Intersession reliability of fast motor mapping using TMS

The organization of the primary motor cortex (M1) can be non-invasively assessed using transcranial magnetic stimulation (TMS) combined with frameless neuro-navigation. By delivering single pulses of TMS over M1 and recording the motor evoked potentials (MEP) from target muscles, the location and size of muscle representations can be obtained to create a “motor map” [[1]Sollmann N. Krieg S.M. Säisänen L. Julkunen P. Mapping of motor function with neuronavigated transcranial magnetic stimulation: a review on clinical application in brain tumors and methods for ensuring feasible accuracy.Brain Sci. 2021; 11: 897https://doi.org/10.3390/brainsci11070897Crossref PubMed Scopus (27) Google Scholar]. Characteristics such as area, volume, and center of gravity (CoG) are quantified from motor maps. Motor mapping typically requires upwards of 30 minutes to complete which reduces its utility in time-sensitive contexts. An alternative approach is called ‘fast motor maps’ which involve TMS pulses delivered pseudo-randomly over a pre-defined grid centered on the motor hotspot of the target muscle and require ∼5 minutes to acquire [[2]van de Ruit M. Perenboom M.J.L. Grey M.J. TMS brain mapping in less than two minutes.Brain Stimul. 2015; 8: 231-239https://doi.org/10.1016/j.brs.2014.10.020Abstract Full Text Full Text PDF PubMed Scopus (76) Google Scholar]. An important consideration in motor mapping is to ensure maps are reliable within and across days. Relative reliability refers to the extent to which groups and individuals are distinguishable from one another. Absolute reliability is the measurement error that occurs from repeat testing of an individual [[3]Schambra H.M. Ogden R.T. Martínez-Hernández I.E. Lin X. Chang Y.B. Rahman A. et al.The reliability of repeated TMS measures in older adults and in patients with subacute and chronic stroke.Front Cell Neurosci. 2015; 9https://doi.org/10.3389/fncel.2015.00335Crossref PubMed Scopus (90) Google Scholar]. Previous research has examined relative reliability within a session and reported moderate to excellent within-session relative reliability for CoG and map area [[2]van de Ruit M. Perenboom M.J.L. Grey M.J. TMS brain mapping in less than two minutes.Brain Stimul. 2015; 8: 231-239https://doi.org/10.1016/j.brs.2014.10.020Abstract Full Text Full Text PDF PubMed Scopus (76) Google Scholar]. Absolute reliability was examined between consecutive days and exhibited low measurement error [[4]Jonker Z.D. van der Vliet R. Hauwert C.M. Gaiser C. Tulen J.H.M. van der Geest J.N. et al.TMS motor mapping: comparing the absolute reliability of digital reconstruction methods to the golden standard.Brain Stimul. 2019; 12: 309-313https://doi.org/10.1016/j.brs.2018.11.005Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar]. Importantly, the relative and absolute reliability of fast motor maps has not been explored across weeks which is relevant to studies designed to explore interventions that require multiple sessions such as in recovery following stroke and experimental neuroplasticity. The goal of the present study was to determine the intersession relative and absolute reliability of fast motor maps acquired over a minimum of one week. This study aims to increase our understanding of fast motor map reliability to further employ this technique in the exploration of motor cortical organization in basic and clinical neuroscience. In this study, thirty-two right-handed males (age = 24 ± 3 years) completed two sessions separated by 18 ± 11 days. The research was approved by Hamilton Integrated Research Ethics Board and conforms to the declaration of Helsinki. Surface EMG (9 mm Ag–AgCl electrodes) of the right first dorsal interossei (FDI) muscle was band-pass filtered (20 Hz–2.5 kHz), amplified 1000× (Intronix, Canada), digitized at 5 kHz and acquired using Signal v6.02 (Cambridge Electronics Design, UK). TMS was delivered with a figure-of-eight branding coil (50 mm diameter) connected to a Magstim Bistim stimulator (Magstim, UK). For all measures, the coil was oriented at a 45° angle in the