Evidence for motor learning in Parkinson's disease: acquisition, automaticity and retention of cued gait performance after training with external rhythmical cues
Open accessAbstract
People with Parkinson's disease (PD) have difficulty learning new motor skills. Evidence suggests external stimuli (cues) may enhance learning; however, this may be specific to cued rather than non-cued performance. We aimed to test effects of cued training on motor learning in PD. We defined motor learning as acquisition (single task), automaticity (dual task) and retention of single- and dual-task performance (follow-up). 153 subjects with PD received 3 weeks cued gait training as part of a randomised trial (the RESCUE trial). We measured changes in cued gait performance with three external rhythmical cues (ERC) (auditory, visual and somatosensory) during single and dual tasks after training and 6 weeks follow-up. Gait was tested without cues to compare specificity of learning (transfer). Subjects were 'on' medication and were cued at preferred step frequency during assessment. Accelerometers recorded gait and walking speed, step length and step frequency were determined from raw data. Data were analysed with SAS using linear regression models. Walking speed and step length significantly increased with all cues after training during both single- and dual-task gait and these effects were retained. Training effects were not specific to cued gait and were observed in dual-task step length, and walking speed however was more limited in single-task non-cued gait. These results support the use of ERC to enhance motor learning in PD as defined by increased acquisition, automaticity and retention. They also highlight the potential for sustained improvement in walking and complex task performance.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Age, cognition, and disease severity could impact exercise effects on motor skill learning.
“Other factors that could impact exercise effects on motor skill learning include age, cognition, and disease severity 35.”
From Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson's disease (2013) · cites this paper as [35]
Different cueing modalities increase retention of learning in Parkinson's disease.
“and increase retention of learning in PD [9, 10].”
Cites
Functional MRI evidence for adult motor cortex plasticity during motor skill learning
Kami, A., Meyer, G., Jezzard, P., Adams, M. M., Turner, R., & Ungerleider, L. G. (1995) · Nature · doi:10.1038/377155a0 · Cited by 1,883 · see citing works
Stride length regulation in Parkinson's disease
Morris, M. E., Iansek, R., Matyas, T. A., & Summers, J. J. (1996) · Brain · doi:10.1093/brain/119.2.551 · Cited by 879 · see citing works
Cueing training in the home improves gait-related mobility in Parkinson's disease: the RESCUE trial
Nieuwboer, A., Kwakkel, G., Rochester, L., Jones, D., van Wegen, E., Willems, A. M., Chavret, F., Hetherington, V, Baker, K., & Lim, I. (2007) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.200x.097923 · Cited by 857 · see citing works
Self-citationRhythmic auditory stimulation in gait training for Parkinson's disease patients
Thaut, M. H., McIntosh, G. C., Rice, R. R., Miller, R. A., Rathbun, J., & Brault, J. M. (1996) · Movement Disorders · doi:10.1002/mds.870110213 · Cited by 839 · see citing works
Motor Learning and Performance
Schmidt, R. A., & Wrisberg, C. A. (1991) · Cited by 668 · see citing works
Anatomy of motor learning. I. Frontal cortex and attention to action
Jueptner, M., Stephan, K. M., Frith, C. D., Brooks, D. J., Frackowiak, R. S. J., & Passingham, R. E. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.3.1313 · Cited by 624 · see citing works
Lim, I., van Wegen, E. E. H., de Goede, C. J. T., Deutekom, M. D. L. F., Nieuwboer, A., Willems, A., Jones, D. E., Rochester, L., & Kwakkel, G. (2005) · Clinical Rehabilitation · doi:10.1191/0269215505cr906oa · Cited by 494 · see citing works
Self-citationRhythmic auditory stimulation modulates gait variability in Parkinson’s disease
Hausdorff, J. M., Lowenthal, J., Herman, T., Gruendlinger, L., Peretz, C., & Giladi, N. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05810.x · Cited by 489 · see citing works
A functional MRI study of automatic movements in patients with Parkinson's disease
Wu, T., & Hallett, M. (2005) · Brain · doi:10.1093/brain/awh569 · Cited by 483 · see citing works
O’Shea, S. D., Morris, M. E., & Iansek, R. (2002) · Physical Therapy · doi:10.1093/ptj/82.9.888 · Cited by 479 · see citing works
Rubinstein, T. C., Giladi, N., & Hausdorff, J. M. (2002) · Movement Disorders · doi:10.1002/mds.10259 · Cited by 364 · see citing works
Rochester, L., Hetherington, V., Jones, D., Nieuwboer, A., Willems, A.-M., Kwakkel, G., & Van Wegen, E. (2004) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2004.01.025 · Cited by 317 · see citing works
Self-citationRochester, L., Hetherington, V., Jones, D. E., Nieuwboer, A., Willems, A., Kwakkel, G., & van Wegen, E. E. H. (2005) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2004.10.040 · Cited by 265 · see citing works
Self-citationGoal-directed secondary motor tasks: Their effects on gait in subjects with Parkinson disease
Bond, J. M., & Morris, M. E. (2000) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/s0003-9993(00)90230-2 · Cited by 232 · see citing works
Neural correlates of dual task performance in patients with Parkinson's disease
Wu, T., & Hallett, M. (2007) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2007.126599 · Cited by 222 · see citing works
Attention to movement modulates activity in sensori-motor areas, including primary motor cortex
Johansen‐Berg, H., & Matthews, P. M. (2002) · Experimental Brain Research · doi:10.1007/s00221-001-0905-8 · Cited by 206 · see citing works
Farley, B. G., & Koshland, G. F. (2005) · Experimental Brain Research · doi:10.1007/s00221-005-0179-7 · Cited by 195 · see citing works
Motor sequence learning and movement disorders
Doyon, J. (2008) · Current Opinion in Neurology · doi:10.1097/wco.0b013e328304b6a3 · Cited by 194 · see citing works
Doyon, J., Laforce, R. J., Bouchard, G., Gaudreau, D., Roy, J., Poirier, M., Bédard, P. J., Bédard, F., & Bouchard, J.-P. (1998) · Neuropsychologia · doi:10.1016/s0028-3932(97)00168-1 · Cited by 192 · see citing works
Baker, K., Rochester, L., & Nieuwboer, A. (2007) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2007.07.026 · Cited by 191 · see citing works
Self-citationIs implicit sequence learning impaired in Parkinson's disease? A meta-analysis.
Siegert, R. J., Taylor, K. D., Weatherall, M., & Abernethy, D. A. (2006) · Neuropsychology · doi:10.1037/0894-4105.20.4.490 · Cited by 177 · see citing works
Motor procedural learning in Parkinson's disease
Muslimović, D., Post, B., Speelman, J. D., & Schmand, B. A. (2007) · Brain · doi:10.1093/brain/awm211 · Cited by 163 · see citing works
Rochester, L., Nieuwboer, A., Baker, K., Hetherington, V., Willems, A.-M., Chavret, F., Kwakkel, G., Van Wegen, E., Lim, I., & Jones, D. (2007) · Journal of Neural Transmission · doi:10.1007/s00702-007-0756-y · Cited by 150 · see citing works
Self-citationStephan, K. M., Thaut, M. H., Wunderlich, G., Schicks, W., Tian, B., Tellmann, L., Schmitz, T. W., Herzog, H. R., McIntosh, G. C., Seitz, R., et al. (2002) · NeuroImage · doi:10.1006/nimg.2001.0929 · Cited by 136 · see citing works
Timing precision in continuation and synchronization tapping
Semjen, A., Schulze, H.-H., & Vorberg, D. (2000) · Psychological Research · doi:10.1007/pl00008172 · Cited by 134 · see citing works
Baker, K., Rochester, L., & Nieuwboer, A. (2007) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2007.09.008 · Cited by 113 · see citing works
Self-citationChanges in the Human Brain during Rhythm Learning
Ramnani, N., & Passingham, R. E. (2001) · Journal of Cognitive Neuroscience · doi:10.1162/089892901753165863 · Cited by 108 · see citing works
Verschueren, S. M. P., Swinnen, S. P., Dom, R., & De Weerdt, W. (1997) · Experimental Brain Research · doi:10.1007/pl00005602 · Cited by 96 · see citing works
Mak, K. Y., & Hui-Chan, C. W. Y. (2007) · Movement Disorders · doi:10.1002/mds.21509 · Cited by 92 · see citing works
Effects of Long-Term Gait Training Using Visual Cues in an Individual With Parkinson Disease
Sidaway, B., Anderson, J. B., Danielson, G., Martin, L., & Smith, G. R. (2006) · Physical Therapy · doi:10.1093/ptj/86.2.186 · Cited by 83 · see citing works
The striatum and probabilistic implicit sequence learning
Wilkinson, L., & Jahanshahi, M. (2006) · Brain Research · doi:10.1016/j.brainres.2006.12.051 · Cited by 75 · see citing works
Concurrent validity of accelerometry to measure gait in Parkinsons Disease
Lord, S., Rochester, L., Baker, K., & Nieuwboer, A. (2008) · Gait & Posture · doi:10.1016/j.gaitpost.2007.04.001 · Cited by 69 · see citing works
Self-citationJessop, R. T., Horowicz, C., & Dibble, L. E. (2006) · Neurorehabilitation and neural repair · doi:10.1177/1545968306287107 · Cited by 69 · see citing works
Facilitation of motor imagery through movement-related cueing
Heremans, E., Helsen, W. F., de Poel, H. J., Alaerts, K., Meyns, P., & Feys, P. (2009) · Brain Research · doi:10.1016/j.brainres.2009.04.041 · Cited by 68 · see citing works
Masuhr, F., Wissel, J., M�ller, J., Scholz, U., & Poewe, W. H. (2000) · Movement Disorders · doi:10.1002/1531-8257(200009)15:5 · Cited by 54 · see citing works
The Rationale For Motor Learning In Parkinson'S Disease
Abbruzzese, G., Trompetto, C., Marinelli, L., et al. (2009) · PubMed · doi:10.5281/zenodo.1312821 · Cited by 53 · see citing works
Functional imaging of sequence learning in Parkinson's disease
Carbon, M., & Eidelberg, D. (2006) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2006.05.005 · Cited by 47 · see citing works
Mentis, M. J., DHAWAN, V. M., Feigin, A., Delalot, D., Zgaljardic, D. J., Edwards, C., & Eidelberg, D. (2003) · Human Brain Mapping · doi:10.1002/hbm.10142 · Cited by 47 · see citing works
Motor learning of hands with auditory cue in patients with Parkinson’s disease
Chuma, T., Reza, F., Ikoma, K., & Mano, Y. (2005) · Journal of Neural Transmission · doi:10.1007/s00702-005-0314-4 · Cited by 44 · see citing works
Learning and retention of movement sequences in Parkinson's disease
Smiley‐Oyen, A. L., Lowry, K. A., & Emerson, Q. R. (2006) · Movement Disorders · doi:10.1002/mds.20906 · Cited by 42 · see citing works
Cueing Gait and Gait-related Mobility in Patients With Parkinson's Disease
Nieuwboer, A., Rochester, L., & Jones, D. E. (2008) · Topics in Geriatric Rehabilitation · doi:10.1097/01.tgr.0000318902.80066.ae · Cited by 21 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson's disease
Petzinger, G. M., Fisher, B. E., McEwen, S., Beeler, J. A., Walsh, J. P., & Jakowec, M. W. (2013) · The Lancet Neurology · doi:10.1016/s1474-4422(13)70123-6 · Cited by 798 · see citing works
Mirelman, A., Maidan, I., Herman, T., Deutsch, J. E., Giladi, N., & Hausdorff, J. M. (2011) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glq201 · Cited by 418 · see citing works
Pompeu, J. E., Mendes, F. A. D. S., Silva, K. G. D., Lobo, A. M., Oliveira, T. D. P., Zomignani, A. P., & Piemonte, M. E. P. (2012) · Physiotherapy · doi:10.1016/j.physio.2012.06.004 · Cited by 354 · see citing works
Ginis, P., Nieuwboer, A., Dorfman, M., Ferrari, A., Gazit, E., Canning, C. G., Rocchi, L., Chiari, L., Hausdorff, J. M., & Mirelman, A. (2016) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2015.11.004 · Cited by 225 · see citing works
Self-citationClinician versus machine: Reliability and responsiveness of motor endpoints in Parkinson's disease
Heldman, D. A., Espay, A. J., LeWitt, P. A., & Giuffrida, J. P. (2014) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2014.02.022 · Cited by 156 · see citing works
A wearable system for gait training in subjects with Parkinson's disease
Casamassima, F., Ferrari, A., Milosevic, B., Ginis, P., Farella, E., & Rocchi, L. (2014) · Sensors · doi:10.3390/s140406229 · Cited by 131 · see citing works
Allen, N. E., Sherrington, C., Suriyarachchi, G. D., Paul, S. S., Song, J., & Canning, C. G. (2012) · Parkinson's Disease · doi:10.1155/2012/854328 · Cited by 110 · see citing works
- Authors
- Rochester, L., Baker, K., Hetherington, V., Jones, D., Willems, A.-M., Kwakkel, G., Van Wegen, E., Lim, I., & Nieuwboer, A.
- Affiliations
- Northumbria University (GB)
- KU Leuven (BE)
- Vrije Universiteit Amsterdam (NL)
- Corresponding author
- Rochester, Lynn
- ORCID
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 2010-03
- Volume
- 1319
- Pages
- 103-111
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W2145386284
- Cited by
- 211
- References
- 41
- Citations by year
- 2026: 8 · 2025: 7 · 2024: 6 · 2023: 10 · 2022: 10 · 2021: 11 · 2020: 13 · 2019: 18 · 2018: 13 · 2017: 11 · 2016: 19 · 2015: 16 · 2014: 28 · 2013: 13 · 2012: 12
- FWCI
- 32.72
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- VU Research Portal (publishedVersion)
- Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
- Northumbria Research Link (Northumbria University) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Newcastle University ePrints (Newcastle Univesity)
- Funders
- National Institute for Health and Care Research
- European Commission
- Topics
- Health Sciences › Health Professions › Physical Therapy, Sports Therapy and Rehabilitation › Balance, Gait, and Falls Prevention
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Health Sciences › Medicine › Rehabilitation › Stroke Rehabilitation and Recovery
- Keywords
- Parkinson's disease, motor learning, auditory cues, visual cues, somatosensory cues, dual-task performance, transfer of learning, walking speed, step length, cadence, gait training
- MeSH terms
- Acoustic Stimulation, Aged, Antiparkinson Agents, Biomechanical Phenomena, Cues, Female, Follow-Up Studies, Gait, Humans, Learning, Male, Memory, Motor Skills, Parkinson Disease, Periodicity, Photic Stimulation, Physical Stimulation, Practice, Psychological, Time Factors, Linear Models, Walking
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