Name: standing neurophysiological assessment of lower extremity muscles post-stroke
Uploaded: 2021-07-26T14:00:00
Description: Watch this Scientific Journal Video about Standing Neurophysiological Assessment of Lower Extremity Muscles Post-Stroke at JoVE.com

The authors would like to acknowledge Mr. Brian Cence and Mrs. Alyssa Chestnut for their contributions to participant recruitment and data collection.
Funding for this project was provided in part by a Technical Development Award from the NIH National Center for Neuromodulation for Rehabilitation (NM4R) (HD086844) and by Veteran&#39;s Affairs Rehabilitation Research and Development Career Development Award 1 (RX003126) and Merit award (RX002665).
The contents of this report do not represent the views of the U.S. Department of Veterans Affairs, U.S. National Institutes of Health, or the United States Government.

All procedures were approved by the Institutional Review Board at the Medical University of South Carolina and conformed to the Declaration of Helsinki.
1. Participant recruitment
<ol>
	<li>Recruit individuals post-stroke from the local database. For this experiment, 16 individuals were recruited from a local electronic recruitment database. In some instances, participants were recruited specifically because they had failed to respond to TMS at rest in previous studies performed by our resea...

<ol>
	<li>Kesar, T. M., Stinear, J. W., Wolf, S. L. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=The+use+of+transcranial+magnetic+stimulation+to+evaluate+cortical+excitability+of+lower+limb+musculature:+Challenges+and+opportunities.">The use of transcranial magnetic stimulation to evaluate cortical excitability of lower limb musculature: Challenges and opportunities.</a> Restorative Neurology and Neuroscience. 36 (3), 333-348 (2018).</li><li>Sivaramakrishnan, A., Madhavan, S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Absence+of+a+transcranial+magnetic+stimulation-induced+lower+limb+corticomotor+response+does+not+affect+walking+speed+in+chronic+stroke+survivors.">Absence of a transcranial magnetic stimulation-induced lower limb corticomotor response does not affect walking speed in chronic stroke survivors.</a> Stroke. 49 (8), 2004-2007 (2018).</li><li>Kindred, J. H., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Individualized+responses+to+ipsilesional+high-frequency+and+contralesional+low-frequency+rTMS+in+chronic+stroke:+A+pilot+study+to+support+the+individualization+of+neuromodulation+for+rehabilitation.">Individualized responses to ipsilesional high-frequency and contralesional low-frequency rTMS in chronic stroke: A pilot study to support the individualization of neuromodulation for rehabilitation.</a> Frontiers in Human Neuroscience. 14, 578127 (2020).</li><li>Lu, M., Ueno, S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Comparison+of+the+induced+fields+using+different+coil+configurations+during+deep+transcranial+magnetic+stimulation.">Comparison of the induced fields using different coil configurations during deep transcranial magnetic stimulation.</a> PLoS One. 12 (6), 0178422 (2017).</li><li>Hess, C. W., Mills, K. R., Murray, N. M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Responses+in+small+hand+muscles+from+magnetic+stimulation+of+the+human+brain.">Responses in small hand muscles from magnetic stimulation of the human brain.</a> The Journal of Physiology. 388, 397-419 (1987).</li><li>Petersen, N., Christensen, L. O., Nielsen, J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=The+effect+of+transcranial+magnetic+stimulation+on+the+soleus+H+reflex+during+human+walking.">The effect of transcranial magnetic stimulation on the soleus H reflex during human walking.</a> The Journal of Physiology. 513, 599-610 (1998).</li><li>Capaday, C., Lavoie, B. A., Barbeau, H., Schneider, C., Bonnard, M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Studies+on+the+corticospinal+control+of+human+walking.+I.+Responses+to+focal+transcranial+magnetic+stimulation+of+the+motor+cortex.">Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex.</a> Journal of Neurophysiology. 81 (1), 129-139 (1999).</li><li>Schubert, M., Curt, A., Colombo, G., Berger, W., Dietz, V. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Voluntary+control+of+human+gait:+conditioning+of+magnetically+evoked+motor+responses+in+a+precision+stepping+task.">Voluntary control of human gait: conditioning of magnetically evoked motor responses in a precision stepping task.</a> Experimental Brain Research. 126 (4), 583-588 (1999).</li><li>Ackermann, H., Scholz, E., Koehler, W., Dichgans, J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Influence+of+posture+and+voluntary+background+contraction+upon+compound+muscle+action+potentials+from+anterior+tibial+and+soleus+muscle+following+transcranial+magnetic+stimulation.">Influence of posture and voluntary background contraction upon compound muscle action potentials from anterior tibial and soleus muscle following transcranial magnetic stimulation.</a> Electroencephalography and Clinical Neurophysiology. 81 (1), 71-80 (1991).</li><li>Lavoie, B. A., Cody, F. W., Capaday, C. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Cortical+control+of+human+soleus+muscle+during+volitional+and+postural+activities+studied+using+focal+magnetic+stimulation.">Cortical control of human soleus muscle during volitional and postural activities studied using focal magnetic stimulation.</a> Experimental Brain Research. 103 (1), 97-107 (1995).</li><li>Soto, O., Valls-Sol&#233;, J., Shanahan, P., Rothwell, J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Reduction+of+intracortical+inhibition+in+soleus+muscle+during+postural+activity.">Reduction of intracortical inhibition in soleus muscle during postural activity.