Disrupted relationship between intrinsic neural timescales and alpha peak frequency during unconscious states – A high-density EEG study

Our brain processes the different timescales of our environment's temporal input stochastics. Is such a temporal input processing mechanism key for consciousness? To address this research question, we calculated measures of input processing on shorter (alpha peak frequency, APF) and longer (aut...

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Main Authors: Andrea Buccellato, Di Zang, Federico Zilio, Javier Gomez-Pilar, Zhe Wang, Zengxin Qi, Ruizhe Zheng, Zeyu Xu, Xuehai Wu, Patrizia Bisiacchi, Alessandra Del Felice, Ying Mao, Georg Northoff
Format: Article
Language:English
Published: Elsevier 2023-01-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811922009235
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author Andrea Buccellato
Di Zang
Federico Zilio
Javier Gomez-Pilar
Zhe Wang
Zengxin Qi
Ruizhe Zheng
Zeyu Xu
Xuehai Wu
Patrizia Bisiacchi
Alessandra Del Felice
Ying Mao
Georg Northoff
author_facet Andrea Buccellato
Di Zang
Federico Zilio
Javier Gomez-Pilar
Zhe Wang
Zengxin Qi
Ruizhe Zheng
Zeyu Xu
Xuehai Wu
Patrizia Bisiacchi
Alessandra Del Felice
Ying Mao
Georg Northoff
author_sort Andrea Buccellato
collection DOAJ
description Our brain processes the different timescales of our environment's temporal input stochastics. Is such a temporal input processing mechanism key for consciousness? To address this research question, we calculated measures of input processing on shorter (alpha peak frequency, APF) and longer (autocorrelation window, ACW) timescales on resting-state high-density EEG (256 channels) recordings and compared them across different consciousness levels (awake/conscious, ketamine and sevoflurane anaesthesia, unresponsive wakefulness, minimally conscious state). We replicate and extend previous findings of: (i) significantly longer ACW values, consistently over all states of unconsciousness, as measured with ACW-0 (an unprecedented longer version of the well-know ACW-50); (ii) significantly slower APF values, as measured with frequency sliding, in all four unconscious states. Most importantly, we report a highly significant correlation of ACW-0 and APF in the conscious state, while their relationship is disrupted in the unconscious states. In sum, we demonstrate the relevance of the brain's capacity for input processing on shorter (APF) and longer (ACW) timescales - including their relationship - for consciousness. Albeit indirectly, e.g., through the analysis of electrophysiological activity at rest, this supports the mechanism of temporo-spatial alignment to the environment's temporal input stochastics, through relating different neural timescales, as one key predisposing factor of consciousness.
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spelling doaj.art-b8857d19612d46b2be293cd07a260f4a2023-01-05T06:23:27ZengElsevierNeuroImage1095-95722023-01-01265119802Disrupted relationship between intrinsic neural timescales and alpha peak frequency during unconscious states – A high-density EEG studyAndrea Buccellato0Di Zang1Federico Zilio2Javier Gomez-Pilar3Zhe Wang4Zengxin Qi5Ruizhe Zheng6Zeyu Xu7Xuehai Wu8Patrizia Bisiacchi9Alessandra Del Felice10Ying Mao11Georg Northoff12Padova Neuroscience Center, University of Padova, Padova, Italy; Department of General Psychology, University of Padova, Padova, Italy; Corresponding authors.Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University,Shanghai, 200040, China; Shanghai Key Laboratory of Brain Function and Restoration and Neural Regeneration, Shanghai, 200040, China; State Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science, School of Basic Medical Sciences and Institutes of Brain Science, Fudan University, Shanghai, 200032, China; National Center for Neurological Disorders, Shanghai, 200040, China; Neurosurgical Institute of Fudan University, Shanghai, 200040, China; Shanghai Clinical Medical Center of Neurosurgery, Shanghai, 200040, ChinaDepartment of Philosophy, Sociology, Education and Applied Psychology, University of Padova, Padua, ItalyBiomedical Engineering Group, University of Valladolid, Paseo de Belén, 15, Valladolid 47011, Spain; Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina, (CIBER-BBN), Valladolid, SpainDepartment of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University,Shanghai, 200040, China; Shanghai Key Laboratory of Brain Function and Restoration and Neural Regeneration, Shanghai, 200040, China; State Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science, School of Basic Medical Sciences and Institutes of Brain Science, Fudan University, Shanghai, 200032, China; National Center for Neurological Disorders, Shanghai, 200040, China; Neurosurgical Institute of Fudan University, Shanghai, 200040, China; Shanghai Clinical Medical Center of Neurosurgery, Shanghai, 200040, ChinaDepartment of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University,Shanghai, 200040, China; Shanghai Key Laboratory of Brain Function and Restoration and Neural Regeneration, Shanghai, 200040, China; State Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science, School of Basic Medical Sciences and Institutes of Brain Science, Fudan University, Shanghai, 200032, China; National Center for Neurological Disorders, Shanghai, 200040, China; Neurosurgical Institute of Fudan University, Shanghai, 200040, China; Shanghai Clinical Medical Center of Neurosurgery, Shanghai, 200040, ChinaDepartment of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University,Shanghai, 200040, China; Shanghai Key Laboratory of Brain Function and Restoration and Neural Regeneration, Shanghai, 200040, China; State Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science, School of Basic Medical Sciences and Institutes of Brain Science, Fudan University, Shanghai, 200032, China; National Center for Neurological Disorders, Shanghai, 200040, China; Neurosurgical Institute of Fudan University, Shanghai, 200040, China; Shanghai Clinical Medical Center of Neurosurgery, Shanghai, 200040, ChinaDepartment of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University,Shanghai, 200040, China; Shanghai Key Laboratory of Brain Function and Restoration and Neural Regeneration, Shanghai, 200040, China; State Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science, School of Basic Medical Sciences and Institutes of Brain Science, Fudan University, Shanghai, 200032, China; National Center for Neurological Disorders, Shanghai, 200040, China; Neurosurgical Institute of Fudan University, Shanghai, 200040, China; Shanghai Clinical Medical Center of Neurosurgery, Shanghai, 200040, ChinaDepartment of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University,Shanghai, 200040, China; Shanghai Key Laboratory of Brain Function and Restoration and Neural Regeneration, Shanghai, 200040, China; State Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science, School of Basic Medical Sciences and Institutes of Brain Science, Fudan University, Shanghai, 200032, China; National Center for Neurological Disorders, Shanghai, 200040, China; Neurosurgical Institute of Fudan University, Shanghai, 200040, China; Shanghai Clinical Medical Center of Neurosurgery, Shanghai, 200040, ChinaPadova Neuroscience Center, University of Padova, Padova, Italy; Department of General Psychology, University of Padova, Padova, ItalyPadova Neuroscience Center, University of Padova, Padova, Italy; Department of Neuroscience, Section of Rehabilitation, University of Padova, Padova, ItalyDepartment of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University,Shanghai, 200040, China; Shanghai Key Laboratory of Brain Function and Restoration and Neural Regeneration, Shanghai, 200040, China; State Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science, School of Basic Medical Sciences and Institutes of Brain Science, Fudan University, Shanghai, 200032, China; National Center for Neurological Disorders, Shanghai, 200040, China; Neurosurgical Institute of Fudan University, Shanghai, 200040, China; Shanghai Clinical Medical Center of Neurosurgery, Shanghai, 200040, China; Corresponding authors.Mind, Brain Imaging and Neuroethics Research Unit, Institute of Mental Health, Royal Ottawa Mental Health Centre and University of Ottawa, Ottawa, Ontario K1Z7K4, Canada; Mental Health Center, Zhejiang University School of Medicine, Hangzhou 310013, Zhejiang Province, China; Centre for Cognition and Brain Disorders, Hangzhou Normal University, Hangzhou 310013, Zhejiang Province, China; Corresponding authors.Our brain processes the different timescales of our environment's temporal input stochastics. Is such a temporal input processing mechanism key for consciousness? To address this research question, we calculated measures of input processing on shorter (alpha peak frequency, APF) and longer (autocorrelation window, ACW) timescales on resting-state high-density EEG (256 channels) recordings and compared them across different consciousness levels (awake/conscious, ketamine and sevoflurane anaesthesia, unresponsive wakefulness, minimally conscious state). We replicate and extend previous findings of: (i) significantly longer ACW values, consistently over all states of unconsciousness, as measured with ACW-0 (an unprecedented longer version of the well-know ACW-50); (ii) significantly slower APF values, as measured with frequency sliding, in all four unconscious states. Most importantly, we report a highly significant correlation of ACW-0 and APF in the conscious state, while their relationship is disrupted in the unconscious states. In sum, we demonstrate the relevance of the brain's capacity for input processing on shorter (APF) and longer (ACW) timescales - including their relationship - for consciousness. Albeit indirectly, e.g., through the analysis of electrophysiological activity at rest, this supports the mechanism of temporo-spatial alignment to the environment's temporal input stochastics, through relating different neural timescales, as one key predisposing factor of consciousness.http://www.sciencedirect.com/science/article/pii/S1053811922009235ElectroencephalographyIntrinsic neural timescalesAlpha peak frequencyDisorders of consciousnessAnaesthesiaTemporal input processing
spellingShingle Andrea Buccellato
Di Zang
Federico Zilio
Javier Gomez-Pilar
Zhe Wang
Zengxin Qi
Ruizhe Zheng
Zeyu Xu
Xuehai Wu
Patrizia Bisiacchi
Alessandra Del Felice
Ying Mao
Georg Northoff
Disrupted relationship between intrinsic neural timescales and alpha peak frequency during unconscious states – A high-density EEG study
NeuroImage
Electroencephalography
Intrinsic neural timescales
Alpha peak frequency
Disorders of consciousness
Anaesthesia
Temporal input processing
title Disrupted relationship between intrinsic neural timescales and alpha peak frequency during unconscious states – A high-density EEG study
title_full Disrupted relationship between intrinsic neural timescales and alpha peak frequency during unconscious states – A high-density EEG study
title_fullStr Disrupted relationship between intrinsic neural timescales and alpha peak frequency during unconscious states – A high-density EEG study
title_full_unstemmed Disrupted relationship between intrinsic neural timescales and alpha peak frequency during unconscious states – A high-density EEG study
title_short Disrupted relationship between intrinsic neural timescales and alpha peak frequency during unconscious states – A high-density EEG study
title_sort disrupted relationship between intrinsic neural timescales and alpha peak frequency during unconscious states a high density eeg study
topic Electroencephalography
Intrinsic neural timescales
Alpha peak frequency
Disorders of consciousness
Anaesthesia
Temporal input processing
url http://www.sciencedirect.com/science/article/pii/S1053811922009235
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