Abnormal Patterns of Corticomuscular and Intermuscular Coherence in Childhood Dystonia

Overview

Journal Clin Neurophysiol

Publisher Elsevier

Specialties Neurology
Psychiatry

Date 2020 Feb 19

PMID 32067914

Citations 10

Authors

Verity M McClelland

Zoran Cvetkovic

Jean-Pierre Lin

Kerry R Mills

Peter Brown

Affiliations

Soon will be listed here.

Abstract

Objective: Sensorimotor processing is abnormal in Idiopathic/Genetic dystonias, but poorly studied in Acquired dystonias. Beta-Corticomuscular coherence (CMC) quantifies coupling between oscillatory electroencephalogram (EEG) and electromyogram (EMG) activity and is modulated by sensory stimuli. We test the hypothesis that sensory modulation of CMC and intermuscular coherence (IMC) is abnormal in Idiopathic/Genetic and Acquired dystonias.

Methods: Participants: 11 children with Acquired dystonia, 5 with Idiopathic/Genetic dystonia, 13 controls (12-18 years). CMC and IMC were recorded during a grasp task, with mechanical perturbations provided by an electromechanical tapper. Coherence patterns pre- and post-stimulus were compared across groups.

Results: Beta-CMC increased post-stimulus in Controls and Acquired dystonia (p = 0.001 and p = 0.010, respectively), but not in Idiopathic/Genetic dystonia (p = 0.799). The modulation differed between groups, being larger in both Controls and Acquired dystonia compared with Idiopathic/Genetic dystonia (p = 0.003 and p = 0.022). Beta-IMC increased significantly post-stimulus in Controls (p = 0.004), but not in dystonia. Prominent 4-12 Hz IMC was seen in all dystonia patients and correlated with severity (rho = 0.618).

Conclusion: Idiopathic/Genetic and Acquired dystonia share an abnormal low-frequency IMC. In contrast, sensory modulation of beta-CMC differed between the two groups.

Significance: The findings suggest that sensorimotor processing is abnormal in Acquired as well as Idiopathic/Genetic dystonia, but that the nature of the abnormality differs.

Citing Articles

The neuromechanical of Beta-band corticomuscular coupling within the human motor system.

Peng J, Zikereya T, Shao Z, Shi K Front Neurosci. 2024; 18:1441002.

PMID: 39211436 PMC: 11358111. DOI: 10.3389/fnins.2024.1441002.

Cross-frequency cortex-muscle interactions are abnormal in young people with dystonia.

Guo Z, Lin J, Simeone O, Mills K, Cvetkovic Z, McClelland V Brain Commun. 2024; 6(2):fcae061.

PMID: 38487552 PMC: 10939448. DOI: 10.1093/braincomms/fcae061.

Corticomuscular and intermuscular coherence are correlated after stroke: a simplified motor control?.

Delcamp C, Gasq D, Cormier C, Amarantini D Brain Commun. 2023; 5(3):fcad187.

PMID: 37377979 PMC: 10292907. DOI: 10.1093/braincomms/fcad187.

Dystonia in Childhood: How Insights from Paediatric Research Enrich the Network Theory of Dystonia.

McClelland V, Lin J Adv Neurobiol. 2023; 31:1-22.

PMID: 37338693 DOI: 10.1007/978-3-031-26220-3_1.

Metabolic patterns in brain 18F-fluorodeoxyglucose PET relate to aetiology in paediatric dystonia.

Tsagkaris S, Yau E, McClelland V, Papandreou A, Siddiqui A, Lumsden D Brain. 2022; 146(6):2512-2523.

PMID: 36445406 PMC: 10232264. DOI: 10.1093/brain/awac439.

References

Magarinos-Ascone C, Regidor I, Gomez-Galan M, Cabanes-Martinez L, Figueiras-Mendez R . Deep brain stimulation in the globus pallidus to treat dystonia: electrophysiological characteristics and 2 years' follow-up in 10 patients. Neuroscience. 2008; 152(2):558-71. DOI: 10.1016/j.neuroscience.2008.01.001. View

Fritsch C, Timmer J . Effects of attention and precision of exerted force on beta range EEG-EMG synchronization during a maintained motor contraction task. Clin Neurophysiol. 2002; 113(1):124-31. DOI: 10.1016/s1388-2457(01)00722-2. View

Kukke S, de Campos A, Damiano D, Alter K, Patronas N, Hallett M . Cortical activation and inter-hemispheric sensorimotor coherence in individuals with arm dystonia due to childhood stroke. Clin Neurophysiol. 2014; 126(8):1589-98. PMC: 4433430. DOI: 10.1016/j.clinph.2014.11.002. View

