Musically cued gait-training improves both perceptual and motor timing in Parkinson's disease

Frontiers in Human Neuroscience

Volumn 8, Issue JULY, 2014, Pages

  Benoit, Charles Etienne ^a,b,c   Dalla Bella, Simone ^a,c,d   Farrugia, Nicolas ^b,e   Obrig, Hellmuth ^b,f   Mainka, Stefan ^g   Kotz, Sonja A ^b,h  

^a UNIVERSITY OF FINANCE AND MANAGEMENT   (Poland)

^b MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

^c UNIVERSITY OF MONTPELLIER   (France)

^d INSTITUT UNIVERSITAIRE DE FRANCE   (France)

^e UNIVERSITY OF LONDON   (United Kingdom)

^f UNIVERSITY HOSPITAL LEIPZIG   (Germany)

^g Kliniken Beelitz GmbH Neurologisches Fachkrankenhaus für Bewegungsstörungen Parkinson   (Germany)

^h UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Auditory cueing; Motor behavior; Parkinson disease; Perception; Timing

Indexed keywords

ADULT; AGED; ARTICLE; ASSOCIATION; AUDITORY DISCRIMINATION; AUDITORY FEEDBACK; AUDITORY STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GAIT; HUMAN; MALE; MOTOR CONTROL; MOTOR PERFORMANCE; MUSIC THERAPY; PARKINSON DISEASE; PERCEPTION; SENSORIMOTOR FUNCTION;

EID: 84905098096     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00494     Document Type: Article

References (71)

