Gait improvement via rhythmic stimulation in Parkinson's disease is linked to rhythmic skills

Simone Dalla Bella, Charles-Etienne Benoit, Nicolas Farrugia, Peter E Keller, Hellmuth Obrig, Stefan Mainka, Sonja A Kotz, Simone Dalla Bella, Charles-Etienne Benoit, Nicolas Farrugia, Peter E Keller, Hellmuth Obrig, Stefan Mainka, Sonja A Kotz

Abstract

Training based on rhythmic auditory stimulation (RAS) can improve gait in patients with idiopathic Parkinson's disease (IPD). Patients typically walk faster and exhibit greater stride length after RAS. However, this effect is highly variable among patients, with some exhibiting little or no response to the intervention. These individual differences may depend on patients' ability to synchronize their movements to a beat. To test this possibility, 14 IPD patients were submitted to RAS for four weeks, in which they walked to music with an embedded metronome. Before and after the training, patients' synchronization was assessed with auditory paced hand tapping and walking to auditory cues. Patients increased gait speed and stride length in non-cued gait after training. However, individual differences were apparent as some patients showed a positive response to RAS and others, either no response, or a negative response. A positive response to RAS was predicted by the synchronization performance in hand tapping and gait tasks. More severe gait impairment, low synchronization variability, and a prompt response to a stimulation change foster a positive response to RAS training. Thus, sensorimotor timing skills underpinning the synchronization of steps to an auditory cue may allow predicting the success of RAS in IPD.

Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1. Individual gait performances in non-cued…
Figure 1. Individual gait performances in non-cued gait pre-, post-training, and at the follow-up in IPD patients.
Gray shading indicates patients showing significant differences in gait speed between pre- and post-treatment according to Hass et al. criteria. *Small effect. **Average effect. ***Large effect.
Figure 2. Probability curves extracted for each…
Figure 2. Probability curves extracted for each predictor in the logistic regression model while controlling for all the other predictors.
The y-axis is the probability that a patient displays a positive response to MCGT. The three values indicated on the x-axis correspond to the mean values of each variable +/− 1 SD calculated from the tested sample of patients.

