Altered spreading of fast aperiodic brain waves relates to disease duration in Amyotrophic Lateral Sclerosis

Arianna Polverino; Emahnuel Troisi Lopez; Marianna Liparoti; Roberta Minino; Antonella Romano; Lorenzo Cipriano; Francesca Trojsi; Viktor Jirsa; Giuseppe Sorrentino; Pierpaolo Sorrentino

doi:10.1016/j.clinph.2024.04.003

Altered spreading of fast aperiodic brain waves relates to disease duration in Amyotrophic Lateral Sclerosis

Clin Neurophysiol. 2024 Apr 16:163:14-21. doi: 10.1016/j.clinph.2024.04.003. Online ahead of print.

Affiliations

¹ Institute of Diagnosis and Treatment Hermitage Capodimonte, 80131 Naples, Italy.
² Institute of Applied Sciences and Intelligent Systems of National Research Council, 80078 Pozzuoli, Italy.
³ Department of Philosophical, Pedagogical and Economic-Quantitative Sciences, University of Chieti-Pescara G. D'Annunzio, 66100 Chieti, Italy.
⁴ Department of Medical, Motor and Wellness Sciences, University of Naples Parthenope, 80133 Naples, Italy.
⁵ Department of Advanced Medical and Surgical Sciences, University of Campania Luigi Vanvitelli, 81100 Naples, Italy.
⁶ Institut de Neurosciences des Systèmes, Inserm, INS, Aix-Marseille University, 13005 Marseille, France.
⁷ Institute of Diagnosis and Treatment Hermitage Capodimonte, 80131 Naples, Italy; Institute of Applied Sciences and Intelligent Systems of National Research Council, 80078 Pozzuoli, Italy; Department of Medical, Motor and Wellness Sciences, University of Naples Parthenope, 80133 Naples, Italy. Electronic address: giuseppe.sorrentino@uniparthenope.it.
⁸ Institute of Applied Sciences and Intelligent Systems of National Research Council, 80078 Pozzuoli, Italy; Institut de Neurosciences des Systèmes, Inserm, INS, Aix-Marseille University, 13005 Marseille, France; Department of Biomedical Sciences, University of Sassari, 07100 Sassari, Italy.

PMID: 38663099
DOI: 10.1016/j.clinph.2024.04.003

Abstract

Objective: To test the hypothesis that patients affected by Amyotrophic Lateral Sclerosis (ALS) show an altered spatio-temporal spreading of neuronal avalanches in the brain, and that this may related to the clinical picture.

Methods: We obtained the source-reconstructed magnetoencephalography (MEG) signals from thirty-six ALS patients and forty-two healthy controls. Then, we used the construct of the avalanche transition matrix (ATM) and the corresponding network parameter nodal strength to quantify the changes in each region, since this parameter provides key information about which brain regions are mostly involved in the spreading avalanches.

Results: ALS patients presented higher values of the nodal strength in both cortical and sub-cortical brain areas. This parameter correlated directly with disease duration.

Conclusions: In this work, we provide a deeper characterization of neuronal avalanches propagation in ALS, describing their spatio-temporal trajectories and identifying the brain regions most likely to be involved in the process. This makes it possible to recognize the brain areas that take part in the pathogenic mechanisms of ALS. Furthermore, the nodal strength of the involved regions correlates directly with disease duration.

Significance: Our results corroborate the clinical relevance of aperiodic, fast large-scale brain activity as a biomarker of microscopic changes induced by neurophysiological processes.

Keywords: Amyotrophic lateral sclerosis; Avalanche transition matrix; Brain dynamics; Functional repertoire; Magnetoencephalography; Neuronal avalanches.