1. Allman, M. J., and Meck, W. H. (2012). Pathophysiological distortions in time perception and timed performance. Brain 135, 656-677. doi:10.1093/brain/awr210
2. Arias, P., and Cudeiro, J. (2008). 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
3. Aschersleben, G. (2002). Temporal control of movements in sensorimotor synchronization. Brain Cogn. 48, 66-79. doi:10.1006/brcg.2001.1304
4. Baker, R. (2006). Gait analysis methods in rehabilitation. J. Neuroeng. Rehabil. 3, 4. doi:10.1186/1743-0003-3-4
5. Blin, O., Ferrandez, A. M., and Serratrice, G. (1990). Quantitative analysis of gait in Parkinson patients: increased variability of stride length. J. Neurol. Sci. 98, 91-97. doi:10.1016/0022-510X(90)90184-O
6. Bloem, B. R. (1992). Postural instability in Parkinson's disease. Clin. Neurol. Neurosurg. 94(Suppl.), S41-S45. doi:10.1016/0303-8467(92)90018-X
7. Bloem, B. R., Hausdorff, J. M., Visser, J. E., and Giladi, N. (2004). Falls and freezing of gait in Parkinson's disease: a review of two interconnected, episodic phenomena. Mov. Disord. 19, 871-884. doi:10.1002/mds.20115
8. Casini, L., and Ivry, R. B. (1999). Effects of divided attention on temporal processing in patients with lesions of the cerebellum or frontal lobe. Neuropsychology 13, 10-21. doi:10.1037/0894-4105.13.1.10
9. Coull, J. T., Cheng, R. K., and Meck, W. H. (2011). Neuroanatomical and neurochemical substrates of timing. Neuropsychopharmacology 36, 3-25. doi:10.1038/npp.2010.113
10. Crawford, J. R., and Garthwaite, P. H. (2002). Investigation of the single case in neuropsychology: confidence limits on the abnormality of test scores and test score differences. Neuropsychologia 40, 1196-1208. doi:10.1016/S0028-3932(01)00224-X
11. de Bruin, N., Doan, J. B., Turnbull, G., Suchowersky, O., Bonfield, S., Hu, B., et al. (2010). 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
12. de la Fuente-Fernandez, R., Ruth, T. J., Sossi, V., Schulzer, M., Calne, D. B., and Stoessl, A. J. (2001). Expectation and dopamine release: mechanism of the placebo effect in Parkinson's disease. Science 293, 1164-1166. doi:10.1126/science.1060937
13. De Renzi, E., and Vignolo, L. A. (1962). The token test: a sensitive test to detect receptive disturbances in aphasics. Brain 85, 665-678. doi:10.1093/brain/85.4.665
14. del Olmo, M. F., Arias, P., Furio, M. C., Pozo, M. A., and Cudeiro, J. (2006). Evaluation of the effect of training using auditory stimulation on rhythmic movement in Parkinsonian patients-a combine motor and [18F]-FDG PET study. Parkinsonism Relat. Disord. 12, 155-164. doi:10.1016/j.parkreldis.2005.11.002
15. Elbaz, A., Bower, J. H., Maraganore, D. M., Mcdonnell, S. K., Peterson, B. J., Ahlskog, J. E., et al. (2002). Risk tables for parkinsonism and Parkinson's disease. J. Clin. Epidemiol. 55, 25-31. doi:10.1016/S0895-4356(01)00425-5
16. Fujii, S., and Schlaug, G. (2013). The Harvard Beat Assessment Test (H-BAT): a battery for assessing beat perception and production and their dissociation. Front. Hum. Neurosci. 7:771. doi:10.3389/fnhum.2013.00771
17. Grabli, D., Karachi, C., Welter, M. L., Lau, B., Hirsch, E. C., Vidailhet, M., et al. (2012). Normal and pathological gait: what we learn from Parkinson's disease. J. Neurol. Neurosurg. Psychiatr. 83, 979-985. doi:10.1136/jnnp-2012-302263
18. Grassi, M., and Soranzo, A. (2009). MLP: a MATLAB toolbox for rapid and reliable auditory threshold estimation. Behav. Res. Methods 41, 20-28. doi:10.3758/BRM.41.1.20
19. Green, D. M. (1993). A maximum-likelihood method for estimating thresholds in a yes-no task. J. Acoust. Soc. Am. 93, 2096-2105. doi:10.1121/1.406162
20. Hallett, M. (2008). The intrinsic and extrinsic aspects of freezing of gait. Mov. Disord. 23(Suppl. 2), S439-S443. doi:10.1002/mds.21836
21. Harrington, D. L., Castillo, G. N., Greenberg, P. A., Song, D. D., Lessig, S., Lee, R. R., et al. (2011). Neurobehavioral mechanisms of temporal processing deficits in Parkinson's disease. PLoS ONE 6:e17461. doi:10.1371/journal.pone.0017461
22. Harrington, D. L., Haaland, K. Y., and Hermanowicz, N. (1998). Temporal processing in the basal ganglia. Neuropsychology 12, 3-12. doi:10.1037/0894-4105.12.1.3
23. Howe, T. E., Lovgreen, B., Cody, F. W., Ashton, V. J., and Oldham, J. A. (2003). 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
24. Hyde, K. L., and Peretz, I. (2003). "Out-of-pitch" but still "in-time". An auditory psychophysical study in congenital amusic adults. Ann. N. Y. Acad. Sci. 999, 173-176. doi:10.1196/annals.1284.023
