Mirror Movements in Multiple Sclerosis -a Clinical, Electrophysiological, and Imaging Study

Overview

Journal BMC Neurol

Publisher Biomed Central

Specialty Neurology

Date 2024 Sep 6

PMID 39242510

Authors

Korbinian Holzapfel

Antonios Bayas

Markus Naumann

Tanupriya Ghosh

Verena Steuerwald

Martin Allweyer

Jan S Kirschke

Lars Behrens

Affiliations

Soon will be listed here.

Abstract

Background: Mirror movements (MM) are commonly caused by a defect of interhemispheric pathways also affected in multiple sclerosis (MS), particularly the corpus callosum. We investigated the prevalence of MM in MS in relation to functional and morphological callosal fiber integrity by transcranial magnetic stimulation (TMS), magnetic resonance imaging (MRI), as well as fatigue.

Methods: In 21 patients with relapsing-remitting MS and 19 healthy controls, MM were assessed and graded (Woods and Teuber scale: MM 1-4) using a bedside test. Fatigue was evaluated using the Fatigue Scale for Motor and Cognitive Functions (FSMC) questionnaire. TMS measured ipsilateral silent period latency and duration. MRI assessed callosal atrophy by measuring the normalized corpus callosum area (nCCA), corpus callosum index (CCI), and lesion volume.

Results: MS patients had significantly more often and pronounced MM compared to healthy controls (p = 0.0002) and nCCA was significantly lower (p = 0.045) in MRI studies. Patients with higher MM scores (MM > 1 vs. MM 0/1) showed significantly more fatigue (higher FSMC sum score, p = 0.04, motor score, p = 0.01). In TMS and MRI studies, no significant differences were found between patients with MM 0/1 and those with MM > 1 (ipsilateral silent period measurements, CCA, CCI and lesion volume).

Conclusions: MM are common in MS and can easily be detected through bedside testing. As MM are associated with fatigue, they might indicate fatigue in MS. It is possible that other cerebral structures, in addition to the corpus callosum, may contribute to the origin of MM in MS.

References

Tartaglia M, Narayanan S, Francis S, Santos A, De Stefano N, Lapierre Y . The relationship between diffuse axonal damage and fatigue in multiple sclerosis. Arch Neurol. 2004; 61(2):201-7. DOI: 10.1001/archneur.61.2.201. View

Magne V, Adde L, Hoare B, Klingels K, Simon-Martinez C, Mailleux L . Assessment of mirror movements in children and adolescents with unilateral cerebral palsy: reliability of the Woods and Teuber scale. Dev Med Child Neurol. 2021; 63(6):736-742. DOI: 10.1111/dmcn.14806. View

Penner I, Raselli C, Stocklin M, Opwis K, Kappos L, Calabrese P . The Fatigue Scale for Motor and Cognitive Functions (FSMC): validation of a new instrument to assess multiple sclerosis-related fatigue. Mult Scler. 2009; 15(12):1509-17. DOI: 10.1177/1352458509348519. View

Liu P, Yuan Y, Zhang N, Liu X, Yu L, Luo B . Mirror Movements in Acquired Neurological Disorders: A Mini-Review. Front Neurol. 2021; 12:736115. PMC: 8488104. DOI: 10.3389/fneur.2021.736115. View

Thompson A, Banwell B, Barkhof F, Carroll W, Coetzee T, Comi G . Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol. 2017; 17(2):162-173. DOI: 10.1016/S1474-4422(17)30470-2. View

Tartaglia M, Narayanan S, Arnold D . Mental fatigue alters the pattern and increases the volume of cerebral activation required for a motor task in multiple sclerosis patients with fatigue. Eur J Neurol. 2008; 15(4):413-9. DOI: 10.1111/j.1468-1331.2008.02090.x. View

Kurtzke J . Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983; 33(11):1444-52. DOI: 10.1212/wnl.33.11.1444. View

Braley T, Chervin R . Fatigue in multiple sclerosis: mechanisms, evaluation, and treatment. Sleep. 2010; 33(8):1061-7. PMC: 2910465. DOI: 10.1093/sleep/33.8.1061. View

Wittenberg G, Bastian A, Dromerick A, Thach W, Powers W . Mirror movements complicate interpretation of cerebral activation changes during recovery from subcortical infarction. Neurorehabil Neural Repair. 2001; 14(3):213-21. DOI: 10.1177/154596830001400307. View

10.

Woods B, TEUBER H . Mirror movements after childhood hemiparesis. Neurology. 1978; 28(11):1152-7. DOI: 10.1212/wnl.28.11.1152. View

11.

Poisson A, Ballanger B, Metereau E, Redoute J, Ibarolla D, Comte J . A functional magnetic resonance imaging study of pathophysiological changes responsible for mirror movements in Parkinson's disease. PLoS One. 2013; 8(6):e66910. PMC: 3692538. DOI: 10.1371/journal.pone.0066910. View

12.

Jung P, Beyerle A, Humpich M, Neumann-Haefelin T, Lanfermann H, Ziemann U . Ipsilateral silent period: a marker of callosal conduction abnormality in early relapsing-remitting multiple sclerosis?. J Neurol Sci. 2006; 250(1-2):133-9. DOI: 10.1016/j.jns.2006.08.008. View

13.

Tellez N, Alonso J, Rio J, Tintore M, Nos C, Montalban X . The basal ganglia: a substrate for fatigue in multiple sclerosis. Neuroradiology. 2007; 50(1):17-23. DOI: 10.1007/s00234-007-0304-3. View

14.

Wittstock M, Wilde N, Grossmann A, Kasper E, Teipel S . Mirror Movements in Amyotrophic Lateral Sclerosis: A Combined Study Using Diffusion Tensor Imaging and Transcranial Magnetic Stimulation. Front Neurol. 2020; 11:164. PMC: 7067896. DOI: 10.3389/fneur.2020.00164. View

15.

Nelles G, Cramer S, Schaechter J, Kaplan J, Finklestein S . Quantitative assessment of mirror movements after stroke. Stroke. 1998; 29(6):1182-7. DOI: 10.1161/01.str.29.6.1182. View

16.

Wittstock M, Meister S, Walter U, Benecke R, Wolters A . Mirror movements in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2011; 12(6):393-7. DOI: 10.3109/17482968.2011.577223. View

17.

Tataroglu C, Genc A, Idiman E, Cakmur R, Idiman F . Cortical silent period and motor evoked potentials in patients with multiple sclerosis. Clin Neurol Neurosurg. 2003; 105(2):105-10. DOI: 10.1016/s0303-8467(02)00127-0. View

18.

Yaldizli O, Penner I, Frontzek K, Naegelin Y, Amann M, Papadopoulou A . The relationship between total and regional corpus callosum atrophy, cognitive impairment and fatigue in multiple sclerosis patients. Mult Scler. 2013; 20(3):356-64. DOI: 10.1177/1352458513496880. View

19.

Pongratz V, Bussas M, Schmidt P, Grahl S, Gasperi C, El Husseini M . Lesion location across diagnostic regions in multiple sclerosis. Neuroimage Clin. 2023; 37:103311. PMC: 9850035. DOI: 10.1016/j.nicl.2022.103311. View

20.

Tisseyre J, Cremoux S, Amarantini D, Tallet J . Increased intensity of unintended mirror muscle contractions after cervical spinal cord injury is associated with changes in interhemispheric and corticomuscular coherences. Behav Brain Res. 2021; 417:113563. DOI: 10.1016/j.bbr.2021.113563. View