Criticality of neuronal avalanches in human sleep and their relationship with sleep macro- and micro-architecture

Summary: Sleep plays a key role in preserving brain function, keeping brain networks in a state that ensures optimal computation. Empirical evidence indicates that this state is consistent with criticality, where scale-free neuronal avalanches emerge. However, the connection between sleep architectu...

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Main Authors: Silvia Scarpetta, Niccolò Morrisi, Carlotta Mutti, Nicoletta Azzi, Irene Trippi, Rosario Ciliento, Ilenia Apicella, Giovanni Messuti, Marianna Angiolelli, Fabrizio Lombardi, Liborio Parrino, Anna Elisabetta Vaudano
Format: Article
Language:English
Published: Elsevier 2023-10-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S258900422301917X
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author Silvia Scarpetta
Niccolò Morrisi
Carlotta Mutti
Nicoletta Azzi
Irene Trippi
Rosario Ciliento
Ilenia Apicella
Giovanni Messuti
Marianna Angiolelli
Fabrizio Lombardi
Liborio Parrino
Anna Elisabetta Vaudano
author_facet Silvia Scarpetta
Niccolò Morrisi
Carlotta Mutti
Nicoletta Azzi
Irene Trippi
Rosario Ciliento
Ilenia Apicella
Giovanni Messuti
Marianna Angiolelli
Fabrizio Lombardi
Liborio Parrino
Anna Elisabetta Vaudano
author_sort Silvia Scarpetta
collection DOAJ
description Summary: Sleep plays a key role in preserving brain function, keeping brain networks in a state that ensures optimal computation. Empirical evidence indicates that this state is consistent with criticality, where scale-free neuronal avalanches emerge. However, the connection between sleep architecture and brain tuning to criticality remains poorly understood. Here, we characterize the critical behavior of avalanches and study their relationship with sleep macro- and micro-architectures, in particular, the cyclic alternating pattern (CAP). We show that avalanches exhibit robust scaling behaviors, with exponents obeying scaling relations consistent with the mean-field directed percolation universality class. We demonstrate that avalanche dynamics is modulated by the NREM-REM cycles and that, within NREM sleep, avalanche occurrence correlates with CAP activation phases—indicating a potential link between CAP and brain tuning to criticality. The results open new perspectives on the collective dynamics underlying CAP function, and on the relationship between sleep architecture, avalanches, and self-organization to criticality.
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spelling doaj.art-8cdf1822ce304e49a121f311840931ce2023-10-28T05:08:42ZengElsevieriScience2589-00422023-10-012610107840Criticality of neuronal avalanches in human sleep and their relationship with sleep macro- and micro-architectureSilvia Scarpetta0Niccolò Morrisi1Carlotta Mutti2Nicoletta Azzi3Irene Trippi4Rosario Ciliento5Ilenia Apicella6Giovanni Messuti7Marianna Angiolelli8Fabrizio Lombardi9Liborio Parrino10Anna Elisabetta Vaudano11Department of Physics, University of Salerno, 84084 Fisciano, Italy; INFN sez. Napoli Gr. Coll. Salerno, 84084 Fisciano, Italy; Corresponding authorNephrology, Dialysis and Transplant Unit, University Hospital of Modena, 41121 Modena, ItalySleep Disorders Center, Department of Medicine and Surgery, University of Parma, 43121 Parma, ItalySleep Disorders Center, Department of Medicine and Surgery, University of Parma, 43121 Parma, ItalySleep Disorders Center, Department of Medicine and Surgery, University of Parma, 43121 Parma, ItalyDepartment of Neurology, University of Wisconsin, Madison, WI 53705, USAINFN sez. Napoli Gr. Coll. Salerno, 84084 Fisciano, Italy; Department of Physics, University of Naples “Federico II”, 80126 Napoli, ItalyDepartment of Physics, University of Salerno, 84084 Fisciano, Italy; INFN sez. Napoli Gr. Coll. Salerno, 84084 Fisciano, ItalyDepartment of Physics, University of Salerno, 84084 Fisciano, Italy; INFN sez. Napoli Gr. Coll. Salerno, 84084 Fisciano, Italy; Engineering Department, University Campus Bio-Medico of Rome, 00128 Roma, ItalyInstitute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria; Department of Biomedical Sciences, University of Padova, Via Ugo Bassi 58B, 35131 Padova, ItalySleep Disorders Center, Department of Medicine and Surgery, University of Parma, 43121 Parma, ItalyNeurology Unit, Azienda Ospedaliero-Universitaria of Modena, OCB Hospital, 41125 Modena, Italy; Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, 41125 Modena, Italy; Corresponding authorSummary: Sleep plays a key role in preserving brain function, keeping brain networks in a state that ensures optimal computation. Empirical evidence indicates that this state is consistent with criticality, where scale-free neuronal avalanches emerge. However, the connection between sleep architecture and brain tuning to criticality remains poorly understood. Here, we characterize the critical behavior of avalanches and study their relationship with sleep macro- and micro-architectures, in particular, the cyclic alternating pattern (CAP). We show that avalanches exhibit robust scaling behaviors, with exponents obeying scaling relations consistent with the mean-field directed percolation universality class. We demonstrate that avalanche dynamics is modulated by the NREM-REM cycles and that, within NREM sleep, avalanche occurrence correlates with CAP activation phases—indicating a potential link between CAP and brain tuning to criticality. The results open new perspectives on the collective dynamics underlying CAP function, and on the relationship between sleep architecture, avalanches, and self-organization to criticality.http://www.sciencedirect.com/science/article/pii/S258900422301917XBiological sciencesNeuroscience
spellingShingle Silvia Scarpetta
Niccolò Morrisi
Carlotta Mutti
Nicoletta Azzi
Irene Trippi
Rosario Ciliento
Ilenia Apicella
Giovanni Messuti
Marianna Angiolelli
Fabrizio Lombardi
Liborio Parrino
Anna Elisabetta Vaudano
Criticality of neuronal avalanches in human sleep and their relationship with sleep macro- and micro-architecture
iScience
Biological sciences
Neuroscience
title Criticality of neuronal avalanches in human sleep and their relationship with sleep macro- and micro-architecture
title_full Criticality of neuronal avalanches in human sleep and their relationship with sleep macro- and micro-architecture
title_fullStr Criticality of neuronal avalanches in human sleep and their relationship with sleep macro- and micro-architecture
title_full_unstemmed Criticality of neuronal avalanches in human sleep and their relationship with sleep macro- and micro-architecture
title_short Criticality of neuronal avalanches in human sleep and their relationship with sleep macro- and micro-architecture
title_sort criticality of neuronal avalanches in human sleep and their relationship with sleep macro and micro architecture
topic Biological sciences
Neuroscience
url http://www.sciencedirect.com/science/article/pii/S258900422301917X
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