Navigated TMS mapping using the grid-based algorithm to evaluate the reorganization of cortical muscle representation in amyotrophic lateral sclerosis

Cover Page

Abstract

Introduction. Motor cortex mapping using navigated transcranial magnetic stimulation (TMS) is a promising method for assessing motor cortex reorganization in amyotrophic lateral sclerosis (ALS). The use of the grid-based algorithm allows the mapping protocol to be standardized and can help to reduce the variability of the assessed parameters.

Study aim — to analyse the reorganization features of the cortical representations of hand muscles in patients with classical ALS using navigated TMS mapping with a grid-based algorithm.

Materials and methods. The study included 14 patients with classical ALS and 9 healthy volunteers. Navigated TMS mapping of the cortical representations of the right abductor pollicis brevis (APB) muscle was performed using a predetermined grid (7×7 square cells) centred around a ‘hot spot’. Five stimuli with an intensity of 110% of the individual resting motor threshold (RMT) were randomly applied to each cell. The RMT and area of cortical representation of the APB muscle were analysed, amplitude or probability weighted.

Results. Patients with ALS showed a statistically significant decrease in the weighted amplitude of the area of cortical representations of the APB muscle compared with healthy volunteers. The RMT, area and weighted probability area of the cortical representations of the APB muscle did not differ significantly between the groups. A statistically significant correlation between RMT and severity of dysfunction and upper motor neuron damage was found in patients with ALS, based on the clinical data. There were no statistically significant correlations between cortical representation parameters and the clinical symptoms in patients with ALS.

Conclusion. Navigated TMS mapping of the motor cortex with a grid-based algorithm in patients with ALS revealed a decrease in the weighted amplitude of the cortical representation area of the APB muscle. It is important to clarify the role of navigated TMS mapping with the proposed algorithm in the diagnosis, prognosis and monitoring of ALS.

About the authors

Ilya S. Bakulin

Research Center of Neurology, Moscow

Author for correspondence.
Email: platonova@neurology.ru
Russian Federation

Dmitry O. Sinitsyn

Research Center of Neurology, Moscow

Email: platonova@neurology.ru
Russian Federation

Alexandra G. Poydasheva

Research Center of Neurology, Moscow

Email: platonova@neurology.ru
Russian Federation

Andrey Yu. Chernyavskiy

K.A. Valiev Institute of Physics and Technology of the Russian Academy of Sciences, Moscow

