Intracortical inhibiton assessment using threshold tracking technique in amyotrophic lateral sclerosis
- Authors: Bakulin I.S.1, Zabirova A.K.1, Poydasheva A.G.1, Sinitsyn D.O.1, Lagoda D.Y.1, Nagieva A.R.1, Zakharova M.N.1, Suponeva N.A.1, Piradov M.A.1
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Affiliations:
- Research Center of Neurology
- Issue: Vol 14, No 4 (2024)
- Pages: 12-20
- Section: ORIGINAL REPORTS
- Published: 09.01.2025
- URL: https://nmb.abvpress.ru/jour/article/view/631
- DOI: https://doi.org/10.17650/2222-8721-2024-14-4-12-20
- ID: 631
Cite item
Full Text
Abstract
Background. Assessment of short-interval intracortical inhibition (SICI) using paired-pulse transcranial magnetic stimulation (TMS) and the threshold tracking technique is a promising approach to develop biomarkers of motor cortex damage in amyotrophic lateral sclerosis (ALS). Both high sensitivity and specificity of this approach were shown previously; however, almost all studies in this field were conducted by one group of authors.
Aim. The replication of data showing impairment of SICI assessed by threshold tracking technique in patients with ALS.
Materials and methods. 18 patients with ALS and 13 healthy volunteers were included into the study. Functional state of the patients was assessed as well as disease duration, form, stage and progression rate. Following values were determined in all participants using TMS: 1) resting motor threshold (MT); 2) mean motor evoked potential (MEP) amplitude of 30 stimuli applied with an intensity of 120 % MT; 3) SICI assessed using an algorithm based on paralleled optimized threshold tracking with interstimulus interval (ISI) of 1.0 ms, 1.5 ms, 2.0 ms, 2.5 ms, 3.0 ms, 3.5 ms, 4.0 ms, 5.0 ms, 7.0 ms, as well as mean inhibition for values with ISI from 1.0 to 3.0 ms and from 1.0 to 7.0 ms.
Results. No significant differences between groups were observed for MT and MEP amplitude. Significant decrease of SICI with ISI 1.0 and 2.0 ms as well as mean SICI from 1.0 and 3.0 ms was observed in ALS. No significant correlations of MT, MEP amplitude or SICI with clinical values were found.
Conclusion. This replication study has shown the ability of paired-pulse TMS with threshold tracking technique to identify the impairment of intracortical inhibition in patients with ALS.
About the authors
I. S. Bakulin
Research Center of Neurology
Author for correspondence.
Email: bakulin@neurology.ru
ORCID iD: 0000-0003-0716-3737
Ilya Sergeevich Bakulin
80 Volokolamskoe Shosse, Моscow 125367
Russian FederationA. Kh. Zabirova
Research Center of Neurology
Email: fake@neicon.ru
ORCID iD: 0000-0001-8544-3107
80 Volokolamskoe Shosse, Моscow 125367
Russian FederationA. G. Poydasheva
Research Center of Neurology
Email: fake@neicon.ru
ORCID iD: 0000-0003-1841-1177
80 Volokolamskoe Shosse, Моscow 125367
Russian FederationD. O. Sinitsyn
Research Center of Neurology
Email: fake@neicon.ru
ORCID iD: 0000-0001-9951-9803
80 Volokolamskoe Shosse, Моscow 125367
Russian FederationD. Yu. Lagoda
Research Center of Neurology
Email: fake@neicon.ru
ORCID iD: 0000-0002-9267-8315
80 Volokolamskoe Shosse, Моscow 125367
Russian FederationA. R. Nagieva
Research Center of Neurology
Email: fake@neicon.ru
ORCID iD: 0009-0000-3653-2736
80 Volokolamskoe Shosse, Моscow 125367
Russian FederationM. N. Zakharova
Research Center of Neurology