</a> Journal of Neurophysiology. 96 (4), 1711-1717 (2006).</li><li>Kesar, T. M., Eicholtz, S., Lin, B. J., Wolf, S. L., Borich, M. R. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Effects+of+posture+and+coactivation+on+corticomotor+excitability+of+ankle+muscles.">Effects of posture and coactivation on corticomotor excitability of ankle muscles.</a> Restorative Neurology and Neuroscience. 36 (1), 131-146 (2018).</li><li>Nandi, T., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=In+standing,+corticospinal+excitability+is+proportional+to+COP+velocity+whereas+M1+excitability+is+participant-specific.">In standing, corticospinal excitability is proportional to COP velocity whereas M1 excitability is participant-specific.</a> Frontiers in Human Neuroscience. 12, 303 (2018).</li><li>Tokuno, C. D., Keller, M., Carpenter, M. G., M&#225;rquez, G., Taube, W. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Alterations+in+the+cortical+control+of+standing+posture+during+varying+levels+of+postural+threat+and+task+difficulty.">Alterations in the cortical control of standing posture during varying levels of postural threat and task difficulty.</a> Journal of Neurophysiology. 120 (3), 1010-1016 (2018).</li><li>Mouthon, A., Taube, W. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Intracortical+inhibition+increases+during+postural+task+execution+in+response+to+balance+training.">Intracortical inhibition increases during postural task execution in response to balance training.</a> Neuroscience. 401, 35-42 (2019).</li><li>Charalambous, C. C., Liang, J. N., Kautz, S. A., George, M. S., Bowden, M. G. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Bilateral+assessment+of+the+corticospinal+pathways+of+the+ankle+muscles+using+navigated+transcranial+magnetic+stimulation.">Bilateral assessment of the corticospinal pathways of the ankle muscles using navigated transcranial magnetic stimulation.</a> Journal of Visualized Experiments: JoVE. (144), (2019).</li><li>Hermens, H. J., Freriks, B., Disselhorst-Klug, C., Rau, G. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Development+of+recommendations+for+SEMG+sensors+and+sensor+placement+procedures.">Development of recommendations for SEMG sensors and sensor placement procedures.</a> Journal of Electromyography and Kinesiology. 10 (5), 361-374 (2000).</li><li>Tankisi, H., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Standards+of+instrumentation+of+EMG.">Standards of instrumentation of EMG.</a> Clinical Neurophysiology. 131 (1), 243-258 (2020).</li><li>Mishory, A., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=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.">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.</a> The Journal of ECT. 20 (3), 160-165 (2004).</li><li>Borckardt, J. J., Nahas, Z., Koola, J., George, M. S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Estimating+resting+motor+thresholds+in+transcranial+magnetic+stimulation+research+and+practice:+a+computer+simulation+evaluation+of+best+methods.">Estimating resting motor thresholds in transcranial magnetic stimulation research and practice: a computer simulation evaluation of best methods.</a> The Journal of ECT. 22 (3), 169-175 (2006).</li><li>McNemar, Q. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Note+on+the+sampling+error+of+the+difference+between+correlated+proportions+or+percentages.">Note on the sampling error of the difference between correlated proportions or percentages.</a> Psychometrika. 12 (2), 153-157 (1947).</li><li>Rossi, S., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Safety+and+recommendations+for+TMS+use+in+healthy+subjects+and+patient+populations,+with+updates+on+training,+ethical+and+regulatory+issues:+Expert+Guidelines.">Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: Expert Guidelines.</a> Clinical Neurophysiology. 132 (1), 269-306 (2021).</li><li>McDonnell, M. N., Stinear, C. M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=TMS+measures+of+motor+cortex+function+after+stroke:+A+meta-analysis.">TMS measures of motor cortex function after stroke: A meta-analysis.</a> Brain Stimulation. 10 (4), 721-734 (2017).</li><li>Reis, J., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Contribution+of+transcranial+magnetic+stimulation+to+the+understanding+of+cortical+mechanisms+involved+in+motor+control.">Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control.</a> The Journal of Physiology. 586 (2), 325-351 (2008).</li><li>Chen, G., Patten, C., Kothari, D. H., Zajac, F. E. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Gait+differences+between+individuals+with+post-stroke+hemiparesis+and+non-disabled+controls+at+matched+speeds.">Gait differences between individuals with post-stroke hemiparesis and non-disabled controls at matched speeds.</a> Gait &amp; Posture. 22 (1), 51-56 (2005).</li><li>Knarr, B. A., Reisman, D. S., Binder-Macleod, S. A., Higginson, J. S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Understanding+compensatory+strategies+for+muscle+weakness+during+gait+by+simulating+activation+deficits+seen+post-stroke.">Understanding compensatory strategies for muscle weakness during gait by simulating activation deficits seen post-stroke.</a> Gait &amp; Posture. 38 (2), 270-275 (2013).</li><li>Ammann, C., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=A+framework+to+assess+the+impact+of+number+of+trials+on+the+amplitude+of+motor+evoked+potentials.">A framework to assess the impact of number of trials on the amplitude of motor evoked potentials.</a> Scientific Reports. 10 (1), 21422 (2020).</li></ol>