25. Iversen, J. R., and Patel, A. D. (2008). The Beat Alignment Test (BAT): surveying beat processing abilities in the general population. Proceedings of the 10th International Conference on Music Perception and Cognition; Sapporo, Japan. 465-468.
26. Jones, C. R., and Jahanshahi, M. (2009). The substantia nigra, the basal ganglia, dopamine and temporal processing. J. Neural Transm. Suppl. 73, 161-171. doi:10.1007/978-3-211-92660-4_13
27. Jones, M. R. (1976). 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
28. Kalbe, E., Calabrese, P., Kohn, N., Hilker, R., Riedel, O., Wittchen, H. U., et al. (2008). 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
29. Koch, G., Costa, A., Brusa, L., Peppe, A., Gatto, I., Torriero, S., et al. (2008). Impaired reproduction of second but not millisecond time intervals in Parkinson's disease. Neuropsychologia 46, 1305-1313. doi:10.1016/j.neuropsychologia.2007.12.005
30. Koller, W. C., and Montgomery, E. B. (1997). Issues in the early diagnosis of Parkinson's disease. Neurology 49, S10-S25. doi:10.1212/WNL.49.1_Suppl_1.S10
31. Kotz, S. A., and Schwartze, M. (2011). 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
32. Kotz, S. A., Schwartze, M., and Schmidt-Kassow, M. (2009). Non-motor basal ganglia functions: a review and proposal for a model of sensory predictability in auditory language perception. Cortex 45, 982-990. doi:10.1016/j.cortex.2009.02.010
33. Kwakkel, G., De Goede, C. J., and Van Wegen, E. E. (2007). Impact of physical therapy for Parkinson's disease: a critical review of the literature. Parkinsonism Relat. Disord. 13(Suppl. 3), S478-S487. doi:10.1016/S1353-8020(08)70053-1
34. Large, E. W. (2008). "Resonating to musical rhythm: theory and experiment, " in The Psychology of Time, ed. S. Grondin (West Yorkshire: Emerald), 189-231.
35. Large, E. W., and Jones, M. R. (1999). The dynamics of attending: how we track time. Psychol. Rev. 106, 119-159. doi:10.1016/j.neuroimage.2011.11.065
36. Lehman, D. A., Toole, T., Lofald, D., and Hirsch, M. A. (2005). 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:10.1097/01.NPT.0000282256.36208.cf
37. Lewis, M. M., Slagle, C. G., Smith, A. B., Truong, Y., Bai, P., Mckeown, M. J., et al. (2007). Task specific influences of Parkinson's disease on the striato-thalamo-cortical and cerebello-thalamo-cortical motor circuitries. Neuroscience 147, 224-235. doi:10.1016/j.neuroscience.2007.04.006
38. Liegeois-Chauvel, C., Peretz, I., Babai, M., Laguitton, V., and Chauvel, P. (1998). Contribution of different cortical areas in the temporal lobes to music processing. Brain 121(Pt 10), 1853-1867. doi:10.1093/brain/121.10.1853
39. Lim, I., Van Wegen, E., De Goede, C., Deutekom, M., Nieuwboer, A., Willems, A., et al. (2005). 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
40. Malapani, C., Dubois, B., Rancurel, G., and Gibbon, J. (1998). Cerebellar dysfunctions of temporal processing in the seconds range in humans. Neuroreport 9, 3907-3912. doi:10.1097/00001756-199812010-00026
41. Marchese, R., Diverio, M., Zucchi, F., Lentino, C., and Abbruzzese, G. (2000). The role of sensory cues in the rehabilitation of parkinsonian patients: a comparison of two physical therapy protocols. Mov. Disord. 15, 879-883. doi:10.1002/1531-8257(200009)15:5<879::AID-MDS1018>3.0.CO;2-9
42. McIntosh, G. C., Brown, S. H., Rice, R. R., and Thaut, M. H. (1997). Rhythmic auditory-motor facilitation of gait patterns in patients with Parkinson's disease. J. Neurol. Neurosurg. Psychiatr. 62, 22-26. doi:10.1136/jnnp.62.1.22
43. Merchant, H., Harrington, D. L., and Meck, W. H. (2013). Neural basis of the perception and estimation of time. Annu. Rev. Neurosci. 36, 313-336. doi:10.1146/annurev-neuro-062012-170349
44. Merchant, H., Luciana, M., Hooper, C., Majestic, S., and Tuite, P. (2008). Interval timing and Parkinson's disease: heterogeneity in temporal performance. Exp. Brain Res. 184, 233-248. doi:10.1007/s00221-007-1097-7
45. Morris, M. E., Huxham, F. E., Mcginley, J., and Iansek, R. (2001). Gait disorders and gait rehabilitation in Parkinson's disease. Adv. Neurol. 87, 347-361.
46. Nieuwboer, A., De Weerdt, W., Dom, R., Truyen, M., Janssens, L., and Kamsma, Y. (2001). The effect of a home physiotherapy program for persons with Parkinson's disease. J. Rehabil. Med. 33, 266-272. doi:10.1080/165019701753236455
47. Nieuwboer, A., Kwakkel, G., Rochester, L., Jones, D., Van Wegen, E., Willems, A. M., et al. (2007). Cueing training in the home improves gait-related mobility in Parkinson's disease: the RESCUE trial. J. Neurol. Neurosurg. Psychiatr. 78, 134-140. doi:10.1136/jnnp.200X.097923