Email: fake@neicon.ru
ORCID iD: 0000-0002-1072-9968
80 Volokolamskoe Shosse, Моscow 125367
Russian FederationN. A. Suponeva
Research Center of Neurology
Email: fake@neicon.ru
ORCID iD: 0000-0003-3956-6362
80 Volokolamskoe Shosse, Моscow 125367
Russian FederationM. A. Piradov
Research Center of Neurology
Email: fake@neicon.ru
ORCID iD: 0000-0002-6338-0392
80 Volokolamskoe Shosse, Моscow 125367
Russian FederationReferences
- Feldman E.L., Goutman S.A., Petri S. et al. Amyotrophic lateral sclerosis. Lancet 2022;400(10360):1363–80. doi: 10.1016/S0140-6736(22)01272-7
- Corcia P., Lunetta C., Vourch P. et al. Time for optimism in amyotrophic lateral sclerosis. Eur J Neurol 2023;30(5):1459–64. doi: 10.1111/ene.15738
- Saini A., Chawla P.A. Breaking barriers with tofersen: Enhancing therapeutic opportunities in amyotrophic lateral sclerosis. Eur J Neurol 2024;31(2):e16140. doi: 10.1111/ene.16140
- 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(5):293–9. doi: 10.1080/146608200300079536
- Shefner J.M., Al-Chalabi A., Baker M.R. et al. A proposal for new diagnostic criteria for ALS. Clin Neurophysiol 2020;131(8):1975–8. doi: 10.1016/j.clinph.2020.04.005
- Bakulin I.S., Zakroyshchikova I.V., Suponeva N.A., Zakharova M.N. Amyotrophic lateral sclerosis: Clinical heterogeneity and approaches to classification. Nervno-myshechnye bolezni = Neuromuscular Diseases 2017;7(3):10–20. (In Russ.). doi: 10.17650/2222-8721-2017-7-3-10-20
- Pinto W.B.V.R., Debona R., Nunes P.P. et al. Atypical motor neuron disease variants: Still a diagnostic challenge in Neurology. Rev Neurol (Paris) 2019;175(4):221–32. doi: 10.1016/j.neurol.2018.04.016
- Kraemer M., Buerger M., Berlit P. Diagnostic problems and delay of diagnosis in amyotrophic lateral sclerosis. Clin Neurol Neurosurg 2010;112(2):103–5. doi: 10.1016/j.clineuro.2009.10.014
- Gwathmey K.G., Corcia P., McDermott C.J. et al. Diagnostic delay in amyotrophic lateral sclerosis. Eur J Neurol 2023;30(9):2595– 601. doi: 10.1111/ene.15874 10. Timmins H.C., Vucic S., Kiernan M.C. Cortical hyperexcitability in amyotrophic lateral sclerosis: From pathogenesis to diagnosis. Curr Opin Neurol 2023;36(4):353–9. doi: 10.1097/WCO.0000000000001162
- Vucic S., Stanley Chen K.H., Kiernan M.C. et al. Clinical diagnostic utility of transcranial magnetic stimulation in neurological disorders. Updated report of an IFCN committee. Clin Neurophysiol 2023;150:131–75. doi: 10.1016/j.clinph.2023.03.010
- Vucic S., de Carvalho M., Bashford J., Alix J.J.P. Contribution of neurophysiology to the diagnosis and monitoring of ALS. Int Rev Neurobiol 2024;176:87–118. doi: 10.1016/bs.irn.2024.04.001
- Crabé R., Aimond F., Gosset P. et al. How degeneration of cells surrounding motoneurons contributes to amyotrophic lateral sclerosis. Cells 2020;9(12):2550. doi: 10.3390/cells9122550
- Vucic S., van den Bos M., Menon P. et al. Utility of threshold tracking transcranial magnetic stimulation in ALS. Clin Neurophysiol Pract 2018;3:164–72. doi: 10.1016/j.cnp.2018.10.002
- Vucic S., Cheah B.C., Yiannikas C., Kiernan M.C. Cortical excitability distinguishes ALS from mimic disorders. Clin Neurophysiol 2011;122(9):1860–6. doi: 10.1016/j.clinph.2010.12.062