The experimental protocol was well tolerated by most participants. One individual was unable to complete the standing TMS evaluation due to preexisting decubitus ulcers secondary to diabetic complications and orthopedic issues involving preexisting knee pain. The amount of loading/unloading of body weight from the legs was minimal. However, there was, on average, a slightly greater downward force measured during the application of the TMS pulses. This is likely due to the weight of the coil and the downward pressure appl...

Transcranial magnetic stimulation (TMS) is an instrument used to measure the behavior of neural circuits. The majority of TMS investigations focusing on the study of motor control/performance have been conducted in the upper extremities. The imbalance between the upper and lower extremity studies is in part due to the additional challenges in measuring the lower extremity corticomotor response (CMR). Some of these methodological obstacles include the smaller cortical representations of the lower extremity muscles within the motor cortex and the deeper location of the representations relative to the scalp1. In populations with neurological injury, additional hurdles are also present. For example, approximately half of the individuals post-stroke show no response to TMS at rest in lower extremity muscles2,3. The lack of post-stroke response to TMS is even seen when patients maintain some volitional control of the muscles, indicating at least a partially intact corticospinal tract.
The lack of measurable TMS responses with maintained motor function contributes to our decreased understanding of post-stroke postural and walking-specific motor control and the neurophysiological effects of neurorehabilitation. However, some of the challenges of lower extremity post-stroke neurophysiological assessments have been overcome. For example, a double-cone coil can be used to reliably activate the lower extremity motoneurons located deep in the interhemispheric fissure1. The double-cone coil produces a larger and stronger magnetic field that penetrates deeper into the brain than the more commonly used figure-of-eight coil4. Another methodological change that can be implemented to increase the responsiveness to TMS is measuring the CMR during a slight voluntary contraction5. Generally, this contraction is performed at a predetermined level of either maximal voluntary joint torque or maximal electromyographic (EMG) muscle activity. Peripheral nerve stimulation can also be used to elicit a maximal muscle response and the recorded EMG of this response can be used to set the targeted voluntary activation of the muscle.
Performing TMS assessment post-stroke during active muscle contraction is fairly common in the upper extremities where isometric tasks can mimic functional activities, for example, grasping/holding objects. In contrast, walking is accomplished through the bilateral activation of multiple muscle groups via cortical, subcortical, and spinal cord structures and requires postural muscle activation to resist the effects of gravity. This activation state is likely not reflected when measuring isolated muscles producing an isometric contraction. Several previous studies directed at understanding postural and walking-specific motor control have delivered TMS pulses while participants were walking6,7,8 and standing9,10,11,12,13,14,15. The measurement of the CMR in the upright position allows for the activation of postural muscles and subcortical components of the postural and gait motor-control networks. To date, there have not been any reports of performing standing TMS assessments in individuals post-stroke.
This study proposes a standardized methodology, built upon the existing body of literature of standing TMS methods6,7,8,9,10,11,12,13,14,15, for standing TMS assessment of the CMR post-stroke. This methodology can be utilized by research groups studying, but not limited to, postural deficits and walking-specific motor control post-stroke and establish greater consistency of TMS procedures. The purpose of this methodological investigation was to determine whether standing TMS assessments are feasible in individuals post-stroke with moderate gait impairments. We hypothesized that performing assessments in the standing position would 1) increase the likelihood of eliciting a measurable response (motor evoked potential, MEP) and 2) that the stimulator power/intensity used to perform standing TMS assessments would be lower than that of the usually performed sitting/resting assessments. We believe the successful completion and widespread use of this protocol may lead to a greater understanding of the neurophysiological aspects of post-stroke postural and walking-specific motor control and the effects of neurorehabilitation.

