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Insights on the Relationship Between Hippocampal Connectivity and Memory Performances at the Early Stage of Multiple Sclerosis

While memory impairment in multiple sclerosis (MS) is known to be associated with hippocampal alterations, whether hippocampal networks could dynamically reorganize as a compensation mechanism is still a matter of debate. In this context, our aim was to identify the patterns of structural and functi...

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Autores principales: Boscheron, Juliette, Ruet, Aurélie, Deloire, Mathilde, Charré-Morin, Julie, Saubusse, Aurore, Brochet, Bruno, Tourdias, Thomas, Koubiyr, Ismail
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8170471/
https://www.ncbi.nlm.nih.gov/pubmed/34093415
http://dx.doi.org/10.3389/fneur.2021.667531
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author Boscheron, Juliette
Ruet, Aurélie
Deloire, Mathilde
Charré-Morin, Julie
Saubusse, Aurore
Brochet, Bruno
Tourdias, Thomas
Koubiyr, Ismail
author_facet Boscheron, Juliette
Ruet, Aurélie
Deloire, Mathilde
Charré-Morin, Julie
Saubusse, Aurore
Brochet, Bruno
Tourdias, Thomas
Koubiyr, Ismail
author_sort Boscheron, Juliette
collection PubMed
description While memory impairment in multiple sclerosis (MS) is known to be associated with hippocampal alterations, whether hippocampal networks could dynamically reorganize as a compensation mechanism is still a matter of debate. In this context, our aim was to identify the patterns of structural and functional connectivity between the hippocampus and the rest of the brain and their possible relevance to memory performances in early MS. Thirty-two patients with a first episode suggestive of MS together with 10 matched healthy controls were prospectively explored at baseline, 1 and 5 years follow up. They were scanned with MRI and underwent a neuropsychological battery of tests that included the Selective Reminding Test and the Brief Visual Memory Test Revised to assess verbal and visuo-spatial memory, respectively. Hippocampal volume was computed together with four graph theory metrics to study the structural and functional connectivity of both hippocampi with the rest of the brain. Associations between network parameters and memory performances were assessed using linear mixed-effects (LME) models. Considering cognitive abilities, verbal memory performances of patients decreased over time while visuo-spatial memory performances were maintained. In parallel, hippocampal volumes decreased significantly while structural and functional connectivity metrics were modified, with an increase in hippocampal connections over time. More precisely, these modifications were indicating a reinforcement of hippocampal short-distance connections. LME models revealed that the drop in verbal memory performances was associated with hippocampal volume loss, while the preservation of visuo-spatial memory performances was linked to decreased hippocampal functional shortest path length. In conclusion, we demonstrated a differential impairment in memory performances in the early stages of MS and an important interplay between hippocampal-related structural and functional networks and those performances. As the structural damage increases, functional reorganization seems to be able to maintain visuo-spatial memory performances with strengthened short-distance connections.
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spelling pubmed-81704712021-06-03 Insights on the Relationship Between Hippocampal Connectivity and Memory Performances at the Early Stage of Multiple Sclerosis Boscheron, Juliette Ruet, Aurélie Deloire, Mathilde Charré-Morin, Julie Saubusse, Aurore Brochet, Bruno Tourdias, Thomas Koubiyr, Ismail Front Neurol Neurology While memory impairment in multiple sclerosis (MS) is known to be associated with hippocampal alterations, whether hippocampal networks could dynamically reorganize as a compensation mechanism is still a matter of debate. In this context, our aim was to identify the patterns of structural and functional connectivity between the hippocampus and the rest of the brain and their possible relevance to memory performances in early MS. Thirty-two patients with a first episode suggestive of MS together with 10 matched healthy controls were prospectively explored at baseline, 1 and 5 years follow up. They were scanned with MRI and underwent a neuropsychological battery of tests that included the Selective Reminding Test and the Brief Visual Memory Test Revised to assess verbal and visuo-spatial memory, respectively. Hippocampal volume was computed together with four graph theory metrics to study the structural and functional connectivity of both hippocampi with the rest of the brain. Associations between network parameters and memory performances were assessed using linear mixed-effects (LME) models. Considering cognitive abilities, verbal memory performances of patients decreased over time while visuo-spatial memory performances were maintained. In parallel, hippocampal volumes decreased significantly while structural and functional connectivity metrics were modified, with an increase in hippocampal connections over time. More precisely, these modifications were indicating a reinforcement of hippocampal short-distance connections. LME models revealed that the drop in verbal memory performances was associated with hippocampal volume loss, while the preservation of visuo-spatial memory performances was linked to decreased hippocampal functional shortest path length. In conclusion, we demonstrated a differential impairment in memory performances in the early stages of MS and an important interplay between hippocampal-related structural and functional networks and those performances. As the structural damage increases, functional reorganization seems to be able to maintain visuo-spatial memory performances with strengthened short-distance connections. Frontiers Media S.A. 2021-05-19 /pmc/articles/PMC8170471/ /pubmed/34093415 http://dx.doi.org/10.3389/fneur.2021.667531 Text en Copyright © 2021 Boscheron, Ruet, Deloire, Charré-Morin, Saubusse, Brochet, Tourdias and Koubiyr. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neurology
Boscheron, Juliette
Ruet, Aurélie
Deloire, Mathilde
Charré-Morin, Julie
Saubusse, Aurore
Brochet, Bruno
Tourdias, Thomas
Koubiyr, Ismail
Insights on the Relationship Between Hippocampal Connectivity and Memory Performances at the Early Stage of Multiple Sclerosis
title Insights on the Relationship Between Hippocampal Connectivity and Memory Performances at the Early Stage of Multiple Sclerosis
title_full Insights on the Relationship Between Hippocampal Connectivity and Memory Performances at the Early Stage of Multiple Sclerosis
title_fullStr Insights on the Relationship Between Hippocampal Connectivity and Memory Performances at the Early Stage of Multiple Sclerosis
title_full_unstemmed Insights on the Relationship Between Hippocampal Connectivity and Memory Performances at the Early Stage of Multiple Sclerosis
title_short Insights on the Relationship Between Hippocampal Connectivity and Memory Performances at the Early Stage of Multiple Sclerosis
title_sort insights on the relationship between hippocampal connectivity and memory performances at the early stage of multiple sclerosis
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8170471/
https://www.ncbi.nlm.nih.gov/pubmed/34093415
http://dx.doi.org/10.3389/fneur.2021.667531
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