posterior-to-anterior (P-A) direction, and Brainsight Neuronavigation was used (Rogue Research, Canada). Fast motor maps were created using 80 TMS pulses delivered at 120 % resting motor threshold (RMT, MTAT) with an inter-stimulus interval of 2s to pseudo-random locations within a 6 × 6 cm area centered over FDI hotspot to create a stimulus distribution density of 2–3 stimuli per cm2. The TMS coil was held and moved by an experienced researcher (SDF). Maps were generated using MATLAB by pairing the stimulus locations with the respective MEP amplitude as performed elsewhere [[2]van de Ruit M. Perenboom M.J.L. Grey M.J. TMS brain mapping in less than two minutes.Brain Stimul. 2015; 8: 231-239https://doi.org/10.1016/j.brs.2014.10.020Abstract Full Text Full Text PDF PubMed Scopus (76) Google Scholar] (supplementary material, Fig. 1). Extreme outliers were removed using Grubb's Test. Normality was assessed by Shapiro Wilk's test. Heteroscedasticity used the R2 value obtained from Bland-Altman plots [[3]Schambra H.M. Ogden R.T. Martínez-Hernández I.E. Lin X. Chang Y.B. Rahman A. et al.The reliability of repeated TMS measures in older adults and in patients with subacute and chronic stroke.Front Cell Neurosci. 2015; 9https://doi.org/10.3389/fncel.2015.00335Crossref PubMed Scopus (90) Google Scholar]. Relative reliability was evaluated using that intraclass correlation coefficient (ICC). Specifically, a 2-way random effects model (2,k) was employed for the calculation of ICC, since all participants were tested by the same experimenter. Similar to previous research, ICC values with 95 % confidence intervals >0.9 were labeled as excellent, 0.75–0.9 as high, 0.5–0.75 as moderate, and <0.5 as poor [[5]Turco C.V. Pesevski A. McNicholas P.D. Beaulieu L.-D. Nelson A.J. Reliability of transcranial magnetic stimulation measures of afferent inhibition.Brain Res. 2019; 1723146394https://doi.org/10.1016/j.brainres.2019.146394Crossref PubMed Scopus (16) Google Scholar] Absolute reliability was assessed using standard error of measurement (SEMeas.). SEMeas% was calculated as [(SEMeas/μ) × 100] and a value < 10 % reflects low measurement error [[3]Schambra H.M. Ogden R.T. Martínez-Hernández I.E. Lin X. Chang Y.B. Rahman A. et al.The reliability of repeated TMS measures in older adults and in patients with subacute and chronic stroke.Front Cell Neurosci. 2015; 9https://doi.org/10.3389/fncel.2015.00335Crossref PubMed Scopus (90) Google Scholar,[5]Turco C.V. Pesevski A. McNicholas P.D. Beaulieu L.-D. Nelson A.J. Reliability of transcranial magnetic stimulation measures of afferent inhibition.Brain Res. 2019; 1723146394https://doi.org/10.1016/j.brainres.2019.146394Crossref PubMed Scopus (16) Google Scholar]. SDCindividual was calculated as [SDCindividual = SEMeas × 1.96 × 2]. This data was used to create estimations of smallest detectable change values at different group sizes (1–100) using the formula [SDCgroup = SDCindividual/ n], where n is the sample size [[6]Beckerman H. Roebroeck M.E. Lankhorst G.J. Becher J.G. Bezemer P.D. Verbeek A.L.M. Smallest real difference, a link between reproducibility and responsiveness.Qual Life Res. 2001; 10: 571-578https://doi.org/10.1023/A:1013138911638Crossref PubMed Scopus (655) Google Scholar]. Analyses were performed on 31 participants as one outlier was removed. All measures were normally distributed and homoscedastic. Reliability statistics are shown in Table 1. CoGy exhibited strong to excellent relative reliability and CoGx demonstrated moderate to strong relative reliability. SEMeas% is <10 % for both measures, indicating low measurement error. Based on SDCindividual, individuals must show a change of ∼8 mm in CoG to be considered real physiological change outside of experimental error. A minimal change of ∼1.5 mm must be present in CoG for a change in a group of 31 participants to be considered real physiological change. For map area, relative reliability was poor to moderate with SEMeas% >10 % indicating large measurement error. Based on SDCindividual, individuals must show a minimal change of 519 mm2 to be attributed to a real change with 95 % confidence. A