Effects of rhythmic-cued gait training on gait-like task related brain activation in people with multiple sclerosis
Open accessAbstract
BACKGROUND: Walking impairment is one of the most debilitating symptoms of multiple sclerosis (MS). A better understanding of brain mechanisms underlying successful gait training could help to improve development of targeted therapy. We therefore investigated changes in brain activation associated with improvements in walking function after rhythmic-cued gait training. METHODS: Thirty-one people with MS (pwMS; median EDSS = 2.5, range:2.0-5.0) and 17 age- and sex-matched healthy controls (HC) completed behavioural and MRI assessments at baseline and post-intervention (four weeks after baseline). All included pwMS received a four-week actual and/or imagined gait training with rhythmic-auditory cueing, while HC received no intervention. All participants performed a bipedal ankle plantar- and dorsiflexion and a corresponding motor-imagery task during fMRI. PwMS displaying a > 5 % walking distance increase in the 2-Minute Walk Test (2MWT) from baseline to post-intervention were defined as responders. RESULTS: Responders did not differ from non-responders in terms of demographics, clinical variables, and walking function at baseline. Responders, non-responders, and HC showed similar movement-related brain activation at baseline. At post-intervention, responders showed decreased brain activation within the premotor cortex, precuneus, and middle frontal gyrus during the movement task. Stronger decreases within these areas were associated with higher walking function improvements in all pwMS after controlling for potential confounders. No association was observed between walking function and motor imagery-related brain activation changes. CONCLUSION: Improved walking function after rhythmic-cued gait training was associated with reduced brain activation in motor planning and attention areas. This suggests a more efficient recruitment of areas subserving motor function after successful training.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Enhanced FC between the precentral gyrus and MFG is an important indicator of cerebral functional adaptation.
“Furthermore, studies involving interventions on limb motor function through brain–computer interfaces or motor training have identified enhanced FC between these regions as an important indicator of cerebral functional adaptation.[38,39]”
From Brain Rewires to Stabilize Walking During Visual Impairment · cites this paper as [39]
The Results (§3.3) report changes in task-related activation in the MFG and premotor cortex, and the Discussion (§4) interprets activation decreases as possible adaptive changes. A search for functional connectivity between the precentral gyrus and MFG found no passage identifying enhanced connectivity between them as an indicator of adaptation. Activation in separate regions does not establish connectivity between them. (LLM, conf=0.76)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS)
Kurtzke, J. F. (1983) · Neurology · doi:10.1212/wnl.33.11.1444 · Cited by 15,011 · see citing works
Advances in functional and structural MR image analysis and implementation as FSL
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E. J., Johansen-Berg, H., Bannister, P. R., De Luca, M., Drobnjak, I., Flitney, D. E., et al. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.07.051 · Cited by 13,630 · see citing works
Jenkinson, M., Beckmann, C. F., Behrens, T. E. J., Woolrich, M. W., & Smith, S. M. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.09.015 · Cited by 11,314 · see citing works
