Adaptive functional reorganization in amyotrophic lateral sclerosis: coexisting degenerative and compensatory changes.


Journal

European journal of neurology
ISSN: 1468-1331
Titre abrégé: Eur J Neurol
Pays: England
ID NLM: 9506311

Informations de publication

Date de publication:
01 2020
Historique:
received: 22 03 2019
accepted: 10 07 2019
pubmed: 17 7 2019
medline: 29 12 2020
entrez: 17 7 2019
Statut: ppublish

Résumé

Considerable functional reorganization takes place in amyotrophic lateral sclerosis (ALS) in face of relentless structural degeneration. This study evaluates functional adaptation in ALS patients with lower motor neuron predominant (LMNp) and upper motor neuron predominant (UMNp) dysfunction. Seventeen LMNp ALS patients, 14 UMNp ALS patients and 14 controls participated in a functional magnetic resonance imaging study. Study-group-specific activation patterns were evaluated during preparation for a motor task. Connectivity analyses were carried out using the supplementary motor area (SMA), cerebellum and striatum as seed regions and correlations were explored with clinical measures. Increased cerebellar, decreased dorsolateral prefrontal cortex and decreased SMA activation were detected in UMNp patients compared to controls. Increased cerebellar activation was also detected in UMNp patients compared to LMNp patients. UMNp patients exhibit increased effective connectivity between the cerebellum and caudate, and decreased connectivity between the SMA and caudate and between the SMA and cerebellum when performing self-initiated movement. In UMNp patients, a positive correlation was detected between clinical variables and striato-cerebellar connectivity. Our findings indicate that, despite the dysfunction of SMA-striatal and SMA-cerebellar networks, cerebello-striatal connectivity increases in ALS indicative of compensatory processes. The coexistence of circuits with decreased and increased connectivity suggests concomitant neurodegenerative and adaptive changes in ALS.

Sections du résumé

BACKGROUND AND PURPOSE
Considerable functional reorganization takes place in amyotrophic lateral sclerosis (ALS) in face of relentless structural degeneration. This study evaluates functional adaptation in ALS patients with lower motor neuron predominant (LMNp) and upper motor neuron predominant (UMNp) dysfunction.
METHODS
Seventeen LMNp ALS patients, 14 UMNp ALS patients and 14 controls participated in a functional magnetic resonance imaging study. Study-group-specific activation patterns were evaluated during preparation for a motor task. Connectivity analyses were carried out using the supplementary motor area (SMA), cerebellum and striatum as seed regions and correlations were explored with clinical measures.
RESULTS
Increased cerebellar, decreased dorsolateral prefrontal cortex and decreased SMA activation were detected in UMNp patients compared to controls. Increased cerebellar activation was also detected in UMNp patients compared to LMNp patients. UMNp patients exhibit increased effective connectivity between the cerebellum and caudate, and decreased connectivity between the SMA and caudate and between the SMA and cerebellum when performing self-initiated movement. In UMNp patients, a positive correlation was detected between clinical variables and striato-cerebellar connectivity.
CONCLUSIONS
Our findings indicate that, despite the dysfunction of SMA-striatal and SMA-cerebellar networks, cerebello-striatal connectivity increases in ALS indicative of compensatory processes. The coexistence of circuits with decreased and increased connectivity suggests concomitant neurodegenerative and adaptive changes in ALS.

Identifiants

pubmed: 31310452
doi: 10.1111/ene.14042
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

121-128

Subventions

Organisme : Investissements d'avenir
Pays : International
Organisme : Institut National pour la Santé et la Recherche Médicale (INSERM)
Pays : International
Organisme : Association for Research on ALS (ARSLA)
Pays : International
Organisme : the Association for Research on ALS (ARSLA)
Pays : International

Informations de copyright

© European Academy of Neurology 2019.

Références

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Auteurs

M Abidi (M)

CeRSM Laboratory, Nanterre University, UPL, Paris, France.

G de Marco (G)

CeRSM Laboratory, Nanterre University, UPL, Paris, France.
COMUE Paris Lumières University, Paris, France.

A Couillandre (A)

CeRSM Laboratory, Nanterre University, UPL, Paris, France.
COMUE Paris Lumières University, Paris, France.

M Feron (M)

CeRSM Laboratory, Nanterre University, UPL, Paris, France.

E Mseddi (E)

CeRSM Laboratory, Nanterre University, UPL, Paris, France.

N Termoz (N)

CeRSM Laboratory, Nanterre University, UPL, Paris, France.
COMUE Paris Lumières University, Paris, France.

G Querin (G)

Department of Neurology, Pitié-Salpêtrière Hospital, Paris, France.
Biomedical Imaging Laboratory, Sorbonne University, Paris, France.

P-F Pradat (PF)

Department of Neurology, Pitié-Salpêtrière Hospital, Paris, France.
Biomedical Imaging Laboratory, Sorbonne University, Paris, France.

P Bede (P)

Department of Neurology, Pitié-Salpêtrière Hospital, Paris, France.
Biomedical Imaging Laboratory, Sorbonne University, Paris, France.
Computational Neuroimaging Group, Trinity College Dublin, Dublin, Ireland.

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