Top

Published in:

Open Access 01-04-2023 | Motor Evoked Potential | Research Article

Effects of trunk neuromuscular electrical stimulation on the motor circuits of able-bodied individuals

Authors: Atsushi Sasaki, Na Cao, Akiko Yuasa, Milos R. Popovic, Kimitaka Nakazawa, Matija Milosevic

Published in: Experimental Brain Research | Issue 4/2023

Abstract

Upper- and lower-limb neuromuscular electrical stimulation (NMES) is known to modulate the excitability of the neural motor circuits. However, it remains unclear whether short-duration trunk muscle NMES could achieve similar neuromodulation effects. We assessed motor evoked potentials (MEPs) elicited through transcranial magnetic stimulation of the primary motor cortex representation of the trunk extensor muscles to evaluate corticospinal excitability. Moreover, cervicomedullary motor evoked potentials (CMEPs) were assessed through cervicomedullary junction magnetic stimulation to evaluate subcortical excitability. Twelve able-bodied individuals participated in the MEP study, and another twelve in the CMEP study. During the interventions, NMES was applied bilaterally to activate the erector spinae muscle and produce intermittent contractions (20 s ON/20 s OFF) for a total of 20 min while participants remained seated. Assessments were performed: (i) before; (ii) during (in brief periods when NMES was OFF); and (iii) immediately after the interventions to compare MEP or CMEP excitability. Our results showed that MEP responses were not affected by trunk NMES, while CMEP responses were facilitated for approximately 8 min during the intervention, and returned to baseline before the end of the 20 min stimulating period. Our findings therefore suggest that short-duration NMES of the trunk extensor muscles likely does not affect the corticospinal excitability, but it has a potential to facilitate subcortical neural circuits immediately after starting the intervention. These findings indicate that short-duration application of NEMS may be helpful in rehabilitation to enhance neuromodulation of the trunk subcortical neural motor circuits.

Andrews RK, Schabrun SM, Ridding MC et al (2013) The effect of electrical stimulation on corticospinal excitability is dependent on application duration: a same subject pre-post test design. J Neuroeng Rehabil 10:1–7. https://doi.org/10.1186/1743-0003-10-51CrossRef

Armstrong KL, Lombardo LM, Foglyano KM et al (2018) Automatic application of neural stimulation during wheelchair propulsion after SCI enhances recovery of upright sitting from destabilizing events. J Neuroeng Rehabil 15:1–13. https://doi.org/10.1186/s12984-018-0362-2CrossRef

Baldissera F, Cavallari P (1993) Short-latency subliminal effects of transcranial magnetic stimulation on forearm motoneurones. Exp Brain Res 96:513–518. https://doi.org/10.1007/BF00234119CrossRefPubMed

Barsi GI, Popovic DB, Tarkka IM et al (2008) Cortical excitability changes following grasping exercise augmented with electrical stimulation. Exp Brain Res 191:57–66. https://doi.org/10.1007/s00221-008-1495-5CrossRefPubMed

Barss TS, Sallis BWM, Miller DJ, Collins DF (2021) Does increasing the number of channels during neuromuscular electrical stimulation reduce fatigability and produce larger contractions with less discomfort? Eur J Appl Physiol 121:2621–2633. https://doi.org/10.1007/s00421-021-04742-0CrossRefPubMed

Benavides FD, Jo HJ, Lundell H et al (2020) Cortical and subcortical effects of transcutaneous spinal cord stimulation in humans with tetraplegia. J Neurosci 40:2633–2643. https://doi.org/10.1523/JNEUROSCI.2374-19.2020CrossRefPubMedPubMedCentral

Bergquist AJ, Clair JM, Lagerquist O et al (2011) Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley. Eur J Appl Physiol 111:2409–2426. https://doi.org/10.1007/s00421-011-2087-9CrossRefPubMed

Butler JE, Taylor JL, Gandevia SC (2003) Responses of human motoneurons to corticospinal stimulation during maximal voluntary contractions and ischemia. J Neurosci 23:10224–10230CrossRefPubMedPubMedCentral

Carson RG, Buick AR (2021) Neuromuscular electrical stimulation-promoted plasticity of the human brain. J Physiol 599:2375–2399. https://doi.org/10.1113/JP278298CrossRefPubMed

Chiou SY, Hurry M, Reed T et al (2018a) Cortical contributions to anticipatory postural adjustments in the trunk. J Physiol 596:1295–1306. https://doi.org/10.1113/JP275312CrossRefPubMedPubMedCentral

