Arterial Spin Labeling Reveals Disrupted Brain Networks and Functional Connectivity in Drug-Resistant Temporal Epilepsy

Resting-state networks (RSNs) and functional connectivity (FC) have been increasingly exploited for mapping brain activity and identifying abnormalities in pathologies, including epilepsy. The majority of studies currently available are based on blood-oxygenation-level-dependent (BOLD) contrast in c...

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Main Authors: Ilaria Boscolo Galazzo, Silvia Francesca Storti, Anna Barnes, Bianca De Blasi, Enrico De Vita, Matthias Koepp, John Sidney Duncan, Ashley Groves, Francesca Benedetta Pizzini, Gloria Menegaz, Francesco Fraioli
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-03-01
Series:Frontiers in Neuroinformatics
Subjects:
ICA
Online Access:https://www.frontiersin.org/article/10.3389/fninf.2018.00101/full
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record_format Article
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language English
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sources DOAJ
author Ilaria Boscolo Galazzo
Silvia Francesca Storti
Anna Barnes
Bianca De Blasi
Enrico De Vita
Matthias Koepp
John Sidney Duncan
Ashley Groves
Francesca Benedetta Pizzini
Gloria Menegaz
Francesco Fraioli
spellingShingle Ilaria Boscolo Galazzo
Silvia Francesca Storti
Anna Barnes
Bianca De Blasi
Enrico De Vita
Matthias Koepp
John Sidney Duncan
Ashley Groves
Francesca Benedetta Pizzini
Gloria Menegaz
Francesco Fraioli
Arterial Spin Labeling Reveals Disrupted Brain Networks and Functional Connectivity in Drug-Resistant Temporal Epilepsy
Frontiers in Neuroinformatics
arterial spin labeling
perfusion
functional connectivity
resting-state
ICA
epilepsy
author_facet Ilaria Boscolo Galazzo
Silvia Francesca Storti
Anna Barnes
Bianca De Blasi
Enrico De Vita
Matthias Koepp
John Sidney Duncan
Ashley Groves
Francesca Benedetta Pizzini
Gloria Menegaz
Francesco Fraioli
author_sort Ilaria Boscolo Galazzo
title Arterial Spin Labeling Reveals Disrupted Brain Networks and Functional Connectivity in Drug-Resistant Temporal Epilepsy
title_short Arterial Spin Labeling Reveals Disrupted Brain Networks and Functional Connectivity in Drug-Resistant Temporal Epilepsy
title_full Arterial Spin Labeling Reveals Disrupted Brain Networks and Functional Connectivity in Drug-Resistant Temporal Epilepsy
title_fullStr Arterial Spin Labeling Reveals Disrupted Brain Networks and Functional Connectivity in Drug-Resistant Temporal Epilepsy
title_full_unstemmed Arterial Spin Labeling Reveals Disrupted Brain Networks and Functional Connectivity in Drug-Resistant Temporal Epilepsy
title_sort arterial spin labeling reveals disrupted brain networks and functional connectivity in drug-resistant temporal epilepsy
publisher Frontiers Media S.A.
series Frontiers in Neuroinformatics
issn 1662-5196
publishDate 2019-03-01
description Resting-state networks (RSNs) and functional connectivity (FC) have been increasingly exploited for mapping brain activity and identifying abnormalities in pathologies, including epilepsy. The majority of studies currently available are based on blood-oxygenation-level-dependent (BOLD) contrast in combination with either independent component analysis (ICA) or pairwise region of interest (ROI) correlations. Despite its success, this approach has several shortcomings as BOLD is only an indirect and non-quantitative measure of brain activity. Conversely, promising results have recently been achieved by arterial spin labeling (ASL) MRI, primarily developed to quantify brain perfusion. However, the wide application of ASL-based FC has been hampered by its complexity and relatively low robustness to noise, leaving several aspects of this approach still largely unexplored. In this study, we firstly aimed at evaluating the effect of noise reduction on spatio-temporal ASL analyses and quantifying the impact of two ad-hoc processing pipelines (basic and advanced) on connectivity measures. Once the optimal strategy had been defined, we investigated the applicability of ASL for connectivity mapping in patients with drug-resistant temporal epilepsy vs. controls (10 per group), aiming at revealing between-group voxel-wise differences in each RSN and ROI-wise FC changes. We first found ASL was able to identify the main network (DMN) along with all the others generally detected with BOLD but never previously reported from ASL. For all RSNs, ICA-based denoising (advanced pipeline) allowed to increase their similarity with the corresponding BOLD template. ASL-based RSNs were visibly consistent with literature findings; however, group differences could be identified in the structure of some networks. Indeed, statistics revealed areas of significant FC decrease in patients within different RSNs, such as DMN and cerebellum (CER), while significant increases were found in some cases, such as the visual networks. Finally, the ROI-based analyses identified several inter-hemispheric dysfunctional links (controls > patients) mainly between areas belonging to the DMN, right-left thalamus and right-left temporal lobe. Conversely, fewer connections, predominantly intra-hemispheric, showed the opposite pattern (controls < patients). All these elements provide novel insights into the pathological modulations characterizing a “network disease” as epilepsy, shading light on the importance of perfusion-based approaches for identifying the disrupted areas and communications between brain regions.
topic arterial spin labeling
perfusion
functional connectivity
resting-state
ICA
epilepsy
url https://www.frontiersin.org/article/10.3389/fninf.2018.00101/full
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spelling doaj-f8d3cf6e484140f89ef7d2cce1e039c52020-11-24T23:32:09ZengFrontiers Media S.A.Frontiers in Neuroinformatics1662-51962019-03-011210.3389/fninf.2018.00101416841Arterial Spin Labeling Reveals Disrupted Brain Networks and Functional Connectivity in Drug-Resistant Temporal EpilepsyIlaria Boscolo Galazzo0Silvia Francesca Storti1Anna Barnes2Bianca De Blasi3Enrico De Vita4Matthias Koepp5John Sidney Duncan6Ashley Groves7Francesca Benedetta Pizzini8Gloria Menegaz9Francesco Fraioli10Department of Computer Science, University of Verona, Verona, ItalyDepartment of Computer Science, University of Verona, Verona, ItalyInstitute of Nuclear Medicine, University College London, London, United KingdomDepartment of Medical Physics, University College London, London, United KingdomDepartment of Biomedical Engineering, School of Biomedical Engineering & Imaging Sciences, King’s Health Partners, King’s College London, London, United KingdomDepartment of Clinical and Experimental Epilepsy, Institute of Neurology, University College London, London, United KingdomDepartment of Clinical and Experimental Epilepsy, Institute of Neurology, University College London, London, United KingdomInstitute of Nuclear Medicine, University College London, London, United KingdomDepartment of Neuroradiology, University Hospital Verona, Verona, ItalyDepartment of Computer Science, University of Verona, Verona, ItalyInstitute of Nuclear Medicine, University College London, London, United KingdomResting-state networks (RSNs) and functional connectivity (FC) have been increasingly exploited for mapping brain activity and identifying abnormalities in pathologies, including epilepsy. The majority of studies currently available are based on blood-oxygenation-level-dependent (BOLD) contrast in combination with either independent component analysis (ICA) or pairwise region of interest (ROI) correlations. Despite its success, this approach has several shortcomings as BOLD is only an indirect and non-quantitative measure of brain activity. Conversely, promising results have recently been achieved by arterial spin labeling (ASL) MRI, primarily developed to quantify brain perfusion. However, the wide application of ASL-based FC has been hampered by its complexity and relatively low robustness to noise, leaving several aspects of this approach still largely unexplored. In this study, we firstly aimed at evaluating the effect of noise reduction on spatio-temporal ASL analyses and quantifying the impact of two ad-hoc processing pipelines (basic and advanced) on connectivity measures. Once the optimal strategy had been defined, we investigated the applicability of ASL for connectivity mapping in patients with drug-resistant temporal epilepsy vs. controls (10 per group), aiming at revealing between-group voxel-wise differences in each RSN and ROI-wise FC changes. We first found ASL was able to identify the main network (DMN) along with all the others generally detected with BOLD but never previously reported from ASL. For all RSNs, ICA-based denoising (advanced pipeline) allowed to increase their similarity with the corresponding BOLD template. ASL-based RSNs were visibly consistent with literature findings; however, group differences could be identified in the structure of some networks. Indeed, statistics revealed areas of significant FC decrease in patients within different RSNs, such as DMN and cerebellum (CER), while significant increases were found in some cases, such as the visual networks. Finally, the ROI-based analyses identified several inter-hemispheric dysfunctional links (controls > patients) mainly between areas belonging to the DMN, right-left thalamus and right-left temporal lobe. Conversely, fewer connections, predominantly intra-hemispheric, showed the opposite pattern (controls < patients). All these elements provide novel insights into the pathological modulations characterizing a “network disease” as epilepsy, shading light on the importance of perfusion-based approaches for identifying the disrupted areas and communications between brain regions.https://www.frontiersin.org/article/10.3389/fninf.2018.00101/fullarterial spin labelingperfusionfunctional connectivityresting-stateICAepilepsy