48. Nombela, C., Hughes, L. E., Owen, A. M., and Grahn, J. A. (2013). Into the groove: can rhythm influence Parkinson's disease? Neurosci. Biobehav. Rev. 37(10 Pt 2), 2564-2570. doi:10.1016/j.neubiorev.2013.08.003
49. O'Boyle, D. J., Freeman, J. S., and Cody, F. W. (1996). The accuracy and precision of timing of self-paced, repetitive movements in subjects with Parkinson's disease. Brain 119(Pt 1), 51-70. doi:10.1093/brain/119.1.51
50. Platel, H., Price, C., Baron, J. C., Wise, R., Lambert, J., Frackowiak, R. S., et al. (1997). The structural components of music perception. A functional anatomical study. Brain 120(Pt 2), 229-243.
51. Repp, B. H. (2005). Sensorimotor synchronization: a review of the tapping literature. Psychon. Bull. Rev. 12, 969-992. doi:10.3758/BF03206433
52. Samii, A., Nutt, J. G., and Ransom, B. R. (2004). Parkinson's disease. Lancet 363, 1783-1793. doi:10.1016/S0140-6736(04)16305-8
53. Schwartze, M., Keller, P. E., Patel, A. D., and Kotz, S. A. (2011). 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
54. Schwartze, M., and Kotz, S. A. (2013). A dual-pathway neural architecture for specific temporal prediction. Neurosci. Biobehav. Rev. 37(10 Pt 2), 2587-2596. doi:10.1016/j.neubiorev.2013.08.005
55. Sen, S., Kawaguchi, A., Truong, Y., Lewis, M. M., and Huang, X. (2010). Dynamic changes in cerebello-thalamo-cortical motor circuitry during progression of Parkinson's disease. Neuroscience 166, 712-719. doi:10.1016/j.neuroscience.2009.12.036
56. Sharma, A., Szeto, K., and Desilets, A. R. (2012). Efficacy and safety of deep brain stimulation as an adjunct to pharmacotherapy for the treatment of Parkinson disease. Ann. Pharmacother. 46, 248-254. doi:10.1345/aph.1Q508
57. Smith, J. G., Harper, D. N., Gittings, D., and Abernethy, D. (2007). The effect of Parkinson's disease on time estimation as a function of stimulus duration range and modality. Brain Cogn. 64, 130-143. doi:10.1016/j.bandc.2007.01.005
58. Sowinski, J., and Dalla Bella, S. (2013). Poor synchronization to the beat may result from deficient auditory-motor mapping. Neuropsychologia 51, 1952-1963. doi:10.1016/j.neuropsychologia.2013.06.027
59. Spaulding, S. J., Barber, B., Colby, M., Cormack, B., Mick, T., and Jenkins, M. E. (2012). 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
60. Spencer, R. M., and Ivry, R. B. (2005). 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
61. Svenningsson, P., Westman, E., Ballard, C., and Aarsland, D. (2012). Cognitive impairment in patients with Parkinson's disease: diagnosis, biomarkers, and treatment. Lancet Neurol. 11, 697-707. doi:10.1016/S1474-4422(12)70152-7
62. Thaut, M. H., McIntosh, G. C., Rice, R. R., Miller, R. A., Rathbun, J., and Brault, J. M. (1996). Rhythmic auditory stimulation in gait training for Parkinson's disease patients. Mov. Disord. 11, 193-200. doi:10.1002/mds.870110213
63. Thaut, M. H., McIntosh, K. W., McIntosh, G. C., and Hoemberg, V. (2001). Auditory rhythmicity enhances movement and speech motor control in patients with Parkinson's disease. Funct. Neurol. 16, 163-172.
64. Wearden, J. H., Smith-Spark, J. H., Cousins, R., Edelstyn, N. M., Cody, F. W., and O'Boyle, D. J. (2008). Stimulus timing by people with Parkinson's disease. Brain Cogn. 67, 264-279. doi:10.1016/j.bandc.2008.01.010
65. Welsh, K. A., Butters, N., Mohs, R. C., Beekly, D., Edland, S., Fillenbaum, G., et al. (1994). The consortium to establish a registry for Alzheimer's disease (CERAD). Part V. A normative study of the neuropsychological battery. Neurology 44, 609-614.
66. Willems, A. M., Nieuwboer, A., Chavret, F., Desloovere, K., Dom, R., Rochester, L., et al. (2006). 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
67. Wing, A. M. (2002). Voluntary timing and brain function: an information processing approach. Brain Cogn. 48, 7-30. doi:10.1006/brcg.2001.1301
68. Wing, A. M., and Kristofferson, A. B. (1973a). Response delays and the timing of discrete motor responses. Percept. Psychophys. 14, 5-12. doi:10.3758/BF03198607
69. Wing, A. M., and Kristofferson, A. B. (1973b). The timing of interresponse intervals. Percept. Psychophys. 13, 455-460. doi:10.3758/BF03205802
70. Wu, T., Wang, J., Wang, C., Hallett, M., Zang, Y., Wu, X., et al. (2012). Basal ganglia circuits changes in Parkinson's disease patients. Neurosci. Lett. 524, 55-59. doi:10.1016/j.neulet.2012.07.012
71. Yesavage, J. A., Brink, T. L., Rose, T. L., Lum, O., Huang, V., Adey, M., et al. (1982). 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