Cognitive, behavioral, and brain functional connectivity correlates of fatigue in amyotrophic lateral sclerosis

Abstract Introduction Fatigue is defined as a symptom of exhaustion unexplained by drug effects or psychiatric disorders and comprises two main components (i.e., central or “mental” and peripheral or “physical” components), both influencing global disability in amyotrophic lateral sclerosis (ALS). W...

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Main Authors: Francesca Trojsi, Federica Di Nardo, Giulia D'Alvano, Carla Passaniti, Minoo Sharbafshaaer, Fabrizio Canale, Antonio Russo, Marcello Silvestro, Luigi Lavorgna, Mario Cirillo, Fabrizio Esposito, Gioacchino Tedeschi, Mattia Siciliano
Format: Article
Language:English
Published: Wiley 2023-07-01
Series:Brain and Behavior
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Online Access:https://doi.org/10.1002/brb3.2931
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author Francesca Trojsi
Federica Di Nardo
Giulia D'Alvano
Carla Passaniti
Minoo Sharbafshaaer
Fabrizio Canale
Antonio Russo
Marcello Silvestro
Luigi Lavorgna
Mario Cirillo
Fabrizio Esposito
Gioacchino Tedeschi
Mattia Siciliano
author_facet Francesca Trojsi
Federica Di Nardo
Giulia D'Alvano
Carla Passaniti
Minoo Sharbafshaaer
Fabrizio Canale
Antonio Russo
Marcello Silvestro
Luigi Lavorgna
Mario Cirillo
Fabrizio Esposito
Gioacchino Tedeschi
Mattia Siciliano
author_sort Francesca Trojsi
collection DOAJ
description Abstract Introduction Fatigue is defined as a symptom of exhaustion unexplained by drug effects or psychiatric disorders and comprises two main components (i.e., central or “mental” and peripheral or “physical” components), both influencing global disability in amyotrophic lateral sclerosis (ALS). We aim at investigating the clinical correlations between “physical” and “mental” components of fatigue, measured by the Multidimensional Fatigue Inventory scale, and motor and cognitive/behavioral disability in a large sample of patients with ALS. We also investigated the correlations between these measures of fatigue and resting‐state functional connectivity of brain functional magnetic resonance imaging (RS‐fMRI) large‐scale networks in a subset of patients. Methods One hundred and thirty ALS patients were assessed for motor disability, cognitive and behavioral dysfunctions, fatigue, anxiety, apathy, and daytime sleepiness. Moreover, the collected clinical parameters were correlated with RS‐fMRI functional connectivity changes in the large‐scale brain networks of 30 ALS patients who underwent MRI. Results Multivariate correlation analysis revealed that “physical” fatigue was related to anxiety and respiratory dysfunction, while “mental” fatigue was related to memory impairment and apathy. Moreover, the mental fatigue score was directly related to functional connectivity in the right and left insula (within the salience network), and inversely related to functional connectivity in the left middle temporal gyrus (within the default mode network). Conclusions Although the “physical” component of fatigue may be influenced by the disease itself, in ALS the “mental” component of fatigue correlates with cognitive and behavioral impairment, as well as with alterations of functional connectivity in extra‐motor networks.
