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      Evaluating Brain Activity in Patients With Chronic Disorders of Consciousness After Traumatic Brain Injury Using EEG Microstate Analysis During Hyperbaric Oxygen Therapy

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          ABSTRACT

          Background

          Hyperbaric oxygen (HBO) therapy is an efficacious intervention for patients with prolonged disorders of consciousness (pDOC). Electroencephalographic (EEG) microstate analysis can provide an assessment of the global state of the brain. Currently, the misdiagnosis rate of consciousness‐level assessments in patients with pDOC is high. Therefore, we aimed to assess the consciousness levels and outcomes of patients by analyzing changes in EEG signals during HBO therapy.

          Methods

          EEG data were collected from 32 patients with traumatic brain injury before and after 20 min of HBO therapy. EEG data were obtained during HBO therapy sessions. Modified k‐means clustering was used to segment EEG signals into microstates. A paired sample t test was used to compare the microstate characteristics before and during HBO therapy.

          Results

          The duration, occurrence, and coverage of microstate D significantly increased in the minimally conscious state (MCS) group after therapy. Significant increases in the same parameters were observed in microstate A among patients in the unresponsive wakefulness state group. Furthermore, patients with greater improvements in Coma Recovery Scale‐Revised scores (i.e., improvements of more than three points) showed significant increases in the duration, occurrence, and coverage of microstate D. Both the MCS group and the improvement group presented significant increases in the duration, occurrence, and coverage of microstate D during therapy.

          Conclusions

          Microstate D may be associated with the recovery of consciousness levels in patients. This study verified the safety and feasibility of real‐time EEG during HBO therapy for patients with pDOC. The changes in EEG microstate characteristics during HBO therapy can serve as a significant complement to electroencephalographic assessment indices for patients with pDOC and may be useful for predicting the recovery of consciousness levels.

          Abstract

          During HBO therapy, patients with pDOC exhibit regular changes in EEG microstates, which could serve as indicators to assess consciousness levels, and the characteristics of microstate D may hold predictive value for the potential recovery of consciousness.

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          Most cited references42

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          The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility.

          To determine the measurement properties and diagnostic utility of the JFK Coma Recovery Scale-Revised (CRS-R). Analysis of interrater and test-retest reliability, internal consistency, concurrent validity, and diagnostic accuracy. Acute inpatient brain injury rehabilitation hospital. Convenience sample of 80 patients with severe acquired brain injury admitted to an inpatient Coma Intervention Program with a diagnosis of either vegetative state (VS) or minimally conscious state (MCS). Not applicable. The CRS-R, the JFK Coma Recovery Scale (CRS), and the Disability Rating Scale (DRS). Interrater and test-retest reliability were high for CRS-R total scores. Subscale analysis showed moderate to high interrater and test-retest agreement although systematic differences in scoring were noted on the visual and oromotor/verbal subscales. CRS-R total scores correlated significantly with total scores on the CRS and DRS indicating acceptable concurrent validity. The CRS-R was able to distinguish 10 patients in an MCS who were otherwise misclassified as in a VS by the DRS. The CRS-R can be administered reliably by trained examiners and repeated measurements yield stable estimates of patient status. CRS-R subscale scores demonstrated good agreement across raters and ratings but should be used cautiously because some scores were underrepresented in the current study. The CRS-R appears capable of differentiating patients in an MCS from those in a VS.
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            BOLD correlates of EEG topography reveal rapid resting-state network dynamics.

            Resting-state functional connectivity studies with fMRI showed that the brain is intrinsically organized into large-scale functional networks for which the hemodynamic signature is stable for about 10s. Spatial analyses of the topography of the spontaneous EEG also show discrete epochs of stable global brain states (so-called microstates), but they remain quasi-stationary for only about 100 ms. In order to test the relationship between the rapidly fluctuating EEG-defined microstates and the slowly oscillating fMRI-defined resting states, we recorded 64-channel EEG in the scanner while subjects were at rest with their eyes closed. Conventional EEG-microstate analysis determined the typical four EEG topographies that dominated across all subjects. The convolution of the time course of these maps with the hemodynamic response function allowed to fit a linear model to the fMRI BOLD responses and revealed four distinct distributed networks. These networks were spatially correlated with four of the resting-state networks (RSNs) that were found by the conventional fMRI group-level independent component analysis (ICA). These RSNs have previously been attributed to phonological processing, visual imagery, attention reorientation, and subjective interoceptive-autonomic processing. We found no EEG-correlate of the default mode network. Thus, the four typical microstates of the spontaneous EEG seem to represent the neurophysiological correlate of four of the RSNs and show that they are fluctuating much more rapidly than fMRI alone suggests. Copyright 2010 Elsevier Inc. All rights reserved.
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              EEG microstates as a tool for studying the temporal dynamics of whole-brain neuronal networks: A review

