{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,7]],"date-time":"2026-03-07T14:05:13Z","timestamp":1772892313535,"version":"3.50.1"},"reference-count":28,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2021,10,2]],"date-time":"2021-10-02T00:00:00Z","timestamp":1633132800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Sensors"],"abstract":"<jats:p>Transcutaneous electrical spinal cord stimulation (tSCS) is a non-invasive neuromodulatory technique that has in recent years been linked to improved volitional limb control in spinal-cord injured individuals. Although the technique is growing in popularity there is still uncertainty regarding the neural mechanisms underpinning sensory and motor recovery. Brain monitoring techniques such as electroencephalography (EEG) may provide further insights to the changes in coritcospinal excitability that have already been demonstrated using other techniques. It is unknown, however, whether intelligible EEG can be extracted while tSCS is being applied, owing to substantial high-amplitude artifacts associated with stimulation-based therapies. Here, for the first time, we characterise the artifacts that manifest in EEG when recorded simultaneously with tSCS. We recorded multi-channel EEG from 21 healthy volunteers as they took part in a resting state and movement task across two sessions: One with tSCS delivered to the cervical region of the neck, and one without tSCS. An offline analysis in the time and frequency domain showed that tSCS manifested as narrow, high-amplitude peaks with a spectral density contained at the stimulation frequency. We quantified the altered signals with descriptive statistics\u2014kurtosis, root-mean-square, complexity, and zero crossings\u2014and applied artifact-suppression techniques\u2014superposition of moving averages, adaptive, median, and notch filtering\u2014to explore whether the effects of tSCS could be suppressed. We found that the superposition of moving averages filter was the most successful technique at returning contaminated EEG to levels statistically similar to that of normal EEG. In the frequency domain, however, notch filtering was more effective at reducing the spectral power contribution of stimulation from frontal and central electrodes. An adaptive filter was more appropriate for channels closer to the stimulation site. Lastly, we found that tSCS posed no detriment the binary classification of upper-limb movements from sensorimotor rhythms, and that adaptive filtering resulted in poorer classification performance. Overall, we showed that, depending on the analysis, EEG monitoring during transcutaneous electrical spinal cord stimulation is feasible. This study supports future investigations using EEG to study the activity of the sensorimotor cortex during tSCS, and potentially paves the way to brain\u2013computer interfaces operating in the presence of spinal stimulation.<\/jats:p>","DOI":"10.3390\/s21196593","type":"journal-article","created":{"date-parts":[[2021,10,10]],"date-time":"2021-10-10T21:37:49Z","timestamp":1633901869000},"page":"6593","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["EEG Monitoring Is Feasible and Reliable during Simultaneous Transcutaneous Electrical Spinal Cord Stimulation"],"prefix":"10.3390","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9993-3649","authenticated-orcid":false,"given":"Ciar\u00e1n","family":"McGeady","sequence":"first","affiliation":[{"name":"Centre for Rehabilitation Engineering, University of Glasgow, Glasgow G12 8QQ, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1585-3247","authenticated-orcid":false,"given":"Aleksandra","family":"Vu\u010dkovi\u0107","sequence":"additional","affiliation":[{"name":"Centre for Rehabilitation Engineering, University of Glasgow, Glasgow G12 8QQ, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3407-9226","authenticated-orcid":false,"given":"Yong-Ping","family":"Zheng","sequence":"additional","affiliation":[{"name":"Department of Biomedical Engineering, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0987-1999","authenticated-orcid":false,"given":"Monzurul","family":"Alam","sequence":"additional","affiliation":[{"name":"Department of Biomedical Engineering, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,10,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.rehab.2015.05.003","article-title":"Transcutaneous electrical spinal-cord stimulation in humans","volume":"58","author":"Gerasimenko","year":"2015","journal-title":"Ann. Phys. Rehabil. Med."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1272","DOI":"10.1109\/TNSRE.2018.2834339","article-title":"Transcutaneous Electrical Spinal Stimulation Promotes Long-Term Recovery of Upper Extremity Function in Chronic Tetraplegia","volume":"26","author":"Inanici","year":"2018","journal-title":"IEEE Trans. Neural Syst. Rehabil. Eng."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1109\/TNSRE.2021.3049133","article-title":"Transcutaneous spinal cord stimulation restores hand and arm function after spinal cord injury","volume":"29","author":"Inanici","year":"2021","journal-title":"IEEE Trans. Neural Syst. Rehabil. Eng."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2540","DOI":"10.1089\/neu.2017.5584","article-title":"Trunk Stability Enabled by Noninvasive Spinal Electrical Stimulation after Spinal Cord Injury","volume":"35","author":"Rath","year":"2018","journal-title":"J. Neurotrauma"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Hofstoetter, U.S., Freundl, B., Binder, H., and Minassian, K. (2018). Common neural structures activated by epidural and transcutaneous lumbar spinal cord stimulation: Elicitation of posterior root-muscle reflexes. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0192013"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2633","DOI":"10.1523\/JNEUROSCI.2374-19.2020","article-title":"Cortical and Subcortical Effects of Transcutaneous Spinal Cord Stimulation in Humans with Tetraplegia","volume":"40","author":"Benavides","year":"2020","journal-title":"J. Neurosci."},{"key":"ref_7","first-page":"1359","article-title":"Intensity and Dose of Neuromuscular Electrical Stimulation Influence Sensorimotor Cortical Excitability","volume":"14","author":"Omedes","year":"2021","journal-title":"Front. Neurosci."