Investigating cortical excitability and inhibition in patients with schizophrenia: A TMS-EEG study

V. Santoro; M. D. Hou; I. Premoli; P. Belardinelli; A. Biondi; A. Carobin; F. Puledda; P. G. Michalopoulou; M. P. Richardson; L. Rocchi; S. S. Shergill

doi:10.1016/j.brainresbull.2024.110972

Investigating cortical excitability and inhibition in patients with schizophrenia: A TMS-EEG study

V. Santoro^*, M. D. Hou, I. Premoli, P. Belardinelli, A. Biondi, A. Carobin, F. Puledda, P. G. Michalopoulou, M. P. Richardson, L. Rocchi, S. S. Shergill

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

5 Citations (Scopus)

Abstract

Background: Transcranial magnetic stimulation (TMS) combined with electromyography (EMG) has widely been used as a non-invasive brain stimulation tool to assess excitation/inhibition (E/I) balance. E/I imbalance is a putative mechanism underlying symptoms in patients with schizophrenia. Combined TMS-electroencephalography (TMS-EEG) provides a detailed examination of cortical excitability to assess the pathophysiology of schizophrenia. This study aimed to investigate differences in TMS-evoked potentials (TEPs), TMS-related spectral perturbations (TRSP) and intertrial coherence (ITC) between patients with schizophrenia and healthy controls. Materials and methods: TMS was applied over the motor cortex during EEG recording. Differences in TEPs, TRSP and ITC between the patient and healthy subjects were analysed for all electrodes at each time point, by applying multiple independent sample t-tests with a cluster-based permutation analysis to correct for multiple comparisons. Results: Patients demonstrated significantly reduced amplitudes of early and late TEP components compared to healthy controls. Patients also showed a significant reduction of early delta (50–160 ms) and theta TRSP (30-250ms),followed by a reduction in alpha and beta suppression (220–560 ms; 190–420 ms). Patients showed a reduction of both early (50–110 ms) gamma increase and later (180–230 ms) gamma suppression. Finally, the ITC was significantly lower in patients in the alpha band, from 30 to 260 ms. Conclusion: Our findings support the putative role of impaired GABA-receptor mediated inhibition in schizophrenia impacting excitatory neurotransmission. Further studies can usefully elucidate mechanisms underlying specific symptoms clusters using TMS-EEG biometrics.

Original language	English
Article number	110972
Journal	Brain Research Bulletin
Volume	212
DOIs	https://doi.org/10.1016/j.brainresbull.2024.110972
Publication status	Published - 15 Jun 2024

Keywords

Electroencephalography (EEG)
Neurophysiology
Schizophrenia
TMS-evoked potentials (TEPs)
TMS-related spectral perturbations (TRSP)
Transcranial magnetic stimulation (TMS)

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10.1016/j.brainresbull.2024.110972

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@article{a39a4ec3a8904f7e8d35fa88694c08d4,

title = "Investigating cortical excitability and inhibition in patients with schizophrenia: A TMS-EEG study",

abstract = "Background: Transcranial magnetic stimulation (TMS) combined with electromyography (EMG) has widely been used as a non-invasive brain stimulation tool to assess excitation/inhibition (E/I) balance. E/I imbalance is a putative mechanism underlying symptoms in patients with schizophrenia. Combined TMS-electroencephalography (TMS-EEG) provides a detailed examination of cortical excitability to assess the pathophysiology of schizophrenia. This study aimed to investigate differences in TMS-evoked potentials (TEPs), TMS-related spectral perturbations (TRSP) and intertrial coherence (ITC) between patients with schizophrenia and healthy controls. Materials and methods: TMS was applied over the motor cortex during EEG recording. Differences in TEPs, TRSP and ITC between the patient and healthy subjects were analysed for all electrodes at each time point, by applying multiple independent sample t-tests with a cluster-based permutation analysis to correct for multiple comparisons. Results: Patients demonstrated significantly reduced amplitudes of early and late TEP components compared to healthy controls. Patients also showed a significant reduction of early delta (50–160 ms) and theta TRSP (30-250ms),followed by a reduction in alpha and beta suppression (220–560 ms; 190–420 ms). Patients showed a reduction of both early (50–110 ms) gamma increase and later (180–230 ms) gamma suppression. Finally, the ITC was significantly lower in patients in the alpha band, from 30 to 260 ms. Conclusion: Our findings support the putative role of impaired GABA-receptor mediated inhibition in schizophrenia impacting excitatory neurotransmission. Further studies can usefully elucidate mechanisms underlying specific symptoms clusters using TMS-EEG biometrics.",

keywords = "Electroencephalography (EEG), Neurophysiology, Schizophrenia, TMS-evoked potentials (TEPs), TMS-related spectral perturbations (TRSP), Transcranial magnetic stimulation (TMS)",

author = "V. Santoro and Hou, {M. D.} and I. Premoli and P. Belardinelli and A. Biondi and A. Carobin and F. Puledda and Michalopoulou, {P. G.} and Richardson, {M. P.} and L. Rocchi and Shergill, {S. S.}",

note = "Publisher Copyright: {\textcopyright} 2024 The Authors",

year = "2024",

month = jun,

day = "15",

doi = "10.1016/j.brainresbull.2024.110972",

language = "English",

volume = "212",

journal = "Brain Research Bulletin",

issn = "0361-9230",

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TY - JOUR

T1 - Investigating cortical excitability and inhibition in patients with schizophrenia

T2 - A TMS-EEG study

AU - Santoro, V.