Chiou SY, Strutton PH, Perez MA (2018b) Crossed corticospinal facilitation between arm and trunk muscles in humans. J Neurophysiol 120:2595–2602. https://doi.org/10.1152/jn.00178.2018CrossRefPubMedPubMedCentral

Cohen J (1988) Statistical power analysis for the behavioral sciences. Academic press

Cottingham SL, Femano PA, Pfaff DW (1988) Vestibulospinal and reticulospinal interactions in the activation of back muscle EMG in the rat. Exp Brain Res 73:198–208CrossRefPubMed

de Noordhout AM, Rapisarda G, Bogacz D et al (1999) Corticomotoneuronal synaptic connections in normal man An electrophysiological study. Brain 122:1327–1340CrossRefPubMed

Elgueta-Cancino E, Massé-Alarie H, Schabrun SM, Hodges PW (2019) Electrical stimulation of back muscles does not prime the corticospinal pathway. Neuromodulation Technol Neural Interface 22:555–563. https://doi.org/10.1111/ner.12978CrossRef

Galea MP, Hammar I, Nilsson E, Jankowska E (2010) Bilateral postsynaptic actions of pyramidal tract and reticulospinal neurons on feline erector spinae motoneurons. J Neurosci 30:858–869. https://doi.org/10.1158/0008-5472.CAN-10-4002.BONECrossRefPubMedPubMedCentral

Goldring S, Aras E, Weber PC (1970) Comparative study of sensory input to motor cortex in animals and man. Electroencephalogr Clin Neurophysiol 29:537–550. https://doi.org/10.1016/0013-4694(70)90096-9CrossRefPubMed

Jean-Charles L, Nepveu JF, Deffeyes JE et al (2017) Interhemispheric interactions between trunk muscle representations of the primary motor cortex. J Neurophysiol 118:1488–1500. https://doi.org/10.1152/jn.00778.2016CrossRefPubMedPubMedCentral

Jimenez S, Mordillo-Mateos L, Dileone M et al (2018) Effects of patterned peripheral nerve stimulation on soleus spinal motor neuron excitability. PLoS One 13:1–13. https://doi.org/10.1371/journal.pone.0192471CrossRef

Kaelin-Lang A, Luft AR, Sawaki L et al (2002) Modulation of human corticomotor excitability by somatosensory input. J Physiol 540:623–633. https://doi.org/10.1113/jphysiol.2001.012801CrossRefPubMedPubMedCentral

Khaslavskaia S, Sinkjaer T (2005) Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive. Exp Brain Res 162:497–502. https://doi.org/10.1007/s00221-004-2153-1CrossRefPubMed

Khaslavskaia S, Ladouceur M, Sinkjaer T (2002) Increase in tibialis anterior motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve. Exp Brain Res 145:309–315. https://doi.org/10.1007/s00221-002-1094-9CrossRefPubMed

Kitago T, Mazzocchio R, Liuzzi G, Cohen LG (2004) Modulation of H-reflex excitability by tetanic stimulation. Clin Neurophysiol 115:858–861. https://doi.org/10.1016/j.clinph.2003.11.029CrossRefPubMed

Knash ME, Kido A, Gorassini M et al (2003) Electrical stimulation of the human common peroneal nerve elicits lasting facilitation of cortical motor-evoked potentials. Exp Brain Res 153:366–377. https://doi.org/10.1007/s00221-003-1628-9CrossRefPubMed

Kukke SN, Triolo RJ (2004) The effects of trunk stimulation on bimanual seated workspace. IEEE Trans Neural Syst Rehabil Eng 12:177–185. https://doi.org/10.1109/TNSRE.2004.827222CrossRefPubMed

Lagerquist O, Mang CS, Collins DF (2012) Changes in spinal but not cortical excitability following combined electrical stimulation of the tibial nerve and voluntary plantar-flexion. Exp Brain Res 222:41–53. https://doi.org/10.1007/s00221-012-3194-5CrossRefPubMed

Mang CS, Lagerquist O, Collins DF (2010) Changes in corticospinal excitability evoked by common peroneal nerve stimulation depend on stimulation frequency. Exp Brain Res 203:11–20. https://doi.org/10.1007/s00221-010-2202-xCrossRefPubMed

