Abstract
Transcranial magnetic stimulation (TMS) motor mapping is a safe, non-invasive method used to study corticomotor organization and intervention-induced plasticity. Reliability of resting maps is well established, but understudied for active maps and unestablished for active maps obtained using robotic TMS techniques. The objective of this study was to determine the reliability of robotic neuro-navigated TMS motor map measures during active muscle contraction. We hypothesized that map area and volume would show excellent short- and medium-term reliability. Twenty healthy adults were tested on 3 days. Active maps of the first dorsal interosseous muscle were created using a 12 × 12 grid (7 mm spacing). Short- (24 h) and medium-term (3–5 weeks) relative (intra-class correlation coefficient) and absolute (minimal detectable change (MDC); standard error of measure) reliabilities were evaluated for map area, volume, center of gravity (CoG), and hotspot magnitude (peak-to-peak MEP amplitude at the hotspot), along with active motor threshold (AMT) and maximum voluntary contraction (MVC). This study found that AMT and MVC had good-to-excellent short- and medium-term reliability. Map CoG (x and y) were the most reliable map measures across sessions with excellent short- and medium-term reliability (p < 0.001). Map area, hotspot magnitude, and map volume followed with better reliability medium-term than short-term, with a change of 28%, 62%, and 78% needed to detect a true medium-term change, respectively. Therefore, robot-guided neuro-navigated TMS active mapping is relatively reliable but varies across measures. This, and MDC, should be considered in interventional study designs.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data are available on reasonable request from the corresponding author.
References
Baumgartner T, Willi M, Jäncke L (2007) Modulation of corticospinal activity by strong emotions evoked by pictures and classical music: a transcranial magnetic stimulation study. NeuroReport 18:261–265. https://doi.org/10.1097/WNR.0B013E328012272E
Carroll TJ, Riek S, Carson RG (2001) Reliability of the input-output properties of the cortico-spinal pathway obtained from transcranial magnetic and electrical stimulation. J Neurosci Methods 112:193–202. https://doi.org/10.1016/S0165-0270(01)00468-X
Caulo M, Briganti C, Mattei PA et al (2007) New morphologic variants of the hand motor cortex as seen with MR imaging in a large study population. Am J Neuroradiol 28:1480–1485. https://doi.org/10.3174/ajnr.A0597
Cavaleri R, Schabrun SM, Chipchase LS (2017) The number of stimuli required to reliably assess corticomotor excitability and primary motor cortical representations using transcranial magnetic stimulation (TMS): a systematic review and meta-analysis. Syst Rev 6:1–11. https://doi.org/10.1186/s13643-017-0440-8
Chang WH, Fried PJ, Saxena S et al (2016) Optimal number of pulses as outcome measures of neuronavigated transcranial magnetic stimulation. Clin Neurophysiol 127:2892–2897. https://doi.org/10.1016/J.CLINPH.2016.04.001
Cicinelli P, Traversa R, Bassi A et al (1997) Interhemispheric differences of hand muscle representation in human motor cortex. Muscle Nerve 20:535–542. https://doi.org/10.1002/(SICI)1097-4598(199705)20:5
Coombes SA, Tandonnet C, Fujiyama H et al (2009) Emotion and motor preparation: a transcranial magnetic stimulation study of corticospinal motor tract excitability. Cogn Affect Behav Neurosci 94(9):380–388. https://doi.org/10.3758/CABN.9.4.380
Damron LA, Dearth DJ, Hoffman RL, Clark BC (2008) Quantification of the corticospinal silent period evoked via transcranial magnetic stimulation. J Neurosci Methods 173:121–128. https://doi.org/10.1016/j.jneumeth.2008.06.001
Di LV, Restuccia D, Oliviero A et al (1998) Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans. J Physiol 508:625–633. https://doi.org/10.1111/j.1469-7793.1998.625bq.x
Ellaway PH, Davey NJ, Maskill DW et al (1998) Variability in the amplitude of skeletal muscle responses to magnetic stimulation of the motor cortex in man1. Electroencephalogr Clin Neurophysiol Mot Control 109:104–113
Friel KM, Kuo H-C, Fuller J et al (2016) Skilled bimanual training drives motor cortex plasticity in children with unilateral cerebral palsy. Neurorehabil Neural Repair 30:834–844. https://doi.org/10.1177/1545968315625838
Gagné M, Hétu S, Reilly KT, Mercier C (2011) The map is not the territory: motor system reorganization in upper limb amputees. Hum Brain Mapp 32:509–519. https://doi.org/10.1002/hbm.21038
Ginhoux R, Renaud P, Zorn L, et al (2013) A custom robot for transcranial magnetic stimulation: first assessment on healthy subjects. In: Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, EMBS. pp 5352–5355
Giuffre A, Kahl CK, Zewdie E et al (2021) Reliability of robotic transcranial magnetic stimulation motor mapping. J Neurophysiol 125:74–85. https://doi.org/10.1152/JN.00527.2020
Goldsworthy MR, Hordacre B, Ridding MC (2016) Minimum number of trials required for within- and between-session reliability of TMS measures of corticospinal excitability. Neuroscience 320:205–209. https://doi.org/10.1016/J.NEUROSCIENCE.2016.02.012
Grab JG, Zewdie E, Carlson HL et al (2018) Robotic TMS mapping of motor cortex in the developing brain. J Neurosci Methods 309:41–54. https://doi.org/10.1016/j.jneumeth.2018.08.007
Grau C, Ginhoux R, Riera A et al (2014) Conscious brain-to-brain communication in humans using non-invasive technologies. PLoS ONE 9:e105225. https://doi.org/10.1371/JOURNAL.PONE.0105225
Hajcak G, Molnar C, George MS et al (2007) Emotion facilitates action: a transcranial magnetic stimulation study of motor cortex excitability during picture viewing. Psychophysiology 44:91–97. https://doi.org/10.1111/J.1469-8986.2006.00487.X
Hasan A, Galea JM, Casula EP et al (2013) Muscle and timing-specific functional connectivity between the dorsolateral prefrontal cortex and the primary motor cortex. J Cogn Neurosci 25:558–570. https://doi.org/10.1162/jocn_a_00338
Jones-Lush LM, Judkins TN, Wittenberg GF (2010) Arm movement maps evoked by cortical magnetic stimulation in a robotic environment. Neuroscience 165:774–781. https://doi.org/10.1016/J.NEUROSCIENCE.2009.10.065
Kahl CK, Kirton A, Pringsheim T et al (2021) Bilateral transcranial magnetic stimulation of the supplementary motor area in children with Tourette syndrome. Dev Med Child Neurol Dmcn. https://doi.org/10.1111/dmcn.14828
Kahl CK, Giuffre A, Wrightson JG et al (2022) Active versus resting neuro-navigated robotic transcranial magnetic stimulation motor mapping. Physiol Rep 10:e15346. https://doi.org/10.14814/PHY2.15346
Kahl CK, Swansburg R, Hai T et al (2022) Differences in neurometabolites and transcranial magnetic stimulation motor maps in children with attention-deficit/hyperactivity disorder. J Psychiatry Neurosci 47:E239–E249. https://doi.org/10.1503/jpn.210186
Kamen G (2004) Reliability of motor-evoked potentials during resting and active contraction conditions. Med Sci Sport Exerc 36:1574–1579. https://doi.org/10.1249/01.MSS.0000139804.02576.6A
Kiers L, Cros D, Chiappa KH, Fang J (1993) Variability of motor potentials evoked by transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol Potentials Sect 89:415–423
Kleim JA, Kleim ED (2007) Cramer SC (2007) Systematic assessment of training-induced changes in corticospinal output to hand using frameless stereotaxic transcranial magnetic stimulation. Nat Protoc 27(2):1675–1684. https://doi.org/10.1038/nprot.2007.206
Klomjai W, Katz R, Lackmy-Vallée A (2015) Basic principles of transcranial magnetic stimulation (TMS) and repetitive TMS (rTMS). Ann Phys Rehabil Med 58:208–213
Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15:155–163. https://doi.org/10.1016/j.jcm.2016.02.012
Littmann AE, McHenry CL, Shields RK (2013) Variability of motor cortical excitability using a novel mapping procedure. J Neurosci Methods 214:137–143. https://doi.org/10.1016/j.jneumeth.2013.01.013
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. https://doi.org/10.1016/j.clinph.2006.02.005
Mortifee P, Stewart H, Schulzer M, Eisen A (1994) Reliability of transcranial magnetic stimulation for mapping the human motor cortex. Electroencephalogr Clin Neurophysiol Evoked Potential 93:131–137. https://doi.org/10.1016/0168-5597(94)90076-0
Ngomo S, Leonard G, Moffet H, Mercier C (2012) Comparison of transcranial magnetic stimulation measures obtained at rest and under active conditions and their reliability. J Neurosci Methods 205:65–71. https://doi.org/10.1016/j.jneumeth.2011.12.012
Ngomo S, Mercier C, Bouyer LJ et al (2015) Alterations in central motor representation increase over time in individuals with rotator cuff tendinopathy. Clin Neurophysiol 126:365–371. https://doi.org/10.1016/j.clinph.2014.05.035
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113. https://doi.org/10.1016/0028-3932(71)90067-4
Rosenkranz K, Rothwell JC (2004) The effect of sensory input and attention on the sensorimotor organization of the hand area of the human motor cortex. J Physiol 561:307–320. https://doi.org/10.1113/JPHYSIOL.2004.069328
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
Rossini PM, Desiato MT, Lavaroni F, Caramia MD (1991) Brain excitability and electroencephalographic activation: non-invasive evaluation in healthy humans via transcranial magnetic stimulation. Brain Res 567:111–119. https://doi.org/10.1016/0006-8993(91)91442-4
Rossini PM, Barker AT, Berardelli A et al (1994) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91:79–92. https://doi.org/10.1016/0013-4694(94)90029-9
Shrout PE, Fleiss JL (1979) Intraclass correlations: Uses in assessing rater reliability. Psychol Bull 86:420–428
Stephani C, Paulus W, Sommer M (2016) The effect of current flow direction on motor hot spot allocation by transcranial magnetic stimulation. Physiol Rep 4:e12666. https://doi.org/10.14814/PHY2.12666
Thompson PD, Day BL, Rothwell JC et al (1991) Further observations on the facilitation of muscle responses to cortical stimulation by voluntary contraction. Electroencephalogr Clin Neurophysiol Evoked Potential 81:397–402. https://doi.org/10.1016/0168-5597(91)90029-W
Van Hedel HJ, Murer C, Dietz V, Curt A (2007) The amplitude of lower leg motor evoked potentials is a reliable measure when controlled for torque and motor task. J Neurol 254:1089–1098. https://doi.org/10.1007/s00415-006-0493-4
van de Ruit M, Grey MJ (2016) The TMS map scales with increased stimulation intensity and muscle activation. Brain Topogr 29:56–66
Van De Ruit M, Perenboom MJL, Grey MJ (2015) TMS brain mapping in less than two minutes. Brain Stimul 8:231–239. https://doi.org/10.1016/j.brs.2014.10.020
Yousry TA, Schmid UD, Alkadhi H et al (1997) Localization of the motor hand area to a knob on the precentral gyrus. A New Landmark. Brain 120:141–157
Zewdie E, Ciechanski P, Kuo HC et al (2019) Safety and tolerability of transcranial magnetic and direct current stimulation in children: Prospective single center evidence from 3.5 million stimulations (under review). Brain Stimul 13(3):565–575
Funding
This work was supported by the Canadian Institute for Health Research (CIHR), the Branch Out Neurological Foundation (BONF), and support for the Scientific Director of the Strategic Clinical Network for Addictions and Mental Health from Alberta Health Services.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
There are no conflicts of interest.
Additional information
Communicated by Winston D Byblow.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Kahl, C.K., Giuffre, A., Wrightson, J.G. et al. Reliability of active robotic neuro-navigated transcranial magnetic stimulation motor maps. Exp Brain Res 241, 355–364 (2023). https://doi.org/10.1007/s00221-022-06523-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-022-06523-3