ATS Statement: Guidelines for the Six-Minute Walk Test
(2002) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.166.1.at1102 · Cited by 11,195 · see citing works
Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria
Thompson, A. J., Banwell, B. L., Barkhof, F., Carroll, W. M., Coetzee, T., Comi, G., Correale, J., Fazekas, F., Filippi, M., Freedman, M. S., et al. (2018) · The Lancet Neurology · doi:10.1016/s1474-4422(17)30470-2 · Cited by 8,167 · see citing works
Self-citationPower, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.018 · Cited by 7,429 · see citing works
What we can do and what we cannot do with fMRI
Logothetis, N. K. (2008) · Nature · doi:10.1038/nature06976 · Cited by 3,612 · see citing works
Accurate, Robust, and Automated Longitudinal and Cross-Sectional Brain Change Analysis
Smith, S. M., Zhang, Y., Jenkinson, M., Chen, J. M., Matthews, P. M., Federico, A., & Stefano, N. D. (2002) · NeuroImage · doi:10.1006/nimg.2002.1040 · Cited by 2,013 · see citing works
Multilevel linear modelling for FMRI group analysis using Bayesian inference
Woolrich, M. W., Behrens, T. E. J., Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.12.023 · Cited by 1,719 · see citing works
Development of a multiple sclerosis functional composite as a clinical trial outcome measure
Cutter, G. (1999) · Brain · doi:10.1093/brain/122.5.871 · Cited by 1,191 · see citing works
Wallin, M. T., Culpepper, W. J., Nichols, E., Bhutta, Z. A., Gebrehiwot, T. T., Hay, S. I., Khalil, I. A., Krohn, K. J., Liang, X., Naghavi, M., et al. (2019) · The Lancet Neurology · doi:10.1016/s1474-4422(18)30443-5 · Cited by 1,108 · see citing works
Recent progress and outstanding issues in motion correction in resting state fMRI
Power, J. D., Schlaggar, B. L., & Petersen, S. E. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2014.10.044 · Cited by 957 · see citing works
The neural network of motor imagery: An ALE meta-analysis
Hétu, S., Grégoire, M., Saimpont, A., Coll, M., Eugène, F., Michon, P., & Jackson, P. L. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.017 · Cited by 900 · see citing works
NIH Toolbox for Assessment of Neurological and Behavioral Function
Gershon, R. C., Wagster, M. V., Hendrie, H. C., Fox, N. A., Cook, K. F., & Nowinski, C. J. (2013) · Neurology · doi:10.1212/wnl.0b013e3182872e5f · Cited by 895 · see citing works
Handbook of Functional MRI Data Analysis
Poldrack, R. A., Mumford, J. A., & Nichols, T. E. (2011) · Cambridge University Press eBooks · doi:10.1017/cbo9780511895029 · Cited by 729 · see citing works
Jakimovski, D., Bittner, S., Zivadinov, R., Morrow, S. A., Benedict, R. H. B., Zipp, F., & Weinstock‐Guttman, B. (2023) · The Lancet · doi:10.1016/s0140-6736(23)01473-3 · Cited by 645 · see citing works
Siegel, J. S., Power, J. D., Dubis, J. W., Vogel, A. C., Church, J. A., Schlaggar, B. L., & Petersen, S. E. (2014) · Human Brain Mapping · doi:10.1002/hbm.22307 · Cited by 546 · see citing works
Neurobiological foundations of neurologic music therapy: rhythmic entrainment and the motor system
Thaut, M. H., McIntosh, G. C., & Hoemberg, V. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.01185 · Cited by 500 · see citing works
The role of anterior cingulate cortex and precuneus in the coordination of motor behaviour
Wenderoth, N., Debaere, F., Sunaert, S. G., & Swinnen, S. P. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04176.x · Cited by 342 · see citing works
Evaluating and reducing the impact of white matter lesions on brain volume measurements
Battaglini, M., Jenkinson, M., & Stefano, N. D. (2011) · Human Brain Mapping · doi:10.1002/hbm.21344 · Cited by 327 · see citing works
