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

Author:

Polverino Arianna1ORCID,Lopez Emahnuel Troisi2ORCID,Liparoti Marianna3ORCID,Minino Roberta4ORCID,Romano Antonella4ORCID,Cipriano Lorenzo4ORCID,Trojsi Francesca5ORCID,Jirsa Viktor6ORCID,Sorrentino Giuseppe7ORCID,Sorrentino Pierpaolo8ORCID

Affiliation:

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 Motor Sciences and Wellness, 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 Motor Sciences and Wellness, University of Naples Parthenope, 80133 Naples, Italy

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

Abstract

Abstract Amyotrophic lateral sclerosis (ALS) is a multisystem disorder, as supported by clinical, molecular and neuroimaging evidence. Functional connectivity (FC) studies show alterations in the topological organization of brain network in ALS patients, demonstrating a hyper-connectedness as the disease progresses. This functionally hyper-connected network can be linked to altered brain dynamics, since the brain activity is characterized by large-scale bursts of activations, defined as neuronal avalanches. The number of unique avalanche patterns (i.e., the size of the functional repertoire) might be used as a readout of brain flexibility. In fact, we have previously shown that the size of the functional repertoire is reduced in ALS and predicts clinical disability. However, this approach did not provide information on the spatio-temporal spreading of neuronal avalanches in the brain. In this work, we hypothesized that ALS patients would show an altered spreading of neuronal avalanches. To test our hypothesis, we obtained the source-reconstructed MEG signals from thirty-six ALS patients and forty-two healthy controls. Then, we used the construct of the avalanche transition matrix (ATM), which represents the probability that two brain regions are consecutively recruited in an avalanche, and used the corresponding network parameter nodal strength to quantify the changes in each region. In fact, this parameter provides key information about which brain regions are mostly involved in the spreading avalanches. Our work demonstrated that ALS patients present higher values of the nodal strength in both cortical and sub-cortical brain areas. Furthermore, the nodal strength correlates directly with disease duration.

Publisher

Research Square Platform LLC

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