Spectral Parameters Modulation and Source Localization of Blink-Related Alpha and Low-Beta Oscillations Differentiate Minimally Conscious State from Vegetative State/Unresponsive Wakefulness Syndrome
Recently, the cortical source of blink-related delta oscillations (delta BROs) in resting healthy subjects has been localized in the posterior cingulate cortex/precuneus (PCC/PCu), one of the main core-hubs of the default-mode network. This has been interpreted as the electrophysiological signature...
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Published in | PloS one Vol. 9; no. 3; p. e93252 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Public Library of Science
27.03.2014
Public Library of Science (PLoS) |
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ISSN | 1932-6203 1932-6203 |
DOI | 10.1371/journal.pone.0093252 |
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Abstract | Recently, the cortical source of blink-related delta oscillations (delta BROs) in resting healthy subjects has been localized in the posterior cingulate cortex/precuneus (PCC/PCu), one of the main core-hubs of the default-mode network. This has been interpreted as the electrophysiological signature of the automatic monitoring of the surrounding environment while subjects are immersed in self-reflecting mental activities. Although delta BROs were directly correlated to the degree of consciousness impairment in patients with disorders of consciousness, they failed to differentiate vegetative state/unresponsive wakefulness syndrome (VS/UWS) from minimally conscious state (MCS). In the present study, we have extended the analysis of BROs to frequency bands other than delta in the attempt to find a biological marker that could support the differential diagnosis between VS/UWS and MCS. Four patients with VS/UWS, 5 patients with MCS, and 12 healthy matched controls (CTRL) underwent standard 19-channels EEG recordings during resting conditions. Three-second-lasting EEG epochs centred on each blink instance were submitted to time-frequency analyses in order to extract the normalized Blink-Related Synchronization/Desynchronization (nBRS/BRD) of three bands of interest (low-alpha, high-alpha and low-beta) in the time-window of 50-550 ms after the blink-peak and to estimate the corresponding cortical sources of electrical activity. VS/UWS nBRS/BRD levels of all three bands were lower than those related to both CTRL and MCS, thus enabling the differential diagnosis between MCS and VS/UWS. Furthermore, MCS showed an intermediate signal intensity on PCC/PCu between CTRL and VS/UWS and a higher signal intensity on the left temporo-parieto-occipital junction and inferior occipito-temporal regions when compared to VS/UWS. This peculiar pattern of activation leads us to hypothesize that resting MCS patients have a bottom-up driven activation of the task positive network and thus are tendentially prone to respond to environmental stimuli, even though in an almost unintentional way. |
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AbstractList | Recently, the cortical source of blink-related delta oscillations (delta BROs) in resting healthy subjects has been localized in the posterior cingulate cortex/precuneus (PCC/PCu), one of the main core-hubs of the default-mode network. This has been interpreted as the electrophysiological signature of the automatic monitoring of the surrounding environment while subjects are immersed in self-reflecting mental activities. Although delta BROs were directly correlated to the degree of consciousness impairment in patients with disorders of consciousness, they failed to differentiate vegetative state/unresponsive wakefulness syndrome (VS/UWS) from minimally conscious state (MCS). In the present study, we have extended the analysis of BROs to frequency bands other than delta in the attempt to find a biological marker that could support the differential diagnosis between VS/UWS and MCS. Four patients with VS/UWS, 5 patients with MCS, and 12 healthy matched controls (CTRL) underwent standard 19-channels EEG recordings during resting conditions. Three-second-lasting EEG epochs centred on each blink instance were submitted to time-frequency analyses in order to extract the normalized Blink-Related Synchronization/Desynchronization (nBRS/BRD) of three bands of interest (low-alpha, high-alpha and