Mang CS, Clair JM, Collins DF (2011) Neuromuscular electrical stimulation has a global effect on corticospinal excitability for leg muscles and a focused effect for hand muscles. Exp Brain Res 209:355–363. https://doi.org/10.1007/s00221-011-2556-8CrossRefPubMed

Milosevic M, Masani K, Kuipers MJ et al (2015a) Trunk control impairment is responsible for postural instability during quiet sitting in individuals with cervical spinal cord injury. Clin Biomech 30:507–512. https://doi.org/10.1016/j.clinbiomech.2015.03.002CrossRef

Milosevic M, Masani K, Wu N et al (2015b) Trunk muscle co-activation using functional electrical stimulation modifies center of pressure fluctuations during quiet sitting by increasing trunk stiffness. J Neuroeng Rehabil 12:1–9. https://doi.org/10.1186/s12984-015-0091-8CrossRef

Milosevic M, Yokoyama H, Grangeon M et al (2017) Muscle synergies reveal impaired trunk muscle coordination strategies in individuals with thoracic spinal cord injury. J Electromyogr Kinesiol 36:40–48. https://doi.org/10.1016/j.jelekin.2017.06.007CrossRefPubMed

Milosevic M, Masugi Y, Obata H et al (2019) Short-term inhibition of spinal reflexes in multiple lower limb muscles after neuromuscular electrical stimulation of ankle plantar flexors. Exp Brain Res 237:467–476. https://doi.org/10.1007/s00221-018-5437-6CrossRefPubMed

Milosevic M, Marquez-Chin C, Masani K et al (2020) Why brain-controlled neuroprosthetics matter: mechanisms underlying electrical stimulation of muscles and nerves in rehabilitation. Biomed Eng Online 19:1–30. https://doi.org/10.1186/s12938-020-00824-wCrossRef

Morita H, Olivier E, Baumgarten J et al (2000) Differential changes in corticospinal and Ia input to tibialis anterior and soleus motor neurones during voluntary contraction in man. Acta Physiol Scand 170:65–76. https://doi.org/10.1046/j.1365-201X.2000.00762.xCrossRefPubMed

Morse DT (1999) MINSIZE2: a computer program for determining effect size and minimum sample size for statistical significance for univariate, multivariate, and nonparametric tests. Educ Psychol Meas 59:518–531CrossRef

Obata H, Ogawa T, Kitamura T et al (2015) Short-term effect of electrical nerve stimulation on spinal reciprocal inhibition during robot-assisted passive stepping in humans. Eur J Neurosci 42:2283–2288. https://doi.org/10.1111/ejn.13000CrossRefPubMed

Palmer E, Ashby P (1992) Corticospinal projections to upper limb motoneurones in humans. J Physiol 448:397–412. https://doi.org/10.1113/jphysiol.1992.sp019048CrossRefPubMedPubMedCentral

Patel K, Milosevic M, Nakazawa K et al (2017) Wheelchair neuroprosthesis for improving dynamic trunk stability. IEEE Trans Neural Syst Rehabil Eng 25:2472–2479. https://doi.org/10.1109/TNSRE.2017.2727072CrossRefPubMed

Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389–443CrossRef

Porter LL, Sakamoto T, Asanuma H (1990) Morphological and physiological identification of neurons in the cat motor cortex which receive direct input from the somatic sensory cortex. Exp Brain Res 80:209–212. https://doi.org/10.1007/BF00228864CrossRefPubMed

Ridding MC, Brouwer B, Miles TS et al (2005) Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res 131:135–143CrossRef

Rosenthal R, Cooper H, Hedges L (1994) Parametric measures of effect size. Handb Res Synth 621:231–244

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 I.F.C.N. committee. Clin Neurophysiol 126:1071–1107. https://doi.org/10.1016/j.clinph.2015.02.001CrossRefPubMedPubMedCentral

Rothwell JC, Thompson PD, Day BL et al (1991) Stimulation of the human motor cortex through the scalp. Exp Physiol 76:159–200. https://doi.org/10.1113/expphysiol.1991.sp003485CrossRefPubMed

Rushton DN (2003) Functional electrical stimulation and rehabilitation—an hypothesis. Eur Rev Med Pharmacol Sci 25:75–78

Sasaki A, Milosevic M, Nakazawa K (2020) Cortical and subcortical neural interactions between trunk and upper-limb muscles in humans. Neuroscience 451:126–136. https://doi.org/10.1016/j.neuroscience.2020.10.011CrossRefPubMed

