANSS negative score and Positive and Negative Syndrome Scale Autism Severity Score (PAUSS). Our findings point to a neurophysiological continuum in schizophrenia, with TRS patients demonstrating the most pronounced cortical hyperexcitability and impaired plasticity, and non-TRS patients showing intermediate deficits.https://doi.org/10.1038/s41537-025-00634-w
spellingShingle Annarita Barone
Gianmaria Senerchia
Giuseppe De Simone
Marco Manzo
Mariateresa Ciccarelli
Stefano Tozza
Valentina Virginia Iuzzolino
Myriam Spisto
Raffaele Dubbioso
Felice Iasevoli
Rosa Iodice
Andrea de Bartolomeis
In vivo assessment of GABAergic inhibition and glutamate facilitation in treatment-resistant schizophrenia: a TMS study integrating clinical, cognitive, and neurophysiological evaluations
Schizophrenia
title In vivo assessment of GABAergic inhibition and glutamate facilitation in treatment-resistant schizophrenia: a TMS study integrating clinical, cognitive, and neurophysiological evaluations
title_full In vivo assessment of GABAergic inhibition and glutamate facilitation in treatment-resistant schizophrenia: a TMS study integrating clinical, cognitive, and neurophysiological evaluations
title_fullStr In vivo assessment of GABAergic inhibition and glutamate facilitation in treatment-resistant schizophrenia: a TMS study integrating clinical, cognitive, and neurophysiological evaluations
title_full_unstemmed In vivo assessment of GABAergic inhibition and glutamate facilitation in treatment-resistant schizophrenia: a TMS study integrating clinical, cognitive, and neurophysiological evaluations
title_short In vivo assessment of GABAergic inhibition and glutamate facilitation in treatment-resistant schizophrenia: a TMS study integrating clinical, cognitive, and neurophysiological evaluations
title_sort in vivo assessment of gabaergic inhibition and glutamate facilitation in treatment resistant schizophrenia a tms study integrating clinical cognitive and neurophysiological evaluations
url https://doi.org/10.1038/s41537-025-00634-w
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