Cargando…

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

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 br...

Descripción completa

Detalles Bibliográficos
Autores principales: Scarpetta, Silvia, Morrisi, Niccolò, Mutti, Carlotta, Azzi, Nicoletta, Trippi, Irene, Ciliento, Rosario, Apicella, Ilenia, Messuti, Giovanni, Angiolelli, Marianna, Lombardi, Fabrizio, Parrino, Liborio, Vaudano, Anna Elisabetta
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10520337/
https://www.ncbi.nlm.nih.gov/pubmed/37766992
http://dx.doi.org/10.1016/j.isci.2023.107840
_version_ 1785109895605911552
author Scarpetta, Silvia
Morrisi, Niccolò
Mutti, Carlotta
Azzi, Nicoletta
Trippi, Irene
Ciliento, Rosario
Apicella, Ilenia
Messuti, Giovanni
Angiolelli, Marianna
Lombardi, Fabrizio
Parrino, Liborio
Vaudano, Anna Elisabetta
author_facet Scarpetta, Silvia
Morrisi, Niccolò
Mutti, Carlotta
Azzi, Nicoletta
Trippi, Irene
Ciliento, Rosario
Apicella, Ilenia
Messuti, Giovanni
Angiolelli, Marianna
Lombardi, Fabrizio
Parrino, Liborio
Vaudano, Anna Elisabetta
author_sort Scarpetta, Silvia
collection PubMed
description 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.
format Online
Article
Text
id pubmed-10520337
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Elsevier
record_format MEDLINE/PubMed
spelling pubmed-105203372023-09-27 Criticality of neuronal avalanches in human sleep and their relationship with sleep macro- and micro-architecture Scarpetta, Silvia Morrisi, Niccolò Mutti, Carlotta Azzi, Nicoletta Trippi, Irene Ciliento, Rosario Apicella, Ilenia Messuti, Giovanni Angiolelli, Marianna Lombardi, Fabrizio Parrino, Liborio Vaudano, Anna Elisabetta iScience Article 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. Elsevier 2023-09-09 /pmc/articles/PMC10520337/ /pubmed/37766992 http://dx.doi.org/10.1016/j.isci.2023.107840 Text en © 2023 The Authors https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Scarpetta, Silvia
Morrisi, Niccolò
Mutti, Carlotta
Azzi, Nicoletta
Trippi, Irene
Ciliento, Rosario
Apicella, Ilenia
Messuti, Giovanni
Angiolelli, Marianna
Lombardi, Fabrizio
Parrino, Liborio
Vaudano, Anna Elisabetta
Criticality of neuronal avalanches in human sleep and their relationship with sleep macro- and micro-architecture
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 Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10520337/
https://www.ncbi.nlm.nih.gov/pubmed/37766992
http://dx.doi.org/10.1016/j.isci.2023.107840
work_keys_str_mv AT scarpettasilvia criticalityofneuronalavalanchesinhumansleepandtheirrelationshipwithsleepmacroandmicroarchitecture
AT morrisiniccolo criticalityofneuronalavalanchesinhumansleepandtheirrelationshipwithsleepmacroandmicroarchitecture
AT mutticarlotta criticalityofneuronalavalanchesinhumansleepandtheirrelationshipwithsleepmacroandmicroarchitecture
AT azzinicoletta criticalityofneuronalavalanchesinhumansleepandtheirrelationshipwithsleepmacroandmicroarchitecture
AT trippiirene criticalityofneuronalavalanchesinhumansleepandtheirrelationshipwithsleepmacroandmicroarchitecture
AT cilientorosario criticalityofneuronalavalanchesinhumansleepandtheirrelationshipwithsleepmacroandmicroarchitecture
AT apicellailenia criticalityofneuronalavalanchesinhumansleepandtheirrelationshipwithsleepmacroandmicroarchitecture
AT messutigiovanni criticalityofneuronalavalanchesinhumansleepandtheirrelationshipwithsleepmacroandmicroarchitecture
AT angiolellimarianna criticalityofneuronalavalanchesinhumansleepandtheirrelationshipwithsleepmacroandmicroarchitecture
AT lombardifabrizio criticalityofneuronalavalanchesinhumansleepandtheirrelationshipwithsleepmacroandmicroarchitecture
AT parrinoliborio criticalityofneuronalavalanchesinhumansleepandtheirrelationshipwithsleepmacroandmicroarchitecture
AT vaudanoannaelisabetta criticalityofneuronalavalanchesinhumansleepandtheirrelationshipwithsleepmacroandmicroarchitecture