Sasaki A, Kaneko N, Masugi Y et al (2021) Task-and intensity-dependent modulation of arm-trunk neural interactions in the corticospinal pathway in humans. eNeuro 8:1–13. https://doi.org/10.1523/ENEURO.0111-21.2021CrossRef

Sayenko DG, Nguyen R, Popovic MR, Masani K (2014) Reducing muscle fatigue during transcutaneous neuromuscular electrical stimulation by spatially and sequentially distributing electrical stimulation sources. Eur J Appl Physiol 114:793–804. https://doi.org/10.1007/s00421-013-2807-4CrossRefPubMedPubMedCentral

Taylor JL (2006) Stimulation at the cervicomedullary junction in human subjects. J Electromyogr Kinesiol 16:215–223. https://doi.org/10.1016/j.jelekin.2005.07.001CrossRefPubMed

Taylor JL, Gandevia SC (2004) Noninvasive stimulation of the human corticospinal tract. J Appl Physiol 96:1496–1503. https://doi.org/10.1152/japplphysiol.01116.2003CrossRefPubMed

Taylor JL, Petersen NT, Butler JE, Gandevia SC (2002) Interaction of transcranial magnetic stimulation and electrical transmastoid stimulation in human subjects. J Physiol 541:949–958. https://doi.org/10.1113/jphysiol.2002.016782CrossRefPubMedPubMedCentral

Thompson AK, Stein RB (2004) Short-term effects of functional electrical stimulation on motor-evoked potentials in ankle flexor and extensor muscles. Exp Brain Res 159:491–500. https://doi.org/10.1007/s00221-004-1972-4CrossRef

Thompson AK, Lapallo B, Duffield M et al (2011) Repetitive common peroneal nerve stimulation increases ankle dorsiflexor motor evoked potentials in incomplete spinal cord lesions. Exp Brain Res 210:143–152. https://doi.org/10.1007/s00221-011-2607-1CrossRefPubMed

Triolo RJ, Boggs L, Miller ME et al (2009) Implanted electrical stimulation of the trunk for seated postural stability and function after cervical spinal cord injury: a single case study. Arch Phys Med Rehabil 90:340–347. https://doi.org/10.1016/j.apmr.2008.07.029CrossRefPubMedPubMedCentral

Ugawa Y, Uesaka Y, Terao Y et al (1994) Magnetic stimulation of corticospinal pathways at the foramen magnum level in humans. Ann Neurol 36:618–624. https://doi.org/10.1002/ana.410360410CrossRefPubMed

Zedka M, Prochazka A, Knight B et al (2004) Voluntary and reflex control of human back muscles during induced pain. J Physiol 520:591–604. https://doi.org/10.1111/j.1469-7793.1999.00591.xCrossRef

Title: Effects of trunk neuromuscular electrical stimulation on the motor circuits of able-bodied individuals
Authors: Atsushi Sasaki
Na Cao
Akiko Yuasa
Milos R. Popovic
Kimitaka Nakazawa
Matija Milosevic
Publication date: 01-04-2023
Publisher: Springer Berlin Heidelberg
Keywords: Motor Evoked Potential
Motor Evoked Potential
Nerve Stimulation
Electromyographic
Transcranial Magnetic Stimulation
Transcranial Magnetic Stimulation
Published in: Experimental Brain Research / Issue 4/2023
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-023-06585-x

Advances in Alzheimer's

Alzheimer's Disease
Independent Medical Education

Alzheimer's research and care is changing rapidly. Keep up with the latest developments from key international conferences, together with expert insights on how to integrate these advances into practice.

This content is intended for healthcare professionals outside of the UK.

Supported by:

Lilly

Developed by: Springer Healthcare IME

Learn more

ERS Congress 2024

Springer Medicine

Effects of trunk neuromuscular electrical stimulation on the motor circuits of able-bodied individuals

Abstract

Advances in Alzheimer's

ERS Congress 2024

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2023

Vestibular perceptual thresholds for rotation about the yaw, roll, and pitch axes

Faces, English words and Chinese characters: a study of dual-task interference in mono-and bilingual speakers

Investigating motor preparation in synchronous hand and foot movements under reactive vs. predictive control

Performance on the balloon analogue risk task and anticipatory response inhibition task is associated with severity of impulse control behaviours in people with Parkinson’s disease

Modulation of corticospinal excitability related to the forearm muscle during robot-assisted stepping in humans

Modulation of somatosensation by transcranial magnetic stimulation over somatosensory cortex: a systematic review

Advances in Alzheimer's