              The present review discusses a well-established method for characterizing resting-state activity of the human brain using multichannel electroencephalography (EEG). This method involves the examination of electrical microstates in the brain, which are defined as successive short time periods during which the configuration of the scalp potential field remains semi-stable, suggesting quasi-simultaneity of activity among the nodes of large-scale networks. A few prototypic microstates, which occur in a repetitive sequence across time, can be reliably identified across participants. Researchers have proposed that these microstates represent the basic building blocks of the chain of spontaneous conscious mental processes, and that their occurrence and temporal dynamics determine the quality of mentation. Several studies have further demonstrated that disturbances of mental processes associated with neurological and psychiatric conditions manifest as changes in the temporal dynamics of specific microstates. Combined EEG-fMRI studies and EEG source imaging studies have indicated that EEG microstates are closely associated with resting-state networks as identified using fMRI. The scale-free properties of the time series of EEG microstates explain why similar networks can be observed at such different time scales. The present review will provide an overview of these EEG microstates, available methods for analysis, the functional interpretations of findings regarding these microstates, and their behavioral and clinical correlates.
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                Author and article information

                Contributors
                zhaoxudong@ibp.ac.cn
                yuqiuhong@bjtth.org
                Journal
                CNS Neurosci Ther
                CNS Neurosci Ther
                10.1111/(ISSN)1755-5949
                CNS
                CNS Neuroscience & Therapeutics
                John Wiley and Sons Inc. (Hoboken )
                1755-5930
                1755-5949
                20 January 2025
                January 2025
                : 31
                : 1 ( doiID: 10.1111/cns.v31.1 )
                : e70220
                Affiliations
                [ 1 ] Department of Neurosurgery, Beijing Tiantan Hospital Capital Medical University Beijing China
                [ 2 ] China National Clinical Research Center for Neurological Diseases Beijing China
                [ 3 ] Institute of Artificial Intelligence Hefei Comprehensive National Science Center Hefei China
                [ 4 ] Department of Hyperbaric Oxygenation, Beijing Tiantan Hospital Capital Medical University Beijing China
                [ 5 ] State Key Laboratory of Brain and Cognitive Science Institute of Biophysics, Chinese Academy of Sciences Beijing China
                [ 6 ] CAS Center for Excellence in Brain Science and Intelligence Technology Beijing China
                [ 7 ] University of Chinese Academy of Sciences Beijing China
                Author notes
                [*] [* ] Correspondence:

                Xudong Zhao ( zhaoxudong@ 123456ibp.ac.cn )

                Qiuhong Yu ( yuqiuhong@ 123456bjtth.org )

                Author information
                https://orcid.org/0000-0002-3369-5588
                https://orcid.org/0000-0003-4749-6210
                https://orcid.org/0000-0001-9470-9966
                Article
                CNS70220 CNSNT-2024-2041.R1
                10.1111/cns.70220
                11746936
                39834088
                5b29e6ef-e57a-472f-b85d-7383005d51ee
                © 2025 The Author(s). CNS Neuroscience & Therapeutics published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 19 December 2024
                : 08 October 2024
                : 06 January 2025
                Page count
                Figures: 11, Tables: 9, Pages: 16, Words: 9200
                Funding
                Funded by: Beijing Municipal Natural Science Foundation , doi 10.13039/501100005089;
                Award ID: 7232046
                Funded by: National Natural Science Foundation of China , doi 10.13039/501100001809;
                Award ID: U21A20388
                Award ID: 31730039
                Award ID: 82272118
                Funded by: Chinese Academy of Sciences grants
                Award ID: ZDBS‐LY‐SM028
                Funded by: STI2030‐Major Projects
                Award ID: 2021ZD0204200
                Funded by: Ministry of Science and Technology of the People’s Republic of China , doi 10.13039/501100002855;
                Award ID: 2019YFA0707103
                Categories
                Original Article
                Original Article
                Custom metadata
                2.0
                January 2025
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.5.2 mode:remove_FC converted:21.01.2025

                Neurosciences
                eeg,hyperbaric oxygen,microstate,prolonged docs,traumatic brain injury
                Neurosciences
                eeg, hyperbaric oxygen, microstate, prolonged docs, traumatic brain injury

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