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

Silvia Scarpetta; Niccolò Morisi; Carlotta Mutti; Nicoletta Azzi; Irene Trippi; Rosario Ciliento; Ilenia Apicella; Giovanni Messuti; Marianna Angiolelli; Fabrizio Lombardi; Liborio Parrino; Anna Elisabetta Vaudano

doi:10.1016/j.isci.2023.107840

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

iScience. 2023 Sep 9;26(10):107840. doi: 10.1016/j.isci.2023.107840. eCollection 2023 Oct 20.

Authors

Silvia Scarpetta^{1

2}, Niccolò Morisi³, Carlotta Mutti⁴, Nicoletta Azzi⁴, Irene Trippi⁴, Rosario Ciliento⁵, Ilenia Apicella^{2

6}, Giovanni Messuti^{1

2}, Marianna Angiolelli^{1

2

7}, Fabrizio Lombardi^{8

9}, Liborio Parrino⁴, Anna Elisabetta Vaudano^{10

11}

Affiliations

¹ Department of Physics, University of Salerno, 84084 Fisciano, Italy.
² INFN sez. Napoli Gr. Coll. Salerno, 84084 Fisciano, Italy.
³ Nephrology, Dialysis and Transplant Unit, University Hospital of Modena, 41121 Modena, Italy.
⁴ Sleep Disorders Center, Department of Medicine and Surgery, University of Parma, 43121 Parma, Italy.
⁵ Department of Neurology, University of Wisconsin, Madison, WI 53705, USA.
⁶ Department of Physics, University of Naples "Federico II", 80126 Napoli, Italy.
⁷ Engineering Department, University Campus Bio-Medico of Rome, 00128 Roma, Italy.
⁸ Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria.
⁹ Department of Biomedical Sciences, University of Padova, Via Ugo Bassi 58B, 35131 Padova, Italy.
¹⁰ Neurology Unit, Azienda Ospedaliero-Universitaria of Modena, OCB Hospital, 41125 Modena, Italy.
¹¹ Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, 41125 Modena, Italy.

Abstract

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.

Keywords: Biological sciences; Neuroscience.