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Measurement error and reliability of TMS metrics collected from biceps and triceps in individuals with chronic incomplete tetraplegia

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Abstract

Transcranial magnetic stimulation (TMS) is used to investigate corticomotor neurophysiology associated with functional recovery in individuals with spinal cord injury (SCI). There is insufficient evidence about test–retest measurement properties of TMS in SCI. Therefore, we investigated test–retest agreement and reliability of TMS metrics representing corticomotor excitability, output, gain, map (representation), and inhibition in individuals with cervical SCI. We collected TMS metrics from biceps and triceps muscles because of the relevance of this proximal muscle pair to the cervical SCI population. Twelve individuals with chronic C3–C6 SCI participated in two TMS sessions separated by ≥ 2 weeks. Measurement agreement was evaluated using t tests, Bland–Altman limits of agreement and relative standard error of measurement (SEM%), while reliability was investigated using intra-class correlation coefficient (ICC) and concordance correlation coefficient (CCC). We calculated the smallest detectable change for all TMS metrics. All TMS metrics except antero-posterior map coordinates and corticomotor inhibition were in agreement upon repeated measurement though limits of agreement were generally large. Measures of corticomotor excitability, output and medio-lateral map coordinates had superior agreement (SEM% < 10). Metrics representing corticomotor excitability, output, and inhibition had good-to-excellent reliability (ICC/CCC > 0.75). The smallest detectable change for TMS metrics was generally high for a single individual, but this value reduced substantially with increase in sample size. We recommend use of corticomotor excitability and recruitment curve area owing to their superior measurement properties. A modest group size (20 or above) yields more stable measurements, which may favor use of TMS metrics in group level modulation after SCI.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Anderson KD (2004) Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma 21:1371–1383. https://doi.org/10.1089/neu.2004.21.1371

    Article  PubMed  Google Scholar 

  • Beaulieu L-D, Flamand VH, Masse-Alarie H, Schneider C (2017) Reliability and minimal detectable change of transcranial magnetic stimulation outcomes in healthy adults: a systematic review. Brain Stimul 10:196–213

    Article  Google Scholar 

  • Berchtold A (2016) Test–retest: agreement or reliability? Methodol Innov 9:2059799116672875

    Google Scholar 

  • Brasil-Neto JP, McShane LM, Fuhr P et al (1992) Topographic mapping of the human motor cortex with magnetic stimulation: factors affecting accuracy and reproducibility. Electroencephalogr Clin Neurophysiol Potentials Sect 85:9–16

    Article  CAS  Google Scholar 

  • Brouwer B, Hopkins-Rosseel DH (1997) Motor cortical mapping of proximal upper extremity muscles following spinal cord injury. Spinal Cord 35:205–212

    Article  CAS  Google Scholar 

  • Carson RG, Nelson BD, Buick AR et al (2013) Characterizing changes in the excitability of corticospinal projections to proximal muscles of the upper limb. Brain Stimul 6:760–768

    Article  Google Scholar 

  • Chen R, Lozano AM, Ashby P (1999) Mechanism of the silent period following transcranial magnetic stimulation evidence from epidural recordings. Exp Brain Res 128:539–542

    Article  CAS  Google Scholar 

  • Cunningham DA, Janini D, Wyant A et al (2016) Post-exercise depression following submaximal and maximal isometric voluntary contraction. Neuroscience 326:95–104

    Article  CAS  Google Scholar 

  • de Vet HCW, Terwee CB, Knol DL, Bouter LM (2006) When to use agreement versus reliability measures. J Clin Epidemiol 59:1033–1039

    Article  Google Scholar 

  • Devanne H, Lavoie BA, Capaday C (1997) Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329–338

    Article  CAS  Google Scholar 

  • Edwards DJ, Cortes M, Rykman-Peltz A et al (2019) Clinical improvement with intensive robot-assisted arm training in chronic stroke is unchanged by supplementary tDCS. Restor Neurol 37:167–180