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spelling doaj.art-c2a7839081af4a578e13927503b85c482023-07-13T04:43:15ZengWileyBrain and Behavior2162-32792023-07-01137n/an/a10.1002/brb3.2931Cognitive, behavioral, and brain functional connectivity correlates of fatigue in amyotrophic lateral sclerosisFrancesca Trojsi0Federica Di Nardo1Giulia D'Alvano2Carla Passaniti3Minoo Sharbafshaaer4Fabrizio Canale5Antonio Russo6Marcello Silvestro7Luigi Lavorgna8Mario Cirillo9Fabrizio Esposito10Gioacchino Tedeschi11Mattia Siciliano12Department of Advanced Medical and Surgical Sciences, MRI Research Center Università degli Studi della Campania “Luigi Vanvitelli” Naples ItalyDepartment of Advanced Medical and Surgical Sciences, MRI Research Center Università degli Studi della Campania “Luigi Vanvitelli” Naples ItalyDepartment of Advanced Medical and Surgical Sciences, MRI Research Center Università degli Studi della Campania “Luigi Vanvitelli” Naples ItalyDepartment of Advanced Medical and Surgical Sciences, MRI Research Center Università degli Studi della Campania “Luigi Vanvitelli” Naples ItalyDepartment of Advanced Medical and Surgical Sciences, MRI Research Center Università degli Studi della Campania “Luigi Vanvitelli” Naples ItalyDepartment of Advanced Medical and Surgical Sciences, MRI Research Center Università degli Studi della Campania “Luigi Vanvitelli” Naples ItalyDepartment of Advanced Medical and Surgical Sciences, MRI Research Center Università degli Studi della Campania “Luigi Vanvitelli” Naples ItalyDepartment of Advanced Medical and Surgical Sciences, MRI Research Center Università degli Studi della Campania “Luigi Vanvitelli” Naples ItalyFirst Division of Neurology University Hospital Università degli studi della Campania “Luigi Vanvitelli” Naples ItalyDepartment of Advanced Medical and Surgical Sciences, MRI Research Center Università degli Studi della Campania “Luigi Vanvitelli” Naples ItalyDepartment of Advanced Medical and Surgical Sciences, MRI Research Center Università degli Studi della Campania “Luigi Vanvitelli” Naples ItalyDepartment of Advanced Medical and Surgical Sciences, MRI Research Center Università degli Studi della Campania “Luigi Vanvitelli” Naples ItalyDepartment of Advanced Medical and Surgical Sciences, MRI Research Center Università degli Studi della Campania “Luigi Vanvitelli” Naples ItalyAbstract Introduction Fatigue is defined as a symptom of exhaustion unexplained by drug effects or psychiatric disorders and comprises two main components (i.e., central or “mental” and peripheral or “physical” components), both influencing global disability in amyotrophic lateral sclerosis (ALS). We aim at investigating the clinical correlations between “physical” and “mental” components of fatigue, measured by the Multidimensional Fatigue Inventory scale, and motor and cognitive/behavioral disability in a large sample of patients with ALS. We also investigated the correlations between these measures of fatigue and resting‐state functional connectivity of brain functional magnetic resonance imaging (RS‐fMRI) large‐scale networks in a subset of patients. Methods One hundred and thirty ALS patients were assessed for motor disability, cognitive and behavioral dysfunctions, fatigue, anxiety, apathy, and daytime sleepiness. Moreover, the collected clinical parameters were correlated with RS‐fMRI functional connectivity changes in the large‐scale brain networks of 30 ALS patients who underwent MRI. Results Multivariate correlation analysis revealed that “physical” fatigue was related to anxiety and respiratory dysfunction, while “mental” fatigue was related to memory impairment and apathy. Moreover, the mental fatigue score was directly related to functional connectivity in the right and left insula (within the salience network), and inversely related to functional connectivity in the left middle temporal gyrus (within the default mode network). Conclusions Although the “physical” component of fatigue may be influenced by the disease itself, in ALS the “mental” component of fatigue correlates with cognitive and behavioral impairment, as well as with alterations of functional connectivity in extra‐motor networks.https://doi.org/10.1002/brb3.2931amyotrophic lateral sclerosisfatiguefunctional connectivityresting‐state functional MRI
spellingShingle Francesca Trojsi
Federica Di Nardo
Giulia D'Alvano
Carla Passaniti
Minoo Sharbafshaaer
Fabrizio Canale
Antonio Russo
Marcello Silvestro
Luigi Lavorgna
Mario Cirillo
Fabrizio Esposito
Gioacchino Tedeschi
Mattia Siciliano
Cognitive, behavioral, and brain functional connectivity correlates of fatigue in amyotrophic lateral sclerosis
Brain and Behavior
amyotrophic lateral sclerosis
fatigue
functional connectivity
resting‐state functional MRI
title Cognitive, behavioral, and brain functional connectivity correlates of fatigue in amyotrophic lateral sclerosis
title_full Cognitive, behavioral, and brain functional connectivity correlates of fatigue in amyotrophic lateral sclerosis
title_fullStr Cognitive, behavioral, and brain functional connectivity correlates of fatigue in amyotrophic lateral sclerosis
title_full_unstemmed Cognitive, behavioral, and brain functional connectivity correlates of fatigue in amyotrophic lateral sclerosis
title_short Cognitive, behavioral, and brain functional connectivity correlates of fatigue in amyotrophic lateral sclerosis
title_sort cognitive behavioral and brain functional connectivity correlates of fatigue in amyotrophic lateral sclerosis
topic amyotrophic lateral sclerosis
fatigue
functional connectivity
resting‐state functional MRI
url https://doi.org/10.1002/brb3.2931
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