Comparison of Rossini–Rothwell and adaptive threshold‐hunting methods on the stability of TMS induced motor evoked potentials amplitudes

Several methods can be used to determine the resting motor threshold (RMT) and by that recording transcranial magnetic stimulation (TMS) induced motor evoked potentials (MEPs). However, no research has compared the test retest reliability of these methods. Thus, the aim of this study was to determine intra‐ and inter‐session reliability of Rossini–Rothwell (R–R) and parameter estimation by sequential testing (PEST) methods on TMS‐induced MEPs and comparison of these two methods on RMT. Twelve healthy individuals participated in this study three times (T1, T2 and T3) over two days. TMS was applied using both R–R and PEST to estimate RMT and average of 25 MEPs were acquired at each of the three time points. The intra‐class correlation coefficient indicated high intra‐session reliability in the MEP amplitudes for both methods (0.79 and 0.88, R–R and PEST respectively). The RMT and MEP amplitudes had higher inter‐session reliability in both methods (0.99 and 0.998, R–R and PEST respectively; 0.84 and 0.76, R–R and PEST respectively). There was no significant difference between methods for RMT at both T1 (maximum stimulator output of R–R vs. PEST, 33.7% ± 7.7% vs. 33.8% ± 7.6%, p = 0.75) and T3 (maximum stimulator output of R–R vs. PEST, 33.5% ± 7.3% vs. 33.7% ± 7.3%, p = 0.19). There was a significant positive correlation between the methods' estimates of RMT, with PEST requiring significantly fewer stimuli. This study shows that the R–R and PEST methods have high intra‐and inter‐session reliability and the same precision, with PEST having the advantage over R–R in speed of estimation of RMT.

[1]  Ryan T. Crews,et al.  Reliability of motor-evoked potentials in the ADM muscle of older adults , 2007, Journal of Neuroscience Methods.

[2]  F. Awiszus TMS and threshold hunting. , 2003, Supplements to Clinical neurophysiology.

[3]  T. Miles,et al.  Age and sex differences in human motor cortex input–output characteristics , 2003, The Journal of physiology.

[4]  Christelle B Ah Sen,et al.  Active and resting motor threshold are efficiently obtained with adaptive threshold hunting , 2017, PloS one.

[5]  J. Rothwell,et al.  A checklist for assessing the methodological quality of studies using transcranial magnetic stimulation to study the motor system: An international consensus study , 2012, Clinical Neurophysiology.

[6]  Gary Kamen,et al.  Reliability of motor-evoked potentials during resting and active contraction conditions. , 2004, Medicine and science in sports and exercise.

[7]  S. Jaberzadeh,et al.  Inter-pulse Interval Affects the Size of Single-pulse TMS-induced Motor Evoked Potentials: A Reliability Study , 2015, Basic and clinical neuroscience.

[8]  N. Schweighofer,et al.  Fast estimation of transcranial magnetic stimulation motor threshold , 2011, Brain Stimulation.

[9]  H. Bostock,et al.  Two phases of intracortical inhibition revealed by transcranial magnetic threshold tracking , 2002, Experimental Brain Research.

[10]  Shapour Jaberzadeh,et al.  A Higher Number of TMS-Elicited MEP from a Combined Hotspot Improves Intra- and Inter-Session Reliability of the Upper Limb Muscles in Healthy Individuals , 2012, PloS one.

[11]  P. Rossini,et al.  Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[12]  A. Costantini,et al.  Motor threshold in transcranial magnetic stimulation: comparison of three estimation methods , 2006, Neurophysiologie Clinique/Clinical Neurophysiology.

[13]  P M Rossini,et al.  Clinical applications of motor evoked potentials. , 1998, Electroencephalography and clinical neurophysiology.

[14]  K L Gilmore,et al.  Using surface electromyography in physiotherapy research. , 1983, The Australian journal of physiotherapy.

[15]  D. Long,et al.  Transcranial Magnetic Stimulation: A Neurochronometrics of Mind , 2004 .

[16]  Jejo D. Koola,et al.  The Maximum-likelihood Strategy for Determining Transcranial Magnetic Stimulation Motor Threshold, Using Parameter Estimation by Sequential Testing Is Faster Than Conventional Methods With Similar Precision , 2004, The journal of ECT.

