Brain fingerprint is based on the aperiodic, scale-free, neuronal activity

Subject differentiation bears the possibility to individualize brain analyses. However, the nature of the processes generating subject-specific features remains unknown. Most of the current literature uses techniques that assume stationarity (e.g., Pearson's correlation), which might fail to ca...

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Main Authors: Pierpaolo Sorrentino, Emahnuel Troisi Lopez, Antonella Romano, Carmine Granata, Marie Constance Corsi, Giuseppe Sorrentino, Viktor Jirsa
Format: Article
Language:English
Published: Elsevier 2023-08-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811923004111
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author Pierpaolo Sorrentino
Emahnuel Troisi Lopez
Antonella Romano
Carmine Granata
Marie Constance Corsi
Giuseppe Sorrentino
Viktor Jirsa
author_facet Pierpaolo Sorrentino
Emahnuel Troisi Lopez
Antonella Romano
Carmine Granata
Marie Constance Corsi
Giuseppe Sorrentino
Viktor Jirsa
author_sort Pierpaolo Sorrentino
collection DOAJ
description Subject differentiation bears the possibility to individualize brain analyses. However, the nature of the processes generating subject-specific features remains unknown. Most of the current literature uses techniques that assume stationarity (e.g., Pearson's correlation), which might fail to capture the non-linear nature of brain activity. We hypothesize that non-linear perturbations (defined as neuronal avalanches in the context of critical dynamics) spread across the brain and carry subject-specific information, contributing the most to differentiability. To test this hypothesis, we compute the avalanche transition matrix (ATM) from source-reconstructed magnetoencephalographic data, as to characterize subject-specific fast dynamics. We perform differentiability analysis based on the ATMs, and compare the performance to that obtained using Pearson's correlation (which assumes stationarity). We demonstrate that selecting the moments and places where neuronal avalanches spread improves differentiation (P < 0.0001, permutation testing), despite the fact that most of the data (i.e., the linear part) are discarded. Our results show that the non-linear part of the brain signals carries most of the subject-specific information, thereby clarifying the nature of the processes that underlie individual differentiation. Borrowing from statistical mechanics, we provide a principled way to link emergent large-scale personalized activations to non-observable, microscopic processes.
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spelling doaj.art-352b1d43ffb94939ba3397f6587266152023-07-05T05:15:36ZengElsevierNeuroImage1095-95722023-08-01277120260Brain fingerprint is based on the aperiodic, scale-free, neuronal activityPierpaolo Sorrentino0Emahnuel Troisi Lopez1Antonella Romano2Carmine Granata3Marie Constance Corsi4Giuseppe Sorrentino5Viktor Jirsa6Institut de Neurosciences des Systèmes, Aix-Marseille Universitè, Marseille, France; Deparment of Biomedical Science, University of Sassari, Sassari, Italy; Institute of Applied Sciences and Intelligent Systems, CNR, Naples, Italy; Correspondence to: Dr. Pierpaolo Sorrentino, Institut de Neurosciences des Systèmes, Aix-Marseille Universitè, 27, Boulevard Jean Moulin, 13005 Marseille, FranceInstitute of Applied Sciences and Intelligent Systems, CNR, Naples, Italy; Department of Motor Sciences and Wellness, University of Naples “Parthenope”, Naples, ItalyDepartment of Motor Sciences and Wellness, University of Naples “Parthenope”, Naples, ItalyInstitute of Applied Sciences and Intelligent Systems, CNR, Naples, ItalySorbonne Université, Institut du Cerveau - Paris Brain Institute - ICM, CNRS, Inria, Inserm, AP-HP, Hôpital de la Pitié Salpêtrière, F-75013, Paris, FranceInstitute of Applied Sciences and Intelligent Systems, CNR, Naples, Italy; Department of Motor Sciences and Wellness, University of Naples “Parthenope”, Naples, Italy; Institute of Diagnosis and Treatment Hermitage Capodimonte, Naples, ItalyInstitut de Neurosciences des Systèmes, Aix-Marseille Universitè, Marseille, FranceSubject differentiation bears the possibility to individualize brain analyses. However, the nature of the processes generating subject-specific features remains unknown. Most of the current literature uses techniques that assume stationarity (e.g., Pearson's correlation), which might fail to capture the non-linear nature of brain activity. We hypothesize that non-linear perturbations (defined as neuronal avalanches in the context of critical dynamics) spread across the brain and carry subject-specific information, contributing the most to differentiability. To test this hypothesis, we compute the avalanche transition matrix (ATM) from source-reconstructed magnetoencephalographic data, as to characterize subject-specific fast dynamics. We perform differentiability analysis based on the ATMs, and compare the performance to that obtained using Pearson's correlation (which assumes stationarity). We demonstrate that selecting the moments and places where neuronal avalanches spread improves differentiation (P < 0.0001, permutation testing), despite the fact that most of the data (i.e., the linear part) are discarded. Our results show that the non-linear part of the brain signals carries most of the subject-specific information, thereby clarifying the nature of the processes that underlie individual differentiation. Borrowing from statistical mechanics, we provide a principled way to link emergent large-scale personalized activations to non-observable, microscopic processes.http://www.sciencedirect.com/science/article/pii/S1053811923004111Neuronal AvalanchesBrain DynamicsBrain DifferentiabilityTransition MatricesMagnetoencephalography
spellingShingle Pierpaolo Sorrentino
Emahnuel Troisi Lopez
Antonella Romano
Carmine Granata
Marie Constance Corsi
Giuseppe Sorrentino
Viktor Jirsa
Brain fingerprint is based on the aperiodic, scale-free, neuronal activity
NeuroImage
Neuronal Avalanches
Brain Dynamics
Brain Differentiability
Transition Matrices
Magnetoencephalography
title Brain fingerprint is based on the aperiodic, scale-free, neuronal activity
title_full Brain fingerprint is based on the aperiodic, scale-free, neuronal activity
title_fullStr Brain fingerprint is based on the aperiodic, scale-free, neuronal activity
title_full_unstemmed Brain fingerprint is based on the aperiodic, scale-free, neuronal activity
title_short Brain fingerprint is based on the aperiodic, scale-free, neuronal activity
title_sort brain fingerprint is based on the aperiodic scale free neuronal activity
topic Neuronal Avalanches
Brain Dynamics
Brain Differentiability
Transition Matrices
Magnetoencephalography
url http://www.sciencedirect.com/science/article/pii/S1053811923004111
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