References

    1. Grabli D. et al.. Normal and pathological gait: what we learn from Parkinson’s disease. J Neurol Neurosurg Psychiatry 83, 979–985, doi: 10.1136/jnnp-2012-302263 (2012).
    1. Elbaz A. et al.. Risk tables for parkinsonism and Parkinson’s disease. J Clin Epidemiol 55, 25–31, doi: 10.1016/S0895-4356(01)00425-5 (2002).
    1. Samii A., Nutt J. G. & Ransom B. R. Parkinson’s disease. Lancet 363, 1783–1793, doi: 10.1016/S0140-6736(04)16305-8 (2004).
    1. Morris M. E., Huxham F., McGinley J., Dodd K. & Iansek R. The biomechanics and motor control of gait in Parkinson disease. Clin Biomech (Bristol, Avon) 16, 459–470, doi: 10.1016/S0268-0033(01)00035-3 (2001).
    1. Contreras A. & Grandas F. Risk of falls in Parkinson’s disease: a cross-sectional study of 160 patients. Parkinsons Dis 2012, 362572, doi: 10.1155/2012/362572 (2012).
    1. de Lau L. M., Verbaan D., van Rooden S. M., Marinus J. & van Hilten J. J. Relation of clinical subtypes in Parkinson’s disease with survival. Mov Disord 29, 150–151, doi: 10.1002/mds.25652 (2014).
    1. Sethi K. Levodopa unresponsive symptoms in Parkinson disease. Mov Disord 23 Suppl 3, S521–533, doi: 10.1002/mds.22049 (2008).
    1. Tomlinson C. L. et al.. Physiotherapy intervention in Parkinson’s disease: systematic review and meta-analysis. BMJ 345, e5004, doi: 10.1136/bmj.e5004 (2013).
    1. Lim I. et al.. Effects of external rhythmical cueing on gait in patients with Parkinson’s disease: a systematic review. Clin Rehabil 19, 695–713, doi: 10.1191/0269215505cr906oa (2005).
    1. Nombela C., Hughes L. E., Owen A. M. & Grahn J. A. Into the groove: can rhythm influence Parkinson’s disease? Neurosci Biobehav Rev 37, 2564–2570, doi: 10.1016/j.neubiorev.2013.08.003 (2013).
    1. Rocha P. A., Porfirio G. M., Ferraz H. B. & Trevisani V. F. Effects of external cues on gait parameters of Parkinson’s disease patients: a systematic review. Clin Neurol Neurosurg 124, 127–134, doi: 10.1016/j.clineuro.2014.06.026 (2014).
    1. Spaulding S. J. et al.. Cueing and gait improvement among people with Parkinson’s disease: a meta-analysis. Arch Phys Med Rehabil 94, 562–570, doi: 10.1016/j.apmr.2012.10.026 (2013).
    1. Arias P. & Cudeiro J. Effects of rhythmic sensory stimulation (auditory, visual) on gait in Parkinson’s disease patients. Exp Brain Res 186, 589–601, doi: 10.1007/s00221-007-1263-y (2008).
    1. Ford M. P., Malone L. A., Nyikos I., Yelisetty R. & Bickel C. S. Gait training with progressive external auditory cueing in persons with Parkinson’s disease. Arch Phys Med Rehabil 91, 1255–1261, doi: 10.1016/j.apmr.2010.04.012 (2010).
    1. Frazzitta G., Maestri R., Uccellini D., Bertotti G. & Abelli P. Rehabilitation treatment of gait in patients with Parkinson’s disease with freezing: a comparison between two physical therapy protocols using visual and auditory cues with or without treadmill training. Mov Disord 24, 1139–1143, doi: 10.1002/mds.22491 (2009).
    1. Thaut M. H. et al.. Rhythmic auditory stimulation in gait training for Parkinson’s disease patients. Mov Disord 11, 193–200, doi: 10.1002/mds.870110213 (1996).
    1. de Bruin N. et al.. Walking with music is a safe and viable tool for gait training in Parkinson’s disease: the effect of a 13-week feasibility study on single and dual task walking. Parkinsons Dis 2010, 483530, doi: 10.4061/2010/483530 (2010).
    1. Elston J., Honan W., Powell R., Gormley J. & Stein K. Do metronomes improve the quality of life in people with Parkinson’s disease? A pragmatic, single-blind, randomized cross-over trial. Clin Rehabil 24, 523–532, doi: 10.1177/0269215509360646 (2010).
    1. Espay A. J. et al.. At-home training with closed-loop augmented-reality cueing device for improving gait in patients with Parkinson disease. J Rehabil Res Dev 47, 573–581, doi: 10.1682/JRRD.2009.10.0165 (2010).
    1. Nieuwboer A. et al.. Cueing training in the home improves gait-related mobility in Parkinson’s disease: the RESCUE trial. J Neurol Neurosurg Psychiatry 78, 134–140, doi: 10.1136/jnnp.200X.097923 (2007).
    1. Fietzek U. M., Schroeteler F. E., Ziegler K., Zwosta J. & Ceballos-Baumann A. O. Randomized cross-over trial to investigate the efficacy of a two-week physiotherapy programme with repetitive exercises of cueing to reduce the severity of freezing of gait in patients with Parkinson’s disease. Clin Rehabil 28, 902–911, doi: 10.1177/0269215514527299 (2014).
    1. de Dreu M. J., van der Wilk A. S., Poppe E., Kwakkel G. & van Wegen E. E. Rehabilitation, exercise therapy and music in patients with Parkinson’s disease: a meta-analysis of the effects of music-based movement therapy on walking ability, balance and quality of life. Parkinsonism Relat Disord 18 Suppl 1, S114–119, doi: 10.1016/S1353-8020(11)70036-0 (2012).
    1. Wittwer J. E., Webster K. E. & Hill K. Music and metronome cues produce different effects on gait spatiotemporal measures but not gait variability in healthy older adults. Gait Posture 37, 219–222, doi: 10.1016/j.gaitpost.2012.07.006 (2013).
    1. Schulz K. F., Altman D. G., Moher D. & group, C. CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials. BMJ 340, c332, doi: 10.1136/bmj.c332 (2010).
    1. Maher C. G., Sherrington C., Herbert R. D., Moseley A. M. & Elkins M. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther 83, 713–721 (2003).
    1. Jahanshahi M. et al.. Dopaminergic modulation of striato-frontal connectivity during motor timing in Parkinson’s disease. Brain 133, 727–745, doi: 10.1093/brain/awq012 (2010).
    1. Allman M. J. & Meck W. H. Pathophysiological distortions in time perception and timed performance. Brain 135, 656–677, doi: 10.1093/brain/awr210 (2012).
    1. Jones C. R. & Jahanshahi M. Motor and perceptual timing in Parkinson’s disease. Adv Exp Med Biol 829, 265–290, doi: 10.1007/978-1-4939-1782-2_14 (2014).
    1. Joundi R. A., Brittain J. S., Green A. L., Aziz T. Z. & Jenkinson N. High-frequency stimulation of the subthalamic nucleus selectively decreases central variance of rhythmic finger tapping in Parkinson’s disease. Neuropsychologia 50, 2460–2466, doi: 10.1016/j.neuropsychologia.2012.06.017 (2012).
    1. Merchant H., Luciana M., Hooper C., Majestic S. & Tuite P. Interval timing and Parkinson’s disease: heterogeneity in temporal performance. Exp Brain Res 184, 233–248, doi: 10.1007/s00221-007-1097-7 (2008).
    1. Grahn J. A. & Brett M. Impairment of beat-based rhythm discrimination in Parkinson’s disease. Cortex 45, 54–61, doi: 10.1016/j.cortex.2008.01.005 (2009).
    1. Spencer R. M. & Ivry R. B. Comparison of patients with Parkinson’s disease or cerebellar lesions in the production of periodic movements involving event-based or emergent timing. Brain Cogn 58, 84–93, doi: 10.1016/j.bandc.2004.09.010 (2005).
    1. Wearden J. H. et al.. Stimulus timing by people with Parkinson’s disease. Brain Cogn 67, 264–279, doi: 10.1016/j.bandc.2008.01.010 (2008).
    1. Kotz S. A. & Schwartze M. Differential input of the supplementary motor area to a dedicated temporal processing network: functional and clinical implications. Front Integr Neurosci 5, 86, doi: 10.3389/fnint.2011.00086 (2011).
    1. Schwartze M. & Kotz S. A. A dual-pathway neural architecture for specific temporal prediction. Neurosci Biobehav Rev 37, 2587–2596, doi: 10.1016/j.neubiorev.2013.08.005 (2013).
    1. del Olmo M. F., Arias P., Furio M. C., Pozo M. A. & Cudeiro J. Evaluation of the effect of training using auditory stimulation on rhythmic movement in Parkinsonian patients - a combined motor and [18F]-FDG PET study. Parkinsonism Relat Disord 12, 155–164, doi: 10.1016/j.parkreldis.2005.11.002 (2006).
    1. Benoit C. E. et al.. Musically cued gait-training improves both perceptual and motor timing in Parkinson’s disease. Front Hum Neurosci 8, 494, doi: 10.3389/fnhum.2014.00494 (2014).
    1. Howe T. E., Lovgreen B., Cody F. W., Ashton V. J. & Oldham J. A. Auditory cues can modify the gait of persons with early-stage Parkinson’s disease: a method for enhancing parkinsonian walking performance? Clin Rehabil 17, 363–367, doi: 10.1191/0269215503cr621oa (2003).
    1. Suteerawattananon M., Morris G. S., Etnyre B. R., Jankovic J. & Protas E. J. Effects of visual and auditory cues on gait in individuals with Parkinson’s disease. J Neurol Sci 219, 63–69, doi: 10.1016/j.jns.2003.12.007 (2004).
    1. Willems A. M. et al.. The use of rhythmic auditory cues to influence gait in patients with Parkinson’s disease, the differential effect for freezers and non-freezers, an explorative study. Disabil Rehabil 28, 721–728, doi: 10.1080/09638280500386569 (2006).
    1. McIntosh G. C., Brown S. H., Rice R. R. & Thaut M. H. Rhythmic auditory-motor facilitation of gait patterns in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 62, 22–26, doi: 10.1136/jnnp.62.1.22 (1997).
    1. Hughes A. J., Daniel S. E., Kilford L. & Lees A. J. Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55, 181–184, doi: 10.1136/jnnp.55.3.181 (1992).
    1. Emre M. et al.. Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22, 1689–1707, doi: 10.1002/mds.21507 (2007).
    1. Fahn S. & Elton R. L. & UPDRS program members. Unified Parkinson’s Disease Rating Scale in Recent developments in Parkinsons disease Vol. 2 (eds Fahn S., Marsden C. D., Calne D. B. & Goldstein M.) 153–163, 293–304 (Macmillan Healthcare Information, 1987).
    1. Hoehn M. M. & Yahr M. D. Parkinsonism: onset, progression and mortality. Neurology 17, 427–442, doi: 10.1212/WNL.17.5.427 (1967).
    1. De Renzi E. & Vignolo L. A. The token test: A sensitive test to detect receptive disturbances in aphasics. Brain 85, 665–678, doi: 10.1093/brain/85.4.665 (1962).
    1. Kalbe E. et al.. Screening for cognitive deficits in Parkinson’s disease with the Parkinson neuropsychometric dementia assessment (PANDA) instrument. Parkinsonism Relat Disord 14, 93–101, doi: 10.1016/j.parkreldis.2007.06.008 (2008).
    1. Welsh K. A. et al.. The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part V. A normative study of the neuropsychological battery. Neurology 44, 609–614, doi: 10.1212/WNL.44.4.609 (1994).
    1. Memory Clinic. Neuropsychologische Testbatterie CERAD-Plus, (date of access: 28/07/2016) (2014).
    1. Yesavage J. A. et al.. Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res 17, 37–49, doi: 10.1016/0022-3956(82)90033-4 (1982).
    1. Tomlinson C. L. et al.. Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25, 2649–2653, doi: 10.1002/mds.23429 (2010).
    1. Baker R. Gait analysis methods in rehabilitation. J Neuroeng Rehabil 3, 4, doi: 10.1186/1743-0003-3-4 (2006).
    1. Dalla Bella S. et al.. BAASTA: Battery for the Assessment of Auditory Sensorimotor and Timing Abilities. Behav Res Meth published online 21 July, doi: 10.3758/s13428-016-0773-6 (2016).
    1. Aschersleben G. Temporal control of movements in sensorimotor synchronization. Brain Cogn 48, 66–79, doi: 10.1006/brcg.2001.1304 (2002).
    1. Repp B. H. Sensorimotor synchronization: a review of the tapping literature. Psychon Bull Rev 12, 969–992, doi: 10.3758/BF03206433 (2005).
    1. O’Connor C. M., Thorpe S. K., O’Malley M. J. & Vaughan C. L. Automatic detection of gait events using kinematic data. Gait Posture 25, 469–474, doi: 10.1016/j.gaitpost.2006.05.016 (2007).
    1. Schwartze M., Keller P. E., Patel A. D. & Kotz S. A. The impact of basal ganglia lesions on sensorimotor synchronization, spontaneous motor tempo, and the detection of tempo changes. Behav Brain Res 216, 685–691, doi: 10.1016/j.bbr.2010.09.015 (2011).
    1. Mates J. A model of synchronization of motor acts to a stimulus sequence. I. Timing and error corrections. Biol Cybern 70, 463–473 (1994).
    1. Repp B. H. & Keller P. E. Adaptation to tempo changes in sensorimotor synchronization: effects of intention, attention, and awareness. Q J Exp Psychol A 57, 499–521, doi: 10.1080/02724980343000369 (2004).
    1. Hass C. J. et al.. Defining the clinically meaningful difference in gait speed in persons with Parkinson disease. J Neurol Phys Ther 38, 233–238, doi: 10.1097/NPT.0000000000000055 (2014).
    1. Lehman D. A., Toole T., Lofald D. & Hirsch M. A. Training with verbal instructional cues results in near-term improvement of gait in people with Parkinson disease. J Neurol Phys Ther 29, 2–8, doi: 10.1097/ (2005).
    1. Jones M. R. Time, our lost dimension: toward a new theory of perception, attention, and memory. Psychol Rev 83, 323–355, doi: 10.1037/0033-295X.83.5.323 (1976).
    1. Large E. W. In The Psychology of Time (ed. Grondin S.) (West Yorkshire, Emerald, 2008).
    1. Dalla Bella S., Benoit C. E., Farrugia N., Schwartze M. & Kotz S. A. Effects of musically cued gait training in Parkinson’s disease: beyond a motor benefit. Ann N Y Acad Sci 1337, 77–85, doi: 10.1111/nyas.12651 (2015).
    1. Tessitore A., Giordano A., De Micco R., Russo A. & Tedeschi G. Sensorimotor connectivity in Parkinson’s disease: the role of functional neuroimaging. Front Neurol 5, 180, doi: 10.3389/fneur.2014.00180 (2014).
    1. Palmer S. J., Ng B., Abugharbieh R., Eigenraam L. & McKeown M. J. Motor reserve and novel area recruitment: amplitude and spatial characteristics of compensation in Parkinson’s disease. Eur J Neurosci 29, 2187–2196, doi: 10.1111/j.1460-9568.2009.06753.x (2009).
    1. Rascol O. et al.. The ipsilateral cerebellar hemisphere is overactive during hand movements in akinetic parkinsonian patients. Brain 120 (Pt 1), 103–110, doi: 10.1093/brain/120.1.103 (1997).
    1. del Olmo M. F., Cheeran B., Koch G. & Rothwell J. C. Role of the cerebellum in externally paced rhythmic finger movements. J Neurophysiol 98, 145–152, doi: 10.1152/jn.01088.2006 (2007).
    1. Manto M. et al.. Consensus paper: roles of the cerebellum in motor control–the diversity of ideas on cerebellar involvement in movement. Cerebellum 11, 457–487, doi: 10.1007/s12311-011-0331-9 (2012).
    1. Witt S. T., Laird A. R. & Meyerand M. E. Functional neuroimaging correlates of finger-tapping task variations: an ALE meta-analysis. Neuroimage 42, 343–356, doi: 10.1016/j.neuroimage.2008.04.025 (2008).
    1. Bastian A. J. Learning to predict the future: the cerebellum adapts feedforward movement control. Curr Opin Neurobiol 16, 645–649, doi: 10.1016/j.conb.2006.08.016 (2006).
    1. Bijsterbosch J. D. et al.. The role of the cerebellum in sub- and supraliminal error correction during sensorimotor synchronization: evidence from fMRI and TMS. J Cogn Neurosci 23, 1100–1112, doi: 10.1162/jocn.2010.21506 (2011).
    1. Schwartze M., Keller P. E. & Kotz S. A. Spontaneous, synchronized, and corrective timing behavior in cerebellar lesion patients. Behav Brain Res 312, 285–293, doi: 10.1016/j.bbr.2016.06.040 (2016).
    1. Grahn J. A. Neural mechanisms of rhythm perception: current findings and future perspectives. Top Cogn Sci 4, 585–606, doi: 10.1111/j.1756-8765.2012.01213.x (2012).
    1. Grahn J. A. & Brett M. Rhythm and beat perception in motor areas of the brain. J Cogn Neurosci 19, 893–906, doi: 10.1162/jocn.2007.19.5.893 (2007).
    1. Coull J. T., Cheng R. K. & Meck W. H. Neuroanatomical and neurochemical substrates of timing. Neuropsychopharmacology 36, 3–25, doi: 10.1038/npp.2010.113 (2011).
    1. Merchant H., Harrington D. L. & Meck W. H. Neural basis of the perception and estimation of time. Annu Rev Neurosci 36, 313–336, doi: 10.1146/annurev-neuro-062012-170349 (2013).

Source: PubMed

Szponzorok és közreműködők

Egészségi állapot

Kábítószer-beavatkozások

3
Iratkozz fel