[17]  P. A. Tonali,et al.  Effects of aging on motor cortex excitability , 2006, Neuroscience Research.

[18]  F. Awiszus,et al.  Characterisation of paired-pulse transcranial magnetic stimulation conditions yielding intracortical inhibition or I-wave facilitation using a threshold-hunting paradigm , 1999, Experimental Brain Research.

[19]  E. Wassermann,et al.  A safety screening questionnaire for transcranial magnetic stimulation , 2001, Clinical Neurophysiology.

[20]  S. Au-Yeung,et al.  Reliability of transcranial magnetic stimulation induced corticomotor excitability measurements for a hand muscle in healthy and chronic stroke subjects , 2014, Journal of the Neurological Sciences.

[21]  R. Cohen Kadosh,et al.  Can transcranial electrical stimulation improve learning difficulties in atypical brain development? A future possibility for cognitive training , 2013, Developmental Cognitive Neuroscience.

[22]  K. Chiappa,et al.  Clinical applications of motor evoked potentials. , 1993, Advances in neurology.

[23]  M. Sale,et al.  Male human motor cortex stimulus-response characteristics are not altered by aging. , 2011, Journal of applied physiology.

[24]  M. Könönen,et al.  Does second-scale intertrial interval affect motor evoked potentials induced by single-pulse transcranial magnetic stimulation? , 2012, Brain Stimulation.

[25]  P. Fitzgerald,et al.  Reliability of Motor Evoked Potentials Induced by Transcranial Magnetic Stimulation: The Effects of Initial Motor Evoked Potentials Removal , 2017, Basic and clinical neuroscience.

[26]  Friedemann Awiszus,et al.  Fast estimation of transcranial magnetic stimulation motor threshold: is it safe? , 2011, Brain Stimulation.

[27]  U. Ziemann,et al.  Hysteresis effects on the input–output curve of motor evoked potentials , 2009, Clinical Neurophysiology.

[28]  J. C. Rothwell,et al.  Magnetic stimulation : motor evoked potentials , 2010 .

[29]  P. Rossini,et al.  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. , 1994, Electroencephalography and clinical neurophysiology.

[30]  D. Altman,et al.  STATISTICAL METHODS FOR ASSESSING AGREEMENT BETWEEN TWO METHODS OF CLINICAL MEASUREMENT , 1986, The Lancet.

[31]  P. Fitzgerald,et al.  Blood Oxygenation Changes Modulated by Coil Orientation During Prefrontal Transcranial Magnetic Stimulation , 2013, Brain Stimulation.

[32]  C. Terwee,et al.  When to use agreement versus reliability measures. , 2006, Journal of clinical epidemiology.

[33]  U. Ziemann,et al.  A practical guide to diagnostic transcranial magnetic stimulation: Report of an IFCN committee , 2012, Clinical Neurophysiology.

[34]  H. Moffet,et al.  Comparison of transcranial magnetic stimulation measures obtained at rest and under active conditions and their reliability , 2012, Journal of Neuroscience Methods.

[35]  K. Mills,et al.  Corticomotor threshold to magnetic stimulation: Normal values and repeatability , 1997, Muscle & nerve.

[36]  G. Thickbroom,et al.  A comparison of relative-frequency and threshold-hunting methods to determine stimulus intensity in transcranial magnetic stimulation , 2013, Clinical Neurophysiology.

[37]  S. A. Brandt,et al.  An initial transient-state and reliable measures of corticospinal excitability in TMS studies , 2009, Clinical Neurophysiology.

[38]  D. Newham,et al.  The Effect of Coil Type and Navigation on the Reliability of Transcranial Magnetic Stimulation , 2012, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[39]  S. Rossi,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 , 2015, Clinical Neurophysiology.

[40]  Leslie G. Portney Dpt PhD Fapta,et al.  Foundations of Clinical Research: Applications to Practice , 2015 .

[41]  V. Santilli,et al.  Reliability of TMS-related measures of tibialis anterior muscle in patients with chronic stroke and healthy subjects , 2011, Journal of the Neurological Sciences.

[42]  A. Beckett,et al.  AKUFO AND IBARAPA. , 1965, Lancet.