Walking to your right music: a randomized controlled trial on the novel use of treadmill plus music in Parkinson's disease

Rocco Salvatore Calabrò, Antonino Naro, Serena Filoni, Massimo Pullia, Luana Billeri, Provvidenza Tomasello, Simona Portaro, Giuseppe Di Lorenzo, Concetta Tomaino, Placido Bramanti, Rocco Salvatore Calabrò, Antonino Naro, Serena Filoni, Massimo Pullia, Luana Billeri, Provvidenza Tomasello, Simona Portaro, Giuseppe Di Lorenzo, Concetta Tomaino, Placido Bramanti

Abstract

Background: Rhythmic Auditory Stimulation (RAS) can compensate for the loss of automatic and rhythmic movements in patients with idiopathic Parkinson's disease (PD). However, the neurophysiological mechanisms underlying the effects of RAS are still poorly understood. We aimed at identifying which mechanisms sustain gait improvement in a cohort of patients with PD who practiced RAS gait training.

Methods: We enrolled 50 patients with PD who were randomly assigned to two different modalities of treadmill gait training using GaitTrainer3 with and without RAS (non_RAS) during an 8-week training program. We measured clinical, kinematic, and electrophysiological effects of both the gait trainings.

Results: We found a greater improvement in Functional Gait Assessment (p < 0.001), Tinetti Falls Efficacy Scale (p < 0.001), Unified Parkinson Disease Rating Scale (p = 0.001), and overall gait quality index (p < 0.001) following RAS than non_RAS training. In addition, the RAS gait training induced a stronger EEG power increase within the sensorimotor rhythms related to specific periods of the gait cycle, and a greater improvement of fronto-centroparietal/temporal electrode connectivity than the non_RAS gait training.

Conclusions: The findings of our study suggest that the usefulness of cueing strategies during gait training consists of a reshape of sensorimotor rhythms and fronto-centroparietal/temporal connectivity. Restoring the internal timing mechanisms that generate and control motor rhythmicity, thus improving gait performance, likely depends on a contribution of the cerebellum. Finally, identifying these mechanisms is crucial to create patient-tailored, RAS-based rehabilitative approaches in PD.

Trial registration: NCT03434496 . Registered 15 February 2018, retrospectively registered.

Keywords: Gait rehabilitation; GaitTrainer3; Parkinson’s disease; Rhythmic auditory stimulation.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Summary of patients’ flow
Fig. 2
Fig. 2
Average post vs. pre changes in ERSs/ERDs and their scalp projections relatively to the full gait cycle in the two groups (RAS and non_RAS gait training). We found a significant strengthening of the central α/β-ERD during single support in the stance phase, of the low frontal β-ERD during the single support in the swing phase, and of the fronto-central α/β-ERS during the double support in the stance phase of the gait cycle. All such changes were more evident following RAS compared to non_RAS training. Average post vs. pre changes in alpha and beta ERD/ERS color maps are coded in blue and red tones, respectively. Electrodes were grouped into frontal F -Fp1/2,F3/4/7/8, centroparietal -C3/4,P3/4-, temporal T -T3/4/5/6, and occipital O -O1/2-
Fig. 3
Fig. 3
Scatter plot graphs for the relationship between the clinical and neurophysiological data