<table border="1" fo:keep-together.within-page="1" fo:keep-with-next.within-page="always">
	<tbody>
		<tr>
			<td>Data Acquisition Software</td>
			<td>MathWorks</td>
			<td>MatLab</td>
			<td>The custom data collection program was written in Matlab. However, other software/hardware providers can be used (e.g. National Instruments, AD Instruments, CED Spike2 or Signal)</td>
		</tr>
		<tr>
			<td>Double-cone coil</td>
			<td>Magstim</td>
			<td>D110</td>
			<td>Double-cone coil for TMS pulse delivery</td>
		</tr>
		<tr>
			<td>Dual force plate</td>
			<td>Advanced Mechanical Technology Inc (AMTI)</td>
			<td>Dual-top Accusway</td>
			<td>Force plate used to measure force/weight distrobution under each leg independently.</td>
		</tr>
		<tr>
			<td>Dual-pulse TMS</td>
			<td>Magstim</td>
			<td>Bistim 200</td>
			<td>Connects two Magstim 200 units together for dual-pulse applications</td>
		</tr>
		<tr>
			<td>EMG pre-amplifiers</td>
			<td>Motion Labs Inc</td>
			<td>MA-422</td>
			<td>Preamplifiers for disposable surface EMG electrodes</td>
		</tr>
		<tr>
			<td>EMG system</td>
			<td>Motion Labs Inc</td>
			<td>MA400</td>
			<td>EMG system for data collection</td>
		</tr>
		<tr>
			<td>Neuronavigation System</td>
			<td>Rogue Research</td>
			<td>Brainsight</td>
			<td>Software and hardware used to ensure consistent placement/delivery of magnetic stimulations. Marking the stimulation location on a participant&#39;s head or on a place showercap can also be used in the absence of neuronavigational software.</td>
		</tr>
		<tr>
			<td>Recruitment Database</td>
			<td>N/A</td>
			<td>N/A</td>
			<td>Electronic database including names of possible individuals who are eligble for your studies.</td>
		</tr>
		<tr>
			<td>TMS unit (x2)</td>
			<td>Magstim</td>
			<td>Magstim 200</td>
			<td>Delivers TMS pulses</td>
		</tr>
	</tbody>
</table>

standing neurophysiological assessment of lower extremity muscles post-stroke

Transcranial magnetic stimulation (TMS) is a common tool used to measure the behavior of motor circuits in healthy and neurologically impaired populations. TMS is used extensively to study motor control and the response to neurorehabilitation of the upper extremities. However, TMS has been less utilized in the study of lower extremity postural and walking-specific motor control. The limited use and the additional methodological challenges of lower extremity TMS assessments have contributed to the lack of consistency in lower extremity TMS procedures within the literature. Inspired by the decreased ability to record lower extremity TMS motor evoked potentials (MEP), this methodological report details steps to enable post-stroke TMS assessments in a standing posture. The standing posture allows for the activation of the neuromuscular system, reflecting a state more akin to the system's state during postural and walking tasks. Using dual-top force plates, we instructed participants to equally distribute their weight between their paretic and non-paretic legs. Visual feedback of the participants' weight distribution was provided. Using image guidance software, we delivered single TMS pulses via a double-cone coil to the participants' lesioned and non-lesioned hemispheres and measured the corticomotor response of the paretic and non-paretic tibialis anterior and soleus muscles. Performing assessments in the standing position increased the TMS response rate and allowed for the use of the lower stimulation intensities compared to the standard sitting/resting position. Utilization of this TMS protocol can provide a common approach to assess the lower extremity corticomotor response post-stroke when the neurorehabilitation of postural and gait impairments are of interest.

One participant was removed from the analysis due to the inability to tolerate the standing TMS procedure due to preexisting knee pain and a diabetic wound received before their arrival to the research laboratory, leaving a final sample size of 15. The diabetic wound was directly over the TA and precluded any sEMG measures of this muscle. There were no major adverse events reported to the investigators during either the sitting or standing TMS procedures. Several minor adverse events were reported, such as neck muscle pa...

Watch this Scientific Journal Video about Standing Neurophysiological Assessment of Lower Extremity Muscles Post-Stroke at JoVE.com

Standing Neurophysiological Assessment of Lower Extremity Muscles Post-Stroke

This protocol describes the process for performing a neurophysiological assessment of the lower extremity muscles, tibialis anterior and soleus, in a standing position using TMS in people post-stroke. This position provides a greater probability of eliciting a post-stroke TMS response and allows for the use of reduced stimulator power during neurophysiological assessments.

Transcranial magnetic stimulation (TMS) is a common tool used to measure the behavior of motor circuits in healthy and neurologically impaired ...

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