Evidence for genetically determined degeneration of proprioceptive tracts in Friedreich ataxia

Brice Marty, Gilles Naeije*, Mathieu Bourguignon, Vincent Wens, Veikko Jousmäki, David R. Lynch, William Gaetz, Serge Goldman, Riitta Hari, Massimo Pandolfo, Xavier De Tiège

*Corresponding author for this work

Research output: Contribution to journalArticleResearchpeer-review

3 Citations (Scopus)

Abstract

ObjectiveTo assess with magnetoencephalography the developmental vs progressive character of the impairment of spinocortical proprioceptive pathways in Friedreich ataxia (FRDA).MethodsNeuromagnetic signals were recorded from 16 right-handed patients with FRDA (9 female patients, mean age 27 years, mean Scale for the Assessment and Rating Of ataxia [SARA] score 22.25) and matched healthy controls while they performed right finger movements either actively or passively. The coupling between movement kinematics (i.e., acceleration) and neuromagnetic signals was assessed by the use of coherence at sensor and source levels. Such coupling, that is, the corticokinematic coherence (CKC), specifically indexes proprioceptive afferent inputs to the contralateral primary sensorimotor (cSM1) cortex. Nonparametric permutations and Spearman rank correlation test were used for statistics.ResultsIn both groups of participants and movement conditions, significant coupling peaked at the cSM1 cortex. Coherence levels were 70% to 75% lower in patients with FRDA than in healthy controls in both movement conditions. In patients with FRDA, coherence levels correlated with genotype alteration (i.e., the size of GAA1 triplet expansion) and the age at symptom onset but not with disease duration or SARA score.ConclusionThis study provides electrophysiologic evidence demonstrating that proprioceptive impairment in FRDA is mostly genetically determined and scarcely progressive after symptom onset. It also positions CKC as a reliable, robust, specific marker of proprioceptive impairment in FRDA.

Original languageEnglish
Pages (from-to)E116-E124
JournalNeurology
Volume93
Issue number2
Early online date13 Jun 2019
DOIs
Publication statusPublished - 9 Jul 2019
Externally publishedYes

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Friedreich Ataxia
Ataxia
Magnetoencephalography
Patient Rights
Age of Onset
Biomechanical Phenomena
Fingers
Genotype

Cite this

Marty, B., Naeije, G., Bourguignon, M., Wens, V., Jousmäki, V., Lynch, D. R., ... De Tiège, X. (2019). Evidence for genetically determined degeneration of proprioceptive tracts in Friedreich ataxia. Neurology, 93(2), E116-E124. https://doi.org/10.1212/WNL.0000000000007750
Marty, Brice ; Naeije, Gilles ; Bourguignon, Mathieu ; Wens, Vincent ; Jousmäki, Veikko ; Lynch, David R. ; Gaetz, William ; Goldman, Serge ; Hari, Riitta ; Pandolfo, Massimo ; De Tiège, Xavier. / Evidence for genetically determined degeneration of proprioceptive tracts in Friedreich ataxia. In: Neurology. 2019 ; Vol. 93, No. 2. pp. E116-E124.
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abstract = "ObjectiveTo assess with magnetoencephalography the developmental vs progressive character of the impairment of spinocortical proprioceptive pathways in Friedreich ataxia (FRDA).MethodsNeuromagnetic signals were recorded from 16 right-handed patients with FRDA (9 female patients, mean age 27 years, mean Scale for the Assessment and Rating Of ataxia [SARA] score 22.25) and matched healthy controls while they performed right finger movements either actively or passively. The coupling between movement kinematics (i.e., acceleration) and neuromagnetic signals was assessed by the use of coherence at sensor and source levels. Such coupling, that is, the corticokinematic coherence (CKC), specifically indexes proprioceptive afferent inputs to the contralateral primary sensorimotor (cSM1) cortex. Nonparametric permutations and Spearman rank correlation test were used for statistics.ResultsIn both groups of participants and movement conditions, significant coupling peaked at the cSM1 cortex. Coherence levels were 70{\%} to 75{\%} lower in patients with FRDA than in healthy controls in both movement conditions. In patients with FRDA, coherence levels correlated with genotype alteration (i.e., the size of GAA1 triplet expansion) and the age at symptom onset but not with disease duration or SARA score.ConclusionThis study provides electrophysiologic evidence demonstrating that proprioceptive impairment in FRDA is mostly genetically determined and scarcely progressive after symptom onset. It also positions CKC as a reliable, robust, specific marker of proprioceptive impairment in FRDA.",
author = "Brice Marty and Gilles Naeije and Mathieu Bourguignon and Vincent Wens and Veikko Jousm{\"a}ki and Lynch, {David R.} and William Gaetz and Serge Goldman and Riitta Hari and Massimo Pandolfo and {De Ti{\`e}ge}, Xavier",
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Marty, B, Naeije, G, Bourguignon, M, Wens, V, Jousmäki, V, Lynch, DR, Gaetz, W, Goldman, S, Hari, R, Pandolfo, M & De Tiège, X 2019, 'Evidence for genetically determined degeneration of proprioceptive tracts in Friedreich ataxia', Neurology, vol. 93, no. 2, pp. E116-E124. https://doi.org/10.1212/WNL.0000000000007750