change of 93 mm2 must be present to be attributed to real physiological change in a group of 31 participants.Table 1Reliability statistics.ICC (95 % CI)SEMeasSEMeas%SDCindividualSDCgroupRMT0.93 (0.86–0.97)2.4 mA6.536.66 mA1.18 mACoGx0.73 (0.45–0.87)2.91 mm1.758.06 mm1.45 mmCoGy0.93 (0.85–0.97)2.93 mm2.628.13 mm1.46 mmMap Area0.17 (−0.71 to 0.60)187.27 mm227.03519.09 mm293.23 mm2SEMeas% expresses the SEMeas as a percentage of the mean.RMT: Resting motor threshold, CI: confidence interval, ICC: intraclass correlation coefficient, SD: standard deviation, SDC: smallest detectable change, SEMeas: standard error of measurement, SEMeas%: relative SEMeas. Open table in a new tab SEMeas% expresses the SEMeas as a percentage of the mean. RMT: Resting motor threshold, CI: confidence interval, ICC: intraclass correlation coefficient, SD: standard deviation, SDC: smallest detectable change, SEMeas: standard error of measurement, SEMeas%: relative SEMeas. The present study is the first to investigate the intersession relative and absolute reliability of fast motor maps over weeks. Using the methodology described by Van de Ruit (2015), results indicate high reliability in measures of CoG, suggesting that studies focusing on intervention-induced changes that require maps acquired over ∼two weeks can reliably use the metric of CoG. Specifically, CoG demonstrated less than 1.5 mm of change required in a sample size of 31 participants to be deemed a real physiological change. CoG has been reported as a metric to examine cortical M1 organization following stroke [[7]Butler A.J. Kahn S. Wolf S.L. Weiss P. Finger extensor variability in TMS parameters among chronic stroke patients.J NeuroEng Rehabil. 2005; 2: 10https://doi.org/10.1186/1743-0003-2-10Crossref PubMed Scopus (49) Google Scholar] and changes in CoG between sessions have been reported after movement therapy in stroke patients [[8]Liepert J. Miltner W.H.R. Bauder H. Sommer M. Dettmers C. Taub E. et al.Motor cortex plasticity during constraint-induced movement therapy in stroke patients.Neurosci Lett. 1998; 250: 5-8https://doi.org/10.1016/S0304-3940(98)00386-3Crossref PubMed Scopus (588) Google Scholar]. Intersession reliability of map area was poor to moderate in this study, in support of findings using traditional mapping [[9]Ngomo S. Leonard G. Moffet H. Mercier C. Comparison of transcranial magnetic stimulation measures obtained at rest and under active conditions and their reliability.J Neurosci Methods. 2012; 205: 65-71https://doi.org/10.1016/j.jneumeth.2011.12.012Crossref PubMed Scopus (124) Google Scholar]. Cavaleri et al. (2018) demonstrated high reliability for map area when maps were acquired 2-h apart (ICC = 0.86) [[10]Cavaleri R. Schabrun S.M. Chipchase L.S. The reliability and validity of rapid transcranial magnetic stimulation mapping.Brain Stimul. 2018; 11: 1291-1295https://doi.org/10.1016/j.brs.2018.07.043Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar], which is quite different from the ∼2 weeks between map acquisition performed herein. Our observation of poor reliability across weeks may relate to changes in cortical excitability from other muscles that may be included in the 6 × 6 cm grid. FCA: Investigation, formal analysis, writing – original draft, writing – review and editing, visualization. SDF: Conceptualization, formal analysis, investigation, writing – original draft, writing – review and editing, visualization. CCD: Investigation, writing – review and editing. CVT: Conceptualization, Writing – Review and Editing. KRR: Investigation, Writing – Review and Editing AJN: Supervision, Conceptualization, Formal analysis, Writing – original draft, writing – review and editing. The authors have no conflicts of interest to declare. This work was supported by the Natural Sciences and Engineering Research Council [RGPIN-2020-06757] to AJN. The authors gratefully acknowledge Mark Van de Ruit for assistance in the fast-mapping technique. The following is the Supplementary data to this article. Download .docx (.39 MB) Help with docx files Multimedia component 1

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