Multiple roles of motor imagery during action observation
Vogt, S., Rienzo, F. D., Collet, C., Collins, A. F., & Guillot, A. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00807 · Cited by 301 · see citing works
Rehabilitation for people with multiple sclerosis: an overview of Cochrane Reviews
Amatya, B., Khan, F., & Galea, M. P. (2019) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd012732.pub2 · Cited by 273 · see citing works
Baert, I., Freeman, J., Smedal, T., Dalgas, U., Romberg, A., Kalron, A., Conyers, H., Elorriaga, I., Gebara, B., Gumse, J., et al. (2014) · Neurorehabilitation and Neural Repair · doi:10.1177/1545968314521010 · Cited by 213 · see citing works
Wiendl, H., Gold, R., Berger, T., Derfuss, T. J., Linker, R. A., Mäurer, M., Aktaş, O., Baum, K., Berghoff, M., Bittner, S., et al. (2021) · Therapeutic Advances in Neurological Disorders · doi:10.1177/17562864211039648 · Cited by 198 · see citing works
Self-citationComparison of the 2- and 6-minute walk test in multiple sclerosis
Gijbels, D., Eijnde, B. O., & Feys, P. (2011) · Multiple Sclerosis Journal · doi:10.1177/1352458511408475 · Cited by 190 · see citing works
Learmonth, Y. C., Dlugonski, D., Pilutti, L. A., Sandroff, B. M., & Motl, R. W. (2013) · Multiple Sclerosis Journal · doi:10.1177/1352458513483890 · Cited by 158 · see citing works
Brain Activity Changes Associated With Treadmill Training After Stroke
Enzinger, C., Dawes, H., Johansen‐Berg, H., Wade, D. T., Bogdanovic, M. D., Collett, J., Guy, C., Kischka, U., Ropele, S., Fazekas, F., et al. (2009) · Stroke · doi:10.1161/strokeaha.109.550053 · Cited by 154 · see citing works
Self-citationAuditory rhythmic cueing in movement rehabilitation: findings and possible mechanisms
Schaefer, R. S. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0402 · Cited by 139 · see citing works
The relationship between the use of kinaesthetic imagery and different visual imagery perspectives
Callow, N., & Hardy, L. (2004) · Journal of Sports Sciences · doi:10.1080/02640410310001641449 · Cited by 129 · see citing works
Functional MRI Correlates of Lower Limb Function in Stroke Victims With Gait Impairment
Enzinger, C., Johansen‐Berg, H., Dawes, H., Bogdanovic, M. D., Collett, J., Guy, C., Ropele, S., Kischka, U., Wade, D. T., Fazekas, F., et al. (2008) · Stroke · doi:10.1161/strokeaha.107.501999 · Cited by 109 · see citing works
Self-citationRocca, M. A., Schoonheim, M. M., Valsasina, P., Geurts, J. J. G., & Filippi, M. (2022) · NeuroImage Clinical · doi:10.1016/j.nicl.2022.103076 · Cited by 99 · see citing works
Self-citationTavazzi, E., Bergsland, N., Cattaneo, D., Gervasoni, E., Laganà, M. M., Dipasquale, O., Grosso, C., Saibene, F. L., Baglio, F., & Rovaris, M. (2018) · Journal of Neurology · doi:10.1007/s00415-018-8859-y · Cited by 76 · see citing works
Beyond clinical changes: Rehabilitation-induced neuroplasticity in MS
Prosperini, L., & Filippo, M. D. (2019) · Multiple Sclerosis Journal · doi:10.1177/1352458519846096 · Cited by 75 · see citing works
Relating Brain Damage to Brain Plasticity in Patients With Multiple Sclerosis
Tomassini, V., Johansen‐Berg, H., Jbabdi, S., Wise, R. G., Pozzilli, C., Palace, J. A., & Matthews, P. M. (2012) · Neurorehabilitation and neural repair · doi:10.1177/1545968311433208 · Cited by 72 · see citing works
Functional magnetic resonance imaging: an introduction to methods
Jellinger, K. A. (2003) · European Journal of Neurology · doi:10.1046/j.1468-1331.2003.00657.x · Cited by 70 · see citing works
Which symptoms contribute the most to patients’ perception of health in multiple sclerosis?