low-beta) in the time-window of 50-550 ms after the blink-peak and to estimate the corresponding cortical sources of electrical activity. VS/UWS nBRS/BRD levels of all three bands were lower than those related to both CTRL and MCS, thus enabling the differential diagnosis between MCS and VS/UWS. Furthermore, MCS showed an intermediate signal intensity on PCC/PCu between CTRL and VS/UWS and a higher signal intensity on the left temporo-parieto-occipital junction and inferior occipito-temporal regions when compared to VS/UWS. This peculiar pattern of activation leads us to hypothesize that resting MCS patients have a bottom-up driven activation of the task positive network and thus are tendentially prone to respond to environmental stimuli, even though in an almost unintentional way. Recently, the cortical source of blink-related delta oscillations (delta BROs) in resting healthy subjects has been localized in the posterior cingulate cortex/precuneus (PCC/PCu), one of the main core-hubs of the default-mode network. This has been interpreted as the electrophysiological signature of the automatic monitoring of the surrounding environment while subjects are immersed in self-reflecting mental activities. Although delta BROs were directly correlated to the degree of consciousness impairment in patients with disorders of consciousness, they failed to differentiate vegetative state/unresponsive wakefulness syndrome (VS/UWS) from minimally conscious state (MCS). In the present study, we have extended the analysis of BROs to frequency bands other than delta in the attempt to find a biological marker that could support the differential diagnosis between VS/UWS and MCS. Four patients with VS/UWS, 5 patients with MCS, and 12 healthy matched controls (CTRL) underwent standard 19-channels EEG recordings during resting conditions. Three-second-lasting EEG epochs centred on each blink instance were submitted to time-frequency analyses in order to extract the normalized Blink-Related Synchronization/Desynchronization (nBRS/BRD) of three bands of interest (low-alpha, high-alpha and low-beta) in the time-window of 50-550 ms after the blink-peak and to estimate the corresponding cortical sources of electrical activity. VS/UWS nBRS/BRD levels of all three bands were lower than those related to both CTRL and MCS, thus enabling the differential diagnosis between MCS and VS/UWS. Furthermore, MCS showed an intermediate signal intensity on PCC/PCu between CTRL and VS/UWS and a higher signal intensity on the left temporo-parieto-occipital junction and inferior occipito-temporal regions when compared to VS/UWS. This peculiar pattern of activation leads us to hypothesize that resting MCS patients have a bottom-up driven activation of the task positive network and thus are tendentially prone to respond to environmental stimuli, even though in an almost unintentional way.Recently, the cortical source of blink-related delta oscillations (delta BROs) in resting healthy subjects has been localized in the posterior cingulate cortex/precuneus (PCC/PCu), one of the main core-hubs of the default-mode network. This has been interpreted as the electrophysiological signature of the automatic monitoring of the surrounding environment while subjects are immersed in self-reflecting mental activities. Although delta BROs were directly correlated to the degree of consciousness impairment in patients with disorders of consciousness, they failed to differentiate vegetative state/unresponsive wakefulness syndrome (VS/UWS) from minimally conscious state (MCS). In the present study, we have extended the analysis of BROs to frequency bands other than delta in the attempt to find a biological marker that could support the differential diagnosis between VS/UWS and MCS. Four patients with VS/UWS, 5 patients with MCS, and 12 healthy matched controls (CTRL) underwent standard 19-channels EEG recordings during resting conditions. Three-second-lasting EEG epochs centred on each blink instance were submitted to time-frequency analyses in order to extract the normalized Blink-Related Synchronization/Desynchronization (nBRS/BRD) of three bands of interest (low-alpha, high-alpha and low-beta) in the time-window of 50-550 ms after the blink-peak and to estimate the corresponding cortical sources of electrical activity. VS/UWS nBRS/BRD levels of all three bands were lower than those related to both CTRL and MCS, thus enabling the differential diagnosis between MCS and VS/UWS. Furthermore, MCS showed an intermediate signal intensity on PCC/PCu between CTRL and VS/UWS and a higher signal intensity on the left temporo-parieto-occipital junction and inferior occipito-temporal regions when compared to VS/UWS. This peculiar pattern of activation leads us to hypothesize that resting MCS patients have a bottom-up driven activation of the task positive network and thus are tendentially prone to respond to environmental stimuli, even though in an almost unintentional way. |
