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

doi:10.1016/j.nicl.2022.103051

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

Neuroimage Clin. 2022:35:103051. doi: 10.1016/j.nicl.2022.103051. Epub 2022 May 17.

Authors

Malek Abidi¹, Pierre-Francois Pradat², Nicolas Termoz¹, Annabelle Couillandre³, Peter Bede⁴, Giovanni de Marco⁵

Affiliations

¹ LINP2 Laboratory, UPL, Paris Nanterre University, France; COMUE Paris Lumières University, France.
² Department of Neurology, Pitié-Salpêtrière University Hospital, Paris, France; Biomedical Imaging Laboratory, Sorbonne University, CNRS, INSERM, Paris, France; Biomedical Sciences Research Institute, Northern Ireland Centre for Stratified Medicine, Ulster University, Londonderry, UK.
³ LINP2 Laboratory, UPL, Paris Nanterre University, France; Université Paris-Saclay,CIAMS, Orsay, France.
⁴ Department of Neurology, Pitié-Salpêtrière University Hospital, Paris, France; Biomedical Imaging Laboratory, Sorbonne University, CNRS, INSERM, Paris, France; Computational Neuroimaging Group, Trinity College Dublin, Ireland.
⁵ LINP2 Laboratory, UPL, Paris Nanterre University, France; COMUE Paris Lumières University, France. Electronic address: demarco.giovanni@gmail.com.

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.

Keywords: ALS; Connectivity; DCM; Motor imagery; Neuroimaging; fMRI.

Publication types

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

MeSH terms

Amyotrophic Lateral Sclerosis* / diagnostic imaging
Bayes Theorem
Humans
Magnetic Resonance Imaging / methods
Motor Cortex*
Postural Balance