Evidence for genetically determined degeneration of proprioceptive tracts in Friedreich ataxia. / Marty, Brice; Naeije, Gilles; Bourguignon, Mathieu; Wens, Vincent; Jousmäki, Veikko; Lynch, David R.; Gaetz, William; Goldman, Serge; Hari, Riitta; Pandolfo, Massimo; De Tiège, Xavier.

In: Neurology, Vol. 93, No. 2, 09.07.2019, p. E116-E124.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - Evidence for genetically determined degeneration of proprioceptive tracts in Friedreich ataxia

AU - Marty, Brice

AU - Naeije, Gilles

AU - Bourguignon, Mathieu

AU - Wens, Vincent

AU - Jousmäki, Veikko

AU - Lynch, David R.

AU - Gaetz, William

AU - Goldman, Serge

AU - Hari, Riitta

AU - Pandolfo, Massimo

AU - De Tiège, Xavier

PY - 2019/7/9

Y1 - 2019/7/9

N2 - ObjectiveTo assess with magnetoencephalography the developmental vs progressive character of the impairment of spinocortical proprioceptive pathways in Friedreich ataxia (FRDA).MethodsNeuromagnetic signals were recorded from 16 right-handed patients with FRDA (9 female patients, mean age 27 years, mean Scale for the Assessment and Rating Of ataxia [SARA] score 22.25) and matched healthy controls while they performed right finger movements either actively or passively. The coupling between movement kinematics (i.e., acceleration) and neuromagnetic signals was assessed by the use of coherence at sensor and source levels. Such coupling, that is, the corticokinematic coherence (CKC), specifically indexes proprioceptive afferent inputs to the contralateral primary sensorimotor (cSM1) cortex. Nonparametric permutations and Spearman rank correlation test were used for statistics.ResultsIn both groups of participants and movement conditions, significant coupling peaked at the cSM1 cortex. Coherence levels were 70% to 75% lower in patients with FRDA than in healthy controls in both movement conditions. In patients with FRDA, coherence levels correlated with genotype alteration (i.e., the size of GAA1 triplet expansion) and the age at symptom onset but not with disease duration or SARA score.ConclusionThis study provides electrophysiologic evidence demonstrating that proprioceptive impairment in FRDA is mostly genetically determined and scarcely progressive after symptom onset. It also positions CKC as a reliable, robust, specific marker of proprioceptive impairment in FRDA.

AB - ObjectiveTo assess with magnetoencephalography the developmental vs progressive character of the impairment of spinocortical proprioceptive pathways in Friedreich ataxia (FRDA).MethodsNeuromagnetic signals were recorded from 16 right-handed patients with FRDA (9 female patients, mean age 27 years, mean Scale for the Assessment and Rating Of ataxia [SARA] score 22.25) and matched healthy controls while they performed right finger movements either actively or passively. The coupling between movement kinematics (i.e., acceleration) and neuromagnetic signals was assessed by the use of coherence at sensor and source levels. Such coupling, that is, the corticokinematic coherence (CKC), specifically indexes proprioceptive afferent inputs to the contralateral primary sensorimotor (cSM1) cortex. Nonparametric permutations and Spearman rank correlation test were used for statistics.ResultsIn both groups of participants and movement conditions, significant coupling peaked at the cSM1 cortex. Coherence levels were 70% to 75% lower in patients with FRDA than in healthy controls in both movement conditions. In patients with FRDA, coherence levels correlated with genotype alteration (i.e., the size of GAA1 triplet expansion) and the age at symptom onset but not with disease duration or SARA score.ConclusionThis study provides electrophysiologic evidence demonstrating that proprioceptive impairment in FRDA is mostly genetically determined and scarcely progressive after symptom onset. It also positions CKC as a reliable, robust, specific marker of proprioceptive impairment in FRDA.

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