    Google Scholar 

  • Freund P, Rothwell J, Craggs M et al (2011) Corticomotor representation to a human forearm muscle changes following cervical spinal cord injury. Eur J Neurosci 34:1839–1846

    Article  Google Scholar 

  • Fuhr P, Agostino R, Hallett M (1991) Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 81:257–262

    Article  CAS  Google Scholar 

  • Gomes-Osman J, Field-Fote EC (2015a) Improvements in hand function in adults with chronic tetraplegia following a multi-day 10Hz rTMS intervention combined with repetitive task practice. J Neurol Phys Ther 39:23

    Article  Google Scholar 

  • Gomes-Osman J, Field-Fote EC (2015b) Cortical vs. afferent stimulation as an adjunct to functional task practice training: a randomized, comparative pilot study in people with cervical spinal cord injury. Clin Rehabil 29:771–782

    Article  Google Scholar 

  • Graves DE, Frankiewicz RG, Donovan WH (2006) Construct validity and dimensional structure of the ASIA motor scale. J Spinal Cord Med 29:39–45

    Article  Google Scholar 

  • Green JB, Sora E, Bialy Y et al (1999) Cortical motor reorganization after paraplegia: an EEG study. J Neurol 53:736

    CAS  Google Scholar 

  • Groppa S, Oliviero A, Eisen A et al (2012) A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol 123:858–882

    Article  CAS  Google Scholar 

  • Hoffman LR, Field-Fote EC (2007) Cortical reorganization following bimanual training and somatosensory stimulation in cervical spinal cord injury: a case report. Phys Ther 87:208–223

    Article  Google Scholar 

  • Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15:155–163

    Article  Google Scholar 

  • Leao MTD, Wiesinger L, Ziemann U et al (2020) Rapid motor cortical reorganization following subacute spinal cord dysfunction. Brain Stimul 13:783–785

    Article  Google Scholar 

  • Levy WJ Jr, Amassian VE, Traad M, Cadwell J (1990) Focal magnetic coil stimulation reveals motor cortical system reorganized in humans after traumatic quadriplegia. Brain Res 510:130–134

    Article  Google Scholar 

  • Malcolm MP, Triggs WJ, Light KE et al (2006) Reliability of motor cortex transcranial magnetic stimulation in four muscle representations. Clin Neurophysiol 117:1037–1046

    Article  CAS  Google Scholar 

  • Marino RJ, Jones L, Kirshblum S et al (2008) Reliability and repeatability of the motor and sensory examination of the international standards for neurological classification of spinal cord injury. J Spinal Cord Med 31:166–170

    Article  Google Scholar 

  • Mokkink LB, Terwee CB, Patrick DL et al (2010) The COSMIN study reached international consensus on taxonomy, terminology, and definitions of measurement properties for health-related patient-reported outcomes. J Clin Epidemiol 63:737–745

    Article  Google Scholar 

  • Oudega M, Perez MA (2012) Corticospinal reorganization after spinal cord injury. J Physiol 590:3647–3663

    Article  CAS  Google Scholar 

  • Palmer E, Ashby P (1992) Corticospinal projections to upper limb motoneurones in humans. J Physiol 448:397–412

    Article  CAS  Google Scholar 

  • Potter-Baker KA, Janini DP, Frost FS et al (2016) Reliability of TMS metrics in patients with chronic incomplete spinal cord injury. Spinal Cord 54:980

    Article  CAS  Google Scholar 

  • Rossi S, Hallett M, Rossini PM et al (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120:2008–2039

    Article  Google Scholar 

  • Rossini PM, Burke D, Chen R et al (2015) 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 IFCN Committee. Clin Neurophysiol 126:1071–1107

    Article  CAS  Google Scholar 

  • Sankarasubramanian V, Roelle SM, Bonnett CE et al (2015) Reproducibility of transcranial magnetic stimulation metrics in the study of proximal upper limb muscles. J Electromyogr 25:754–764

    Article  Google Scholar 

  • Schambra HM, Ogden RT, Martínez-Hernández I et al (2015) The reliability of repeated TMS measures in older adults and in patients with subacute and chronic stroke. Front Cell Neurosci 9:335