Audience | Academic |
Author | Olcese, Umberto Arrighi, Pieranna Andre, Paolo Frisoli, Antonio Bergamasco, Massimo Rossi, Bruno Piarulli, Andrea Bonfiglio, Luca Carboncini, Maria Chiara |
AuthorAffiliation | 2 TeCIP Institute, PERCRO Laboratory, Scuola Superiore Sant'Anna, Pisa, Italy Weill Cornell Medical College, United States of America 1 Department of Translational Research on New Technologies in Medicine and Surgery, School of Physical Medicine and Rehabilitation, University of Pisa, Pisa, Italy 4 Department of Medical and Surgical Sciences and Neuroscience, University of Siena, Siena, Italy 3 Department of Neuroscience and Brain Technologies, Italian Institute of Technology, Genova, Italy |
AuthorAffiliation_xml | – name: 1 Department of Translational Research on New Technologies in Medicine and Surgery, School of Physical Medicine and Rehabilitation, University of Pisa, Pisa, Italy – name: 2 TeCIP Institute, PERCRO Laboratory, Scuola Superiore Sant'Anna, Pisa, Italy – name: 3 Department of Neuroscience and Brain Technologies, Italian Institute of Technology, Genova, Italy – name: 4 Department of Medical and Surgical Sciences and Neuroscience, University of Siena, Siena, Italy – name: Weill Cornell Medical College, United States of America |
Author_xml | – sequence: 1 givenname: Luca surname: Bonfiglio fullname: Bonfiglio, Luca – sequence: 2 givenname: Andrea surname: Piarulli fullname: Piarulli, Andrea – sequence: 3 givenname: Umberto surname: Olcese fullname: Olcese, Umberto – sequence: 4 givenname: Paolo surname: Andre fullname: Andre, Paolo – sequence: 5 givenname: Pieranna surname: Arrighi fullname: Arrighi, Pieranna – sequence: 6 givenname: Antonio surname: Frisoli fullname: Frisoli, Antonio – sequence: 7 givenname: Bruno surname: Rossi fullname: Rossi, Bruno – sequence: 8 givenname: Massimo surname: Bergamasco fullname: Bergamasco, Massimo – sequence: 9 givenname: Maria Chiara surname: Carboncini fullname: Carboncini, Maria Chiara |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24676098$$D View this record in MEDLINE/PubMed |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceived and designed the experiments: LB AP UO AF BR MB MCC. Performed the experiments: LB P. Andre P. Arrighi. Analyzed the data: AP UO. Contributed reagents/materials/analysis tools: AP UO. Wrote the paper: LB AP. Competing Interests: The authors have declared that no competing interests exist. |
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SubjectTerms | Activation Adult Aged Alpha Rhythm Analysis Analysis of Variance Beta Rhythm Biology and Life Sciences Biomarkers Blinking Brain Mapping Brain research Case-Control Studies Computer and Information Sciences Consciousness Cortex (cingulate) Cortex (occipital) Cortex (parietal) Cortex (temporal) Diagnosis Diagnosis, Differential Differential diagnosis EEG Electroencephalography Environmental effects Environmental monitoring Female Frequencies Gyrus Cinguli - physiopathology Humans Laboratories Localization Male Medical research Medicine Medicine and Health Sciences Memory Middle Aged Neurosciences Oscillations Patients Persistent vegetative state Persistent Vegetative State - diagnosis Persistent Vegetative State - etiology Persistent Vegetative State - physiopathology Rehabilitation Research and Analysis Methods Self awareness Sleep and wakefulness Surgery Synchronism Synchronization Syndrome Temporal lobe Trends Wakefulness Windows (intervals) Young Adult |
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Title | Spectral Parameters Modulation and Source Localization of Blink-Related Alpha and Low-Beta Oscillations Differentiate Minimally Conscious State from Vegetative State/Unresponsive Wakefulness Syndrome |
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