Email: platonova@neurology.ru
Russian Federation

Natalia A. Suponeva

Research Center of Neurology, Moscow

Email: platonova@neurology.ru
Russian Federation

Maria N. Zakharova

Research Center of Neurology, Moscow

Email: platonova@neurology.ru
Russian Federation

Mikhail A. Piradov

Research Center of Neurology, Moscow

Email: platonova@neurology.ru
Russian Federation

References

  1. Phillips C.G., Porter R. Corticospinal Neurones: Their Role in Movement. N.Y., 1977.
  2. Porter R., Lemon R. Corticospinal Function and Voluntary Movement. Oxford, 1993.
  3. Schieber M.H. Constraints on somatotopic organization in the primary motor cortex. J Neurophysiol 2001; 86: 2125–2143. doi: 10.1152/jn.2001.86.5.2125. PMID: 11698506.
  4. Rossini P.M., Burke D., Chen R. et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: Basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 2015; 126: 1071–1107. doi: 10.1016/j.clinph.2015.02.001. PMID: 25797650.
  5. Poydasheva A.G., Bakulin I.S., Chernyavskiy A.Yu. et al. [Motor cortex mapping with navigated transcranial magnetic stimulation and its clinical application]. Meditsinskiy alfavit 2017; 2(22): 21–25. (In Russ.)
  6. Krieg S.M., Lioumis P., Mäkelä J.P. et al. Protocol for motor and language mapping by navigated TMS in patients and healthy volunteers; workshop report. Acta Neurochir (Wien) 2017; 159: 1187–1195. doi: 10.1007/s00701-017-3187-z. PMID: 28456870.
  7. Weiss C., Nettekoven C., Rehme A.K. et al. Mapping the hand, foot and face representations in the primary motor cortex — retest reliability of neuronavigated TMS versus functional MRI. Neuroimage 2013; 66: 531–542. doi: 10.1016/j.neuroimage.2012.10.046. PMID: 23116812.
  8. Lüdemann-Podubecká J., Nowak D.A. Mapping cortical hand motor representation using TMS: A method to assess brain plasticity and a surrogate marker for recovery of function after stroke? Neurosci Biobehav Rev 2016; 69: 239–251. doi: 10.1016/j.neubiorev.2016.07.006. PMID: 27435238.
  9. Chervyakov A.V., Piradov M.A., Savitskaya N.G. et al. [New step to a personalized medicine. Navigation transcranial magnetic stimulation (NBS eXimia Nexstim)]. Annals of clinical and experimental neurology 2012; 6(3): 37–46. doi: 10.18454/ACEN.2017.2.11. (In Russ.)
  10. Ruohonen J., Karhu J. Navigated transcranial magnetic stimulation. Neurophysiol Clin 2010; 40: 7–17. doi: 10.1016/j.neucli.2010.01.006. PMID: 20230931.
  11. Tarapore P.E., Tate M.C., Findlay A.M. et al. Preoperative multimodal motor mapping: a comparison of magnetoencephalography imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation. J Neurosurg 2012; 117: 354–362. doi: 10.3171/2012.5.JNS112124. PMID: 22702484.
  12. Wittenberg G.F. Motor mapping in cerebral palsy. Dev Med Child Neurol 2009; 51 (Suppl 4): 134–139. doi: 10.1111/j.1469-8749.2009.03426.x. PMID: 19740221.
  13. Quartarone A. Transcranial magnetic stimulation in dystonia. Handb Clin Neurol 2013; 116: 543–553. doi: 10.1016/B978-0-444-53497-2.00043-7.PMID: 24112922.
  14. Barz A., Noack A., Baumgarten P. et al. Motor cortex reorganization in patients with glioma assessed by repeated navigated transcranial magnetic stimulation — a longitudinal study. World Neurosurg 2018; 112: e442–e453. doi: 10.1016/j.wneu.2018.01.059. PMID: 29360588.
  15. Labyt E., Houdayer E., Cassim F. et al. Motor representation areas in epileptic patients with focal motor seizures: a TMS study. Epilepsy Res 2007; 75(2–3):197–205. doi: 10.1016/j.eplepsyres.2007.06.004. PMID: 17628428.
  16. Bakulin I.S., Poydasheva A.G., Chernyavskiy A.Yu. et al. [Methods of detecting lesions of upper motor neuron in amyotrophic lateral sclerosis using transcranial magnetic stimulation]. Annals of clinical and experimental neurology 2018; 12(2): 45–54.doi: 10.25692/ACEN.2018.2.7. (In Russ.)
  17. Bakulin I.S., Chervyakov A.V., Suponeva N.A. et al. Motor cortex hyperexcitability, neuroplasticity and degeneration in amyotrophic lateral sclerosis. In:H. Foyaca-Sibat (ed.) Novel Aspects of Amyotrophic Lateral Sclerosis. Rijeka, 2016: 47–72.
  18. de Carvalho M., Miranda P.C., Luís M.L. et al. Cortical muscle representation in amyotrophic lateral sclerosis patients: changes with disease evolution. Muscle Nerve 1999; 22: 1684–1692. PMID: 10567081.