- Menon P., Geevasinga N., Yiannikas C. et al. Sensitivity and specificity of threshold tracking transcranial magnetic stimulation for diagnosis of amyotrophic lateral sclerosis: A prospective study. Lancet Neurol 2015;14(5):478–84. doi: 10.1016/S1474-4422(15)00014-9 17. Geevasinga N., Menon P., Yiannikas C. et al. Diagnostic utility of cortical excitability studies in amyotrophic lateral sclerosis. Eur J Neurol 2014;21(12):1451–7. doi: 10.1111/ene.12422
- Geevasinga N., Howells J., Menon P. et al. Amyotrophic lateral sclerosis diagnostic index: Toward a personalized diagnosis of ALS. Neurology 2019;92(6):e536–47. doi: 10.1212/WNL.0000000000006876
- Tankisi H., Nielsen C.S., Howells J. et al. Early diagnosis of amyotrophic lateral sclerosis by threshold tracking and conventional transcranial magnetic stimulation. Eur J Neurol 2021;28(9):3030–9. doi: 10.1111/ene.15010
- Bakulin I.S., Zabirova A.H., Poydasheva A.G. et al. Reliability of intracortical inhibiton measured using threshold tracking technique. Nervno-myshechnye bolezni = Neuromuscular Diseases 2023;13(4):10–9. (In Russ.). doi: 10.17650/2222-8721-2023-13-4-10-19
- Roche J.C., Rojas-Garcia R., Scott K.M. et al. A proposed staging system for amyotrophic lateral sclerosis. Brain 2012;135(Pt 3):847–52. doi: 10.1093/brain/awr351
- Groppa S., Oliviero A., Eisen A. et al. A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol 2012;123(5):858–82. doi: 10.1016/j.clinph.2012.01.010
- Higashihara M., Pavey N., Menon P. et al. Reduction in short interval intracortical inhibition from the early stage reflects the pathophysiology in amyotrophic lateral sclerosis: A meta-analysis study. Eur J Neurol 2024;31(7):e16281. doi: 10.1111/ene.16281
- Nielsen C.S., Samusyte G., Pugdahl K. et al. Test-retest reliability of short-interval intracortical inhibition assessed by thresholdtracking and automated conventional techniques. eNeuro 2021;8(5):ENEURO.0103-21.2021. doi: 10.1523/ENEURO.0103-21.2021
- Tankisi H., Cengiz B., Howells J. et al. Short-interval intracortical inhibition as a function of inter-stimulus interval: Three methods compared. Brain Stimul 2021;14(1):22–32. doi: 10.1016/j.brs.2020.11.002
- Samusyte G., Bostock H., Rothwell J., Koltzenburg M. Shortinterval intracortical inhibition: Comparison between conventional and threshold-tracking techniques. Brain Stimul 2018;11(4):806–17. doi: 10.1016/j.brs.2018.03.002
- McMackin R., Tadjine Y., Fasano A. et al. Examining short interval intracortical inhibition with different transcranial magnetic stimulation-induced current directions in ALS. Clin Neurophysiol Pract 2024;9:120–9. doi: 10.1016/j.cnp.2024.03.001
- Tankisi H., Pia H., Strunge K. et al. Three different short-interval intracortical inhibition methods in early diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener 2023;24(1-2):139–47. doi: 10.1080/21678421.2022.2101926
- Menon P., Higashihara M., van den Bos M. et al. Cortical hyperexcitability evolves with disease progression in ALS. Ann Clin Transl Neurol 2020;7(5):733–41. doi: 10.1002/acn3.51039
- Shibuya K., Park S.B., Geevasinga N. et al. Threshold tracking transcranial magnetic stimulation: Effects of age and gender on motor cortical function. Clin Neurophysiol 2016;127(6):2355–61. doi: 10.1016/j.clinph.2016.03.009
- Peinemann A., Lehner C., Conrad B., Siebner H.R. Age-related decrease in paired-pulse intracortical inhibition in the human primary motor cortex. Neurosci Lett 2001;313(1–2):33–6. doi: 10.1016/s0304-3940(01)02239-x
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