AU - Hou, M. D.

AU - Premoli, I.

AU - Belardinelli, P.

AU - Biondi, A.

AU - Carobin, A.

AU - Puledda, F.

AU - Michalopoulou, P. G.

AU - Richardson, M. P.

AU - Rocchi, L.

AU - Shergill, S. S.

PY - 2024/6/15

Y1 - 2024/6/15

N2 - Background: Transcranial magnetic stimulation (TMS) combined with electromyography (EMG) has widely been used as a non-invasive brain stimulation tool to assess excitation/inhibition (E/I) balance. E/I imbalance is a putative mechanism underlying symptoms in patients with schizophrenia. Combined TMS-electroencephalography (TMS-EEG) provides a detailed examination of cortical excitability to assess the pathophysiology of schizophrenia. This study aimed to investigate differences in TMS-evoked potentials (TEPs), TMS-related spectral perturbations (TRSP) and intertrial coherence (ITC) between patients with schizophrenia and healthy controls. Materials and methods: TMS was applied over the motor cortex during EEG recording. Differences in TEPs, TRSP and ITC between the patient and healthy subjects were analysed for all electrodes at each time point, by applying multiple independent sample t-tests with a cluster-based permutation analysis to correct for multiple comparisons. Results: Patients demonstrated significantly reduced amplitudes of early and late TEP components compared to healthy controls. Patients also showed a significant reduction of early delta (50–160 ms) and theta TRSP (30-250ms),followed by a reduction in alpha and beta suppression (220–560 ms; 190–420 ms). Patients showed a reduction of both early (50–110 ms) gamma increase and later (180–230 ms) gamma suppression. Finally, the ITC was significantly lower in patients in the alpha band, from 30 to 260 ms. Conclusion: Our findings support the putative role of impaired GABA-receptor mediated inhibition in schizophrenia impacting excitatory neurotransmission. Further studies can usefully elucidate mechanisms underlying specific symptoms clusters using TMS-EEG biometrics.

AB - Background: Transcranial magnetic stimulation (TMS) combined with electromyography (EMG) has widely been used as a non-invasive brain stimulation tool to assess excitation/inhibition (E/I) balance. E/I imbalance is a putative mechanism underlying symptoms in patients with schizophrenia. Combined TMS-electroencephalography (TMS-EEG) provides a detailed examination of cortical excitability to assess the pathophysiology of schizophrenia. This study aimed to investigate differences in TMS-evoked potentials (TEPs), TMS-related spectral perturbations (TRSP) and intertrial coherence (ITC) between patients with schizophrenia and healthy controls. Materials and methods: TMS was applied over the motor cortex during EEG recording. Differences in TEPs, TRSP and ITC between the patient and healthy subjects were analysed for all electrodes at each time point, by applying multiple independent sample t-tests with a cluster-based permutation analysis to correct for multiple comparisons. Results: Patients demonstrated significantly reduced amplitudes of early and late TEP components compared to healthy controls. Patients also showed a significant reduction of early delta (50–160 ms) and theta TRSP (30-250ms),followed by a reduction in alpha and beta suppression (220–560 ms; 190–420 ms). Patients showed a reduction of both early (50–110 ms) gamma increase and later (180–230 ms) gamma suppression. Finally, the ITC was significantly lower in patients in the alpha band, from 30 to 260 ms. Conclusion: Our findings support the putative role of impaired GABA-receptor mediated inhibition in schizophrenia impacting excitatory neurotransmission. Further studies can usefully elucidate mechanisms underlying specific symptoms clusters using TMS-EEG biometrics.

KW - Electroencephalography (EEG)

KW - Neurophysiology

KW - Schizophrenia

KW - TMS-evoked potentials (TEPs)

KW - TMS-related spectral perturbations (TRSP)

KW - Transcranial magnetic stimulation (TMS)

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U2 - 10.1016/j.brainresbull.2024.110972

DO - 10.1016/j.brainresbull.2024.110972

M3 - Article

C2 - 38710310

AN - SCOPUS:85192110001

SN - 0361-9230

VL - 212

JO - Brain Research Bulletin

JF - Brain Research Bulletin

M1 - 110972

ER -

Investigating cortical excitability and inhibition in patients with schizophrenia: A TMS-EEG study

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Keywords

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