Green, R. R., Cutter, G., Friendly, M., & Kister, I. (2017) · Multiple Sclerosis Journal - Experimental Translational and Clinical · doi:10.1177/2055217317728301 · Cited by 67 · see citing works
Brain mapping in multiple sclerosis: Lessons learned about the human brain
Filippi, M., Preziosa, P., & Rocca, M. A. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.09.021 · Cited by 62 · see citing works
Self-citationSeebacher, B., Kuisma, R., Glynn, A., & Berger, T. (2016) · Multiple Sclerosis Journal · doi:10.1177/1352458516644058 · Cited by 57 · see citing works
Self-citationSystematic Review on Exercise Training as a Neuroplasticity-Inducing Behavior in Multiple Sclerosis
Sandroff, B. M., Jones, C. D., Baird, J. F., & Motl, R. W. (2020) · Neurorehabilitation and neural repair · doi:10.1177/1545968320921836 · Cited by 56 · see citing works
Interactive Rhythmic Cue Facilitates Gait Relearning in Patients with Parkinson's Disease
Uchitomi, H., Ota, L., Ogawa, K., Orimo, S., & Miyake, Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072176 · Cited by 49 · see citing works
Rocca, M. A., Gatti, R., Agosta, F., Broglia, P., Rossi, P., Riboldi, E., Corti, M., Comi, G., & Filippi, M. (2009) · Journal of Neurology · doi:10.1007/s00415-009-0116-y · Cited by 38 · see citing works
Self-citationLabriffe, M., Annweiler, C., Amirova, L. E., Gauquelin‐Koch, G., Minassian, A. T., Leiber, L., Beauchet, O., Custaud, M., & Dinomais, M. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00106 · Cited by 37 · see citing works
Tavazzi, E., Cazzoli, M., Pirastru, A., Blasi, V., Rovaris, M., Bergsland, N., & Baglio, F. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.707675 · Cited by 37 · see citing works
Bonzano, L., Pedullà, L., Tacchino, A., Brichetto, G., Battaglia, M. A., Mancardi, G., & Bove, M. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.05.004 · Cited by 33 · see citing works
Motor Imagery as a Function of Disease Severity in Multiple Sclerosis: An fMRI Study
Tacchino, A., Saiote, C., Brichetto, G., Bommarito, G., Roccatagliata, L., Cordano, C., Battaglia, M. A., Mancardi, G., & Inglese, M. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00628 · Cited by 32 · see citing works
Seebacher, B., Kuisma, R., Glynn, A., & Berger, T. (2018) · Multiple Sclerosis Journal · doi:10.1177/1352458518795332 · Cited by 31 · see citing works
Self-citationMotor programme activating therapy influences adaptive brain functions in multiple sclerosis
Řasová, K., Procházková, M., Tintěra, J., Ibrahim, I., Zimová, D., & Štětkářová, I. (2014) · International Journal of Rehabilitation Research · doi:10.1097/mrr.0000000000000090 · Cited by 30 · see citing works
Rocca, M. A., Preziosa, P., & Filippi, M. (2018) · Expert Review of Neurotherapeutics · doi:10.1080/14737175.2019.1555038 · Cited by 28 · see citing works
Self-citationInteractive cueing with walk-Mate for Hemiparetic Stroke Rehabilitation
Takeshi, M. U. T. O., Herzberger, B., Hermsdoerfer, J., et al. (2012) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/1743-0003-9-58 · Cited by 27 · see citing works
Péran, P., Nemmi, F., Dutilleul, C., Finamore, L., Caravasso, C. F., Troisi, E., Iosa, M., Sabatini, U., & Grasso, M. G. (2020) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2020.102127 · Cited by 26 · see citing works
Strik, M., Shanahan, C. J., van der Walt, A., et al. (2021) · Human Brain Mapping · doi:10.1002/hbm.25389 · Cited by 15 · see citing works
Zuber, P., Tsagkas, C., Papadopoulou, A., Gaetano, L., Huerbin, M., Geiter, E., Altermatt, A., Parmar, K., Ettlin, T. M., Schuster‐Amft, C., et al. (2020) · Journal of Neurology · doi:10.1007/s00415-020-09768-6 · Cited by 14 · see citing works
Sandroff, B. M., Rafizadeh, C. M., & Motl, R. W. (2023) · Sensors · doi:10.3390/s23094530 · Cited by 11 · see citing works
Motor imagery has a priming effect on motor execution in people with multiple sclerosis
Tacchino, A., Pedullà, L., Podda, J., Bragadin, M. M., Battaglia, M. A., Bisio, A., Bove, M., & Brichetto, G. (2023) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2023.1179789 · Cited by 11 · see citing works
Rocca, M. A., Romanò, F., Tedone, N., & Filippi, M. (2024) · Journal of Neurology · doi:10.1007/s00415-024-12395-0 · Cited by 10 · see citing works
Self-citationSeebacher, B., Helmlinger, B., Pinter, D., Ehling, R., Hegen, H., Ropele, S., Reishofer, G., Enzinger, C., Brenneis, C., & Deisenhammer, F. (2022) · BMJ Open · doi:10.1136/bmjopen-2021-056666 · Cited by 8 · see citing works
Self-citationSeebacher, B., Helmlinger, B., Pinter, D., et al. (2024) · Neurorehabilitation and neural repair · doi:10.1177/15459683241260724 · Cited by 8 · see citing works
Self-citationHechenberger, S., Helmlinger, B., Tinauer, C., et al. (2024) · Journal of Neurology · doi:10.1007/s00415-024-12274-8 · Cited by 6 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- M.H. Thaut, Rhythm, Music, and the Brain, Routledge, New York, 2007, https:// doi.org/10.4324/9780203958827. Epub ahead of print 2007. · DOI
Cited by
Sorted by citations
(n.d.) · Chinese Medical Journal / Neuroscience News · doi:10.1097/cm9.0000000000004040
“[38,39] In the current study, insufficient optical flow likely required the brain to recruit greater motor planning and attentional resources.”
- Authors
- Helmlinger, B., Seebacher, B., Ropele, S., Hechenberger, S., Heschl, B., Reishofer, G., Jordan, S., Tinauer, C., Wurth, S., Valsasina, P., Rocca, M. A., Filippi, M., Ehling, R., Reindl, M., Khalil, M., Deisenhammer, F., Brenneis, C., Enzinger, C., & Pinter, D.
- Affiliations
- Medical University of Graz (AT)
- Innsbruck Medical University (AT)
- IRCCS Ospedale San Raffaele (IT)
- Vita-Salute San Raffaele University (IT)
- Corresponding author
- Pinter, Daniela
- ORCID
- Helmlinger, Birgit
- Seebacher, Barbara
- Ropele, Stefan
- Hechenberger, Stefanie
- Heschl, Bettina
- Reishofer, Gernot
- Tinauer, Christian
- Wurth, Sebastian
- Valsasina, Paola
- Rocca, Maria Assunta
- Filippi, Massimo
- Ehling, Rainer
- Reindl, Markus
- Khalil, Michael
- Deisenhammer, Florian
- Brenneis, Christian
- Enzinger, Christian
- Pinter, Daniela
- Venue
- Journal of the Neurological Sciences
- Publisher
- Elsevier BV
- Published
- 2025-04
- Volume
- 471
- Pages
- 123426
- ISSN
- 0022-510X (ISSN-L)
- OpenAlex
- W4407397854
- Cited by
- 4
- References
- 58
- Citations by year
- 2026: 3 · 2025: 1
- FWCI
- 2.64
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of the Neurological Sciences (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Archivio Istituzionale della Ricerca - Università Vita-Salute San Raffaele (submittedVersion, cc-by)
- Funders
- Bristol-Myers Squibb Company (NA-CL-MS-PI-13909)
- Austrian Academy of Sciences
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Health Sciences › Medicine › Rehabilitation › Stroke Rehabilitation and Recovery
- Health Sciences › Health Professions › Physical Therapy, Sports Therapy and Rehabilitation › Balance, Gait, and Falls Prevention
- Keywords
- multiple sclerosis, gait training, rhythmic auditory cueing, motor imagery, brain activation, gait disturbance, premotor cortex, precuneus, middle frontal gyrus, motor planning, attention, treatment response, ankle dorsiflexion, plantar flexion
- MeSH terms
- Adult, Brain, Cues, Exercise Therapy, Female, Gait, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Multiple Sclerosis, Walking, Treatment Outcome, Gait Disorders, Neurologic
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review