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Schestatsky, P., Morales-Quezada, L., and Fregni, F. (2013). Simultaneous EEG Monitoring During Transcranial Direct Current Stimulation. J. Vis. Exp. JoVE, 50426.","DOI":"10.3791\/50426"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"135","DOI":"10.3389\/fnhum.2016.00135","article-title":"Transcranial Alternating Current Stimulation with Sawtooth Waves: Simultaneous Stimulation and EEG Recording","volume":"10","author":"Dowsett","year":"2016","journal-title":"Front. Hum. Neurosci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2170","DOI":"10.1016\/j.clinph.2018.07.023","article-title":"Removing deep brain stimulation artifacts from the electroencephalogram: Issues, recommendations and an open-source toolbox","volume":"129","author":"Lio","year":"2018","journal-title":"Clin. Neurophysiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1425","DOI":"10.1109\/TBME.2014.2312397","article-title":"Brain\u2014Computer Interfaces Using Sensorimotor Rhythms: Current State and Future Perspectives","volume":"61","author":"Yuan","year":"2014","journal-title":"IEEE Trans. Biomed. Eng."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Kohli, S., and Casson, A.J. (2019). Removal of Gross Artifacts of Transcranial Alternating Current Stimulation in Simultaneous EEG Monitoring. Sensors, 19.","DOI":"10.3390\/s19010190"},{"key":"ref_13","unstructured":"Guggenberger, R. (2021, March 01). agricolab\/pyARtACS: Python Modules for Removal of Periodic Artifacts, Even when Non-Stationary and Non-Sinusoidal. Developed with Application for tACS-EEG in Mind. Available online: https:\/\/github.com\/agricolab\/pyARtACS."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1109\/86.593293","article-title":"Functional neuromuscular stimulation controlled by surface electromyographic signals produced by volitional activation of the same muscle: Adaptive removal of the muscle response from the recorded EMG-signal","volume":"5","author":"Sennels","year":"1997","journal-title":"IEEE Trans. Rehabil. Eng."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"21242","DOI":"10.1038\/s41598-020-77664-0","article-title":"Active proportional electromyogram controlled functional electrical stimulation system","volume":"10","author":"Osuagwu","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_16","unstructured":"Hari, R., and Puce, A. (2017). MEG-EEG Primer, Oxford University Press."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1109\/MSP.2008.4408441","article-title":"Optimizing Spatial filters for Robust EEG Single-Trial Analysis","volume":"25","author":"Blankertz","year":"2008","journal-title":"IEEE Signal Process. Mag."},{"key":"ref_18","first-page":"52","article-title":"Better than random? A closer look on BCI results","volume":"10","author":"Scherer","year":"2008","journal-title":"Int. J. Bioelectromagn."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2765","DOI":"10.1016\/j.clinph.2007.07.028","article-title":"EEG differences between eyes-closed and eyes-open resting conditions","volume":"118","author":"Barry","year":"2007","journal-title":"Clin. Neurophysiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1360","DOI":"10.1016\/j.clinph.2014.10.007","article-title":"Influence of motor imagination on cortical activation during functional electrical stimulation","volume":"126","author":"Reynolds","year":"2015","journal-title":"Clin. Neurophysiol."},{"key":"ref_21","first-page":"267","article-title":"MEG and EEG data analysis with MNE-Python","volume":"26","author":"Gramfort","year":"2013","journal-title":"Front. Neurosci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.jneumeth.2003.10.009","article-title":"EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis","volume":"134","author":"Delorme","year":"2004","journal-title":"J. Neurosci. Methods"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2145","DOI":"10.1089\/neu.2017.5461","article-title":"Non-Invasive Activation of Cervical Spinal Networks after Severe Paralysis","volume":"35","author":"Gad","year":"2018","journal-title":"J. Neurotrauma"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"3167","DOI":"10.1109\/TNSRE.2020.3048592","article-title":"Cervical Spinal Cord Transcutaneous Stimulation Improves Upper Extremity and Hand Function in People With Complete Tetraplegia: A Case Study","volume":"28","author":"Zhang","year":"2020","journal-title":"IEEE Trans. Neural Syst. Rehabil. Eng."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1177\/1545968315591706","article-title":"Spinal Rhythm Generation by Step-Induced Feedback and Transcutaneous Posterior Root Stimulation in Complete Spinal Cord\u2013Injured Individuals","volume":"30","author":"Minassian","year":"2016","journal-title":"Neurorehabilit. Neural Repair"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Meyer, C., Hofstoetter, U.S., Hubli, M., Hassani, R.H., Rinaldo, C., Curt, A., and Bolliger, M. (2020). Immediate Effects of Transcutaneous Spinal Cord Stimulation on Motor Function in Chronic, Sensorimotor Incomplete Spinal Cord Injury. J. Clin. Med., 9.","DOI":"10.3390\/jcm9113541"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1089\/neu.2019.6588","article-title":"Transcutaneous Spinal Cord Stimulation Induces Temporary Attenuation of Spasticity in Individuals with Spinal Cord Injury","volume":"37","author":"Hofstoetter","year":"2020","journal-title":"J. Neurotrauma"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1016\/j.neuroimage.2011.12.039","article-title":"Towards the utilization of EEG as a brain imaging tool","volume":"61","author":"Michel","year":"2012","journal-title":"NeuroImage"}],"container-title":["Sensors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1424-8220\/21\/19\/6593\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:08:48Z","timestamp":1760166528000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1424-8220\/21\/19\/6593"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,2]]},"references-count":28,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2021,10]]}},"alternative-id":["s21196593"],"URL":"https:\/\/doi.org\/10.3390\/s21196593","relation":{},"ISSN":["1424-8220"],"issn-type":[{"value":"1424-8220","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,10,2]]}}}