  19. Chervyakov A.V., Bakulin I.S., Savitskaya N.G. et al. Navigated transcranial magnetic stimulation in amyotrophic lateral sclerosis. Muscle Nerve 2015; 51: 125–131. doi: 10.1002/mus.24345. PMID: 25049055.
  20. Cavaleri R., Schabrun S.M., Chipchase L.S. The number of stimuli required to reliably assess corticomotor excitability and primary motorcortical representations using transcranial magnetic stimulation (TMS): a systematic reviewand meta-analysis. Syst Rev 2017; 6: 48. doi: 10.1186/s13643-017-0440-8. PMID: 28264713.
  21. Pellegrini M., Zoghi M., Jaberzadeh S. The effect of transcranial magnetic stimulation test intensity on the amplitude, variability and reliability of motor evoked potentials. Brain Res 2018; 1700: 190–198. doi: 10.1016/j.brainres.2018.09.002. PMID: 30194017.
  22. Kraus D., Gharabaghi A. Neuromuscular Plasticity: Disentangling Stable and Variable Motor Maps in the Human Sensorimotor Cortex. Neural Plast 2016; 2016: 7365609. doi: 10.1155/2016/7365609. PMID: 2761024.
  23. Chervyakov A.V., Sinitsyn D.O., Piradov M.A. Variability of neuronal responses: types and functional significance in neuroplasticity and neural darwinism. Front Hum Neurosci 2016; 10: 603. PMID: 27932969.
  24. Brooks B.R., Miller R.G., Swash M. et al. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 2000; 1; 293–239. PMID: 11464847.
  25. Cedarbaum J.M., Stambler N., Malta E. et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci 1999; 169: 13–21. PMID: 10540002.
  26. Florence J.M., Pandya S., King W.M. et al. Clinical trials in Duchenne dystrophy. Standardization and reliability of evaluation procedures. Phys Ther 1984; 64: 41–45. PMID: 6361809.
  27. Turner M.R., Cagnin A., Turkheimer F.E. et al. Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)-PK11195 positron emission tomography study. Neurobiol Dis 2004; 15: 601–609. PMID: 15056468.
  28. Khondkarian O.A., Bunina T.L., Zavalishin I.A. [Lateral amyotrophic sclerosis]. Moscow, 1978. (In Russ.)
  29. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971; 9: 97–113. PMID: 5146491.
  30. Huynh W., Simon N.G., Grosskreutz J. et al. Assessment of the upper motor neuron in amyotrophic lateral sclerosis. Clin Neurophysiol 2016; 127: 2643–2660. doi: 10.1016/j.clinph.2016.04.025. PMID: 27291884.
  31. Vucic S., Ziemann U., Eisen A. et al. Transcranial magnetic stimulation and amyotrophic lateral sclerosis: pathophysiological insights J Neurol Neurosurg Psychiatry 2013; 84: 1161–1170. doi: 10.1136/jnnp-2012-304019. PMID: 23264687.
  32. Geevasinga N., Menon P., Özdinler P.H. et al. Pathophysiological and diagnostic implications of cortical dysfunction in ALS. Nat Rev Neurol 2016; 12:651–661. doi: 10.1038/nrneurol.2016.140. PMID: 27658852.
  33. Huynh W., Dharmadasa T., Vucic S., Kiernan M.C. Functional biomarkers for amyotrophic lateral sclerosis. Front Neurol 2019; 9: 1141. doi: 10.3389/fneur.2018.01141. PMID: 30662429.
  34. Eisen A., Pant B., Stewart H. Cortical excitability in amyotrophic lateral sclerosis: a clue to pathogenesis. Can J Neurol Sci 1993; 20: 11–16. PMID: 8096792.
  35. Mills K.R., Nithi K.A. Corticomotor threshold is reduced in early sporadic amyotrophic lateral sclerosis. Muscle Nerve 1997; 20: 1137–1141. PMID: 9270669.
  36. Oliveri M., Brighina F., La Bua V. et al. Reorganization of cortical motor area in prior polio patients. Clin Neurophysiol 1999; 110: 806–812. PMID: 10400193.
  37. Matamala J.M., Geevasinga N., Huynh W. et al. Cortical function and corticomotoneuronal adaptation in monomelic amyotrophy. Clin Neurophysiol 2017; 128: 1488–1495. doi: 10.1016/j.clinph.2017.05.005. PMID: 28624492.
  38. Farrar M.A., Vucic S., Johnston H.M., Kiernan M.C. Corticomotoneuronal integrity and adaptation in spinal muscular atrophy. Arch Neurol 2012; 69: 467–473. doi: 10.1001/archneurol.2011.1697. PMID: 22491191.

Statistics

Views

Abstract: 684

PDF (Russian): 493

Article Metrics

Metrics Loading ...

Dimensions

PlumX


Copyright (c) 2019 Bakulin I.S., Sinitsyn D.O., Poydasheva A.G., Chernyavskiy A.Y., Suponeva N.A., Zakharova M.N., Piradov M.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies