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

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

NeuroImage (Jan 2023)

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

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

Affiliations

Andrea Buccellato: Padova Neuroscience Center, University of Padova, Padova, Italy; Department of General Psychology, University of Padova, Padova, Italy; Corresponding authors.
Di Zang: 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, China
Federico Zilio: Department of Philosophy, Sociology, Education and Applied Psychology, University of Padova, Padua, Italy
Javier Gomez-Pilar: Biomedical 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, Spain
Zhe Wang: 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, China
Zengxin Qi: 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, China
Ruizhe Zheng: 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, China
Zeyu Xu: 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, China
Xuehai Wu: 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, China
Patrizia Bisiacchi: Padova Neuroscience Center, University of Padova, Padova, Italy; Department of General Psychology, University of Padova, Padova, Italy
Alessandra Del Felice: Padova Neuroscience Center, University of Padova, Padova, Italy; Department of Neuroscience, Section of Rehabilitation, University of Padova, Padova, Italy
Ying Mao: 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, China; Corresponding authors.
Georg Northoff: 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.

Journal volume & issue: Vol. 265
p. 119802

Abstract

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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.

Published in NeuroImage

ISSN: 1053-8119 (Print); 1095-9572 (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry
Website: https://www.journals.elsevier.com/neuroimage

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