    Article  Google Scholar 

  • Smith HC, Savic G, Frankel HL et al (2000) Corticospinal function studied over time following incomplete spinal cord injury. Spinal Cord 38:292–300

    Article  CAS  Google Scholar 

  • Streletz LJ, Belevich JKS, Jones SM et al (1995) Transcranial magnetic stimulation: cortical motor maps in acute spinal cord injury. Brain Topogr 7:245–250

    Article  CAS  Google Scholar 

  • van Kuijk AA, Pasman JW, Hendricks HT et al (2009) Predicting hand motor recovery in severe stroke: the role of motor evoked potentials in relation to early clinical assessment. NeuroRehabilitation 23:45–51

    Google Scholar 

  • Van Kuijk AAA, Bakker CD, Hendriks JCM et al (2014) Definition dependent properties of the cortical silent period in upper-extremity muscles, a methodological study. J Neuroeng Rehabil 11:1–9

    Article  Google Scholar 

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Acknowledgements

We thank Yin-Liang Lin for assistance with data collection, Daniel Janini for the initial analysis, and Patrick Chabra, Corin Bonnett, and Sarah Roelle for the recruitment efforts. We also thank all research participants for their valuable time and efforts.

Funding

The U.S. Army Medical Research Acquisition Activity, 820 Chandler Street, Fort Detrick MD 21702-5014 is the awarding and administering acquisition office. This work was supported by the USAMRAA through the Spinal Cord Injury Research Programs under Award Nos. W81XWH1810530 and W81XWH1110707 to EP. Opinions, interpretations, conclusions and recommendations are those of the author and are not necessarily endorsed by the Department of Defense or U.S. Army). This work was also supported by Conquer Paralysis Now grant (CPN1512) to EP and Cleveland Clinic Research Programs Committee award (2016-195) to KPB.

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Authors and Affiliations

  1. Plow Lab (ND 20), Department of Biomedical Engineering, Lerner Research Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, ND20, Cleveland, OH, 44195, USA

    Tarun Arora, Kyle O’Laughlin & Ela B. Plow

  2. Department of Molecular Science, School of Medicine, The University of Texas Rio Grande Valley, Edinburg, TX, USA

    Kelsey Potter-Baker

  3. Department of Quantitative Health Sciences, Cleveland Clinic Foundation, Cleveland, OH, USA

    Manshi Li & Xiaofeng Wang

  4. MetroHealth Center for Rehabilitation Research, Cleveland, OH, USA

    David Cunningham

  5. Department of Physical Medicine and Rehabilitaiton, Case Western Reserve University, Cleveland, OH, USA

    David Cunningham

  6. Cleveland Functional Electrical Stimulation Center, Cleveland, OH, USA

    David Cunningham

  7. Department of Physical Medicine and Rehabilitation, Cleveland Clinic Foundation, Cleveland, USA

    Francois Bethoux, Frederick Frost & Ela B. Plow

Authors
  1. Tarun Arora
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  2. Kelsey Potter-Baker
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  3. Kyle O’Laughlin
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  4. Manshi Li
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  5. Xiaofeng Wang
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  6. David Cunningham
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  7. Francois Bethoux
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  8. Frederick Frost
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  9. Ela B. Plow
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Corresponding author

Correspondence to Ela B. Plow.

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On behalf of all the authors, the corresponding author states that there is no conflict of interest.

Ethical approval

The study was approved by the Institutional Review Board of the Cleveland Clinic and the Human Research Protections Office of the U.S. Department of Defense.

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All the participants provided written informed consent.

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Communicated by Winston D Byblow.

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Arora, T., Potter-Baker, K., O’Laughlin, K. et al. Measurement error and reliability of TMS metrics collected from biceps and triceps in individuals with chronic incomplete tetraplegia. Exp Brain Res 239, 3077–3089 (2021). https://doi.org/10.1007/s00221-021-06160-2

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  • DOI: https://doi.org/10.1007/s00221-021-06160-2

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