Motor imagery in amyotrophic lateral Sclerosis: An fMRI study of postural control

Malek Abidi, Pierre-Francois Pradat, Nicolas Termoz, Annabelle Couillandre, Peter Bede, Giovanni de Marco

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Abstract

Background: The functional reorganization of brain networks sustaining gait is poorly characterized in amyotrophic lateral sclerosis (ALS) despite ample evidence of progressive disconnection between brain regions. The main objective of this fMRI study is to assess gait imagery-specific networks in ALS patients using dynamic causal modeling (DCM) complemented by parametric empirical Bayes (PEB) framework. Method: Seventeen lower motor neuron predominant (LMNp) ALS patients, fourteen upper motor neuron predominant (UMNp) ALS patients and fourteen healthy controls participated in this study. Each subject performed a dual motor imagery task: normal and precision gait. The Movement Imagery Questionnaire (MIQ-rs) and imagery time (IT) were used to evaluate gait imagery in each participant. In a neurobiological computational model, the circuits involved in imagined gait and postural control were investigated by modelling the relationship between normal/precision gait and connection strengths. Results: Behavioral results showed significant increase in IT in UMNp patients compared to healthy controls (P corrected < 0.05) and LMNp (P corrected < 0.05). During precision gait, healthy controls activate the model's circuits involved in the imagined gait and postural control. In UMNp, decreased connectivity (inhibition) from basal ganglia (BG) to supplementary motor area (SMA) and from SMA to posterior parietal cortex (PPC) is observed. Contrary to healthy controls, DCM detects no cerebellar-PPC connectivity in neither UMNp nor LMNp ALS. During precision gait, bilateral connectivity (excitability) between SMA and BG is observed in the LMNp group contrary to UMNp and healthy controls. Conclusions: Our findings demonstrate the utility of implementing both DCM and PEB to characterize connectivity patterns in specific patient phenotypes. Our approach enables the identification of specific circuits involved in postural deficits, and our findings suggest a putative excitatory–inhibitory imbalance. More broadly, our data demonstrate how clinical manifestations are underpinned by network-specific disconnection phenomena in ALS.

Original languageEnglish
Article number103051
Pages (from-to)1-9
Number of pages9
JournalNeuroImage: Clinical
Volume35
Early online date17 May 2022
DOIs
Publication statusPublished online - 17 May 2022

Bibliographical note

Funding Information:
This study was funded by a grant from the Association for Research on ALS (ARSLA) and the Institut National pour la Santé et la Recherche Médicale (INSERM). The research leading to these results has also received support from the programme “Investissements d'avenir” (ANR-10-IAIHU-06). Professor Bede is supported by the Health Research Board, Ireland (HRB EIA-2017-019 and HRB JPND-Cofund2-2019-1), the Spastic Paraplegia Foundation, Inc. (SPF), the EU Joint Programme – Neurodegenerative Disease Research (JPND), and the Iris O'Brien Foundation.

Publisher Copyright:
© 2022 The Author(s)

Keywords

  • Neuroimaging
  • Motor imagery
  • DCM
  • Connectivity
  • fMRI
  • ALS

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