Chakarov V, Naranjo J, Schulte-Monting J, Omlor W, Huethe F, Kristeva R . Beta-range EEG-EMG coherence with isometric compensation for increasing modulated low-level forces. J Neurophysiol. 2009; 102(2):1115-20. DOI: 10.1152/jn.91095.2008. View

Koy A, Timmermann L . Deep brain stimulation in cerebral palsy: Challenges and opportunities. Eur J Paediatr Neurol. 2016; 21(1):118-121. DOI: 10.1016/j.ejpn.2016.05.015. View

Tijssen M, Marsden J, Brown P . Frequency analysis of EMG activity in patients with idiopathic torticollis. Brain. 2000; 123 ( Pt 4):677-86. DOI: 10.1093/brain/123.4.677. View

Hallett M . Neurophysiology of dystonia: The role of inhibition. Neurobiol Dis. 2010; 42(2):177-84. PMC: 3016461. DOI: 10.1016/j.nbd.2010.08.025. View

Neumann W, Jha A, Bock A, Huebl J, Horn A, Schneider G . Cortico-pallidal oscillatory connectivity in patients with dystonia. Brain. 2015; 138(Pt 7):1894-906. DOI: 10.1093/brain/awv109. View

Tinazzi M, Priori A, Bertolasi L, Frasson E, Mauguiere F, Fiaschi A . Abnormal central integration of a dual somatosensory input in dystonia. Evidence for sensory overflow. Brain. 1999; 123 ( Pt 1):42-50. DOI: 10.1093/brain/123.1.42. View

10.

Tinazzi M, Rosso T, Fiaschi A . Role of the somatosensory system in primary dystonia. Mov Disord. 2003; 18(6):605-22. DOI: 10.1002/mds.10398. View

11.

Foncke E, Bour L, van der Meer J, Koelman J, Tijssen M . Abnormal low frequency drive in myoclonus-dystonia patients correlates with presence of dystonia. Mov Disord. 2007; 22(9):1299-307. DOI: 10.1002/mds.21519. View

12.

Xu Y, McClelland V, Cvetkovic Z, Mills K . Corticomuscular Coherence With Time Lag With Application to Delay Estimation. IEEE Trans Biomed Eng. 2016; 64(3):588-600. DOI: 10.1109/TBME.2016.2569492. View

13.

Quartarone A, Morgante F, Santangelo A, Rizzo V, Bagnato S, Terranova C . Abnormal plasticity of sensorimotor circuits extends beyond the affected body part in focal dystonia. J Neurol Neurosurg Psychiatry. 2007; 79(9):985-90. DOI: 10.1136/jnnp.2007.121632. View

14.

Ismail F, Fatemi A, Johnston M . Cerebral plasticity: Windows of opportunity in the developing brain. Eur J Paediatr Neurol. 2016; 21(1):23-48. DOI: 10.1016/j.ejpn.2016.07.007. View

15.

Cordivari C, Lees A, Misra V, Brown P . EMG-EMG coherence in writer's cramp. Mov Disord. 2002; 17(5):1011-6. DOI: 10.1002/mds.10212. View

16.

Keenan K, Farina D, Maluf K, Merletti R, Enoka R . Influence of amplitude cancellation on the simulated surface electromyogram. J Appl Physiol (1985). 2004; 98(1):120-31. DOI: 10.1152/japplphysiol.00894.2004. View

17.

Starr P, Rau G, Davis V, Marks Jr W, Ostrem J, Simmons D . Spontaneous pallidal neuronal activity in human dystonia: comparison with Parkinson's disease and normal macaque. J Neurophysiol. 2005; 93(6):3165-76. DOI: 10.1152/jn.00971.2004. View

18.

Conway B, Halliday D, Farmer S, Shahani U, Maas P, Weir A . Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. J Physiol. 1995; 489 ( Pt 3):917-24. PMC: 1156860. DOI: 10.1113/jphysiol.1995.sp021104. View

19.

Doldersum E, van Zijl J, Beudel M, Eggink H, Brandsma R, Pina-Fuentes D . Intermuscular coherence as biomarker for pallidal deep brain stimulation efficacy in dystonia. Clin Neurophysiol. 2019; 130(8):1351-1357. DOI: 10.1016/j.clinph.2019.04.717. View

20.

Farmer S, Sheean G, Mayston M, Rothwell J, Marsden C, Conway B . Abnormal motor unit synchronization of antagonist muscles underlies pathological co-contraction in upper limb dystonia. Brain. 1998; 121 ( Pt 5):801-14. DOI: 10.1093/brain/121.5.801. View