References

    1. Arias P, Cudeiro J. Effects of rhythmic sensory stimulation (auditory, visual) on gait in Parkinson’s disease patients. Exp Brain Res. 2008;186(4):589–601. doi: 10.1007/s00221-007-1263-y.
    1. Ashoori A, Eagleman DM, Jankovic J. Effects of auditory rhythm and music on gait disturbances in Parkinson's disease. Front Neurol. 2015;6:234. doi: 10.3389/fneur.2015.00234.
    1. Beninato M, Fernandes A, Plummer LS. Minimal clinically important difference of the functional gait assessment in older adults. Phys Ther. 2014;94(11):1594–1603. doi: 10.2522/ptj.20130596.
    1. Braunlich K, Seger CA, Jentink KG, Buard I, Kluger BM, Thaut MH. Rhythmic auditory cues shape neural network recruitment in Parkinson's disease during repetitive motor behavior. Eur J Neurosci. 2019;49(6):849–858. doi: 10.1111/ejn.14227.
    1. Bukowska AA, Krężałek P, Mirek E, Bujas P, Marchewka A. Neurologic music therapy training for mobility and stability rehabilitation with Parkinson's disease - a pilot study. Front Hum Neurosci. 2016;9:710. doi: 10.3389/fnhum.2015.00710.
    1. Calabrò RS, Naro A, Russo M, Bramanti P, Carioti L, Balletta T, Buda A, Manuli A, Filoni S, Bramanti A. Shaping neuroplasticity by using powered exoskeletons in patients with stroke: a randomized clinical trial. J Neuroeng Rehabil. 2018;15(1):35. doi: 10.1186/s12984-018-0377-8.
    1. Calabrò RS, Naro A, Russo M, Leo A, De Luca R, Balletta T, Buda A, La Rosa G, Bramanti A, Bramanti P. The role of virtual reality in improving motor performance as revealed by EEG: a randomized clinical trial. J Neuroeng Rehabil. 2017;14(1):53. doi: 10.1186/s12984-017-0268-4.
    1. Chen JL, Penhune VB, Zatorre RJ. Listening to musical rhythms recruits motor regions of the brain. Cereb Cortex. 2008;18(12):2844–2854. doi: 10.1093/cercor/bhn042.
    1. Coull JT, Cheng RK, Meck WH. Neuroanatomical and neurochemical substrates of timing. Neuropsychopharmacology. 2011;36(1):3–25. doi: 10.1038/npp.2010.113.
    1. da Silva PL, Schoueri JHM, de Alcantara Sousa LV, Raimundo RD, da Silva ME, Correa JA, Adami F. Regional differences in the temporal evolution of stroke: a population-based study of Brazil according to sex in individuals aged 15–49 years between 1997 and 2012. BMC Res Notes. 2018;11(1):326. doi: 10.1186/s13104-018-3439-x.
    1. de Bruin N, Doan JB, Turnbull G, Suchowersky O, Bonfield S, Hu B, Brown LA. 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;2010:1–9. doi: 10.4061/2010/483530.
    1. de Dreu MJ, van der Wilk AS, Poppe E, Kwakkel G, Wegen v. EE 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. 2012;18(Suppl 1):S114–S119. doi: 10.1016/S1353-8020(11)70036-0.
    1. De Icco R, Tassorelli C, Berra E, Bolla M, Pacchetti C, Sandrini G. Acute and chronic effect of acoustic and visual cues on gait training in Parkinson’s disease: a randomized, controlled study. Parkinsons Dis. 2015;2015:978590.
    1. del Olmo MF, Cudeiro J. Temporal variability of gait in Parkinson disease: effects of a rehabilitation programme based on rhythmic sound cues. Parkinsonism Relat Disord. 2005;11(1):25–33. doi: 10.1016/j.parkreldis.2004.09.002.
    1. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods. 2004;134(1):9–21. doi: 10.1016/j.jneumeth.2003.10.009.
    1. Edelman GM, Gally JA. Degeneracy and complexity in biological systems. Proc Natl Acad Sci U S A. 2001;98:13763–13768. doi: 10.1073/pnas.231499798.
    1. Engel AK, Fries P. Beta-band oscillations--signalling the status quo? Curr Opin Neurobiol. 2010;20(2):156–165. doi: 10.1016/j.conb.2010.02.015.
    1. Formaggio E, Storti SF, Boscolo Galazzo I, Gandolfi M, Geroin C, Smania N, Spezia L, Waldner A, Fiaschi A, Manganotti P. Modulation of event-related desynchronization in robot-assisted hand performance: brain oscillatory changes in active, passive and imagined movements. J Neuroeng Rehabil. 2013;10:24. doi: 10.1186/1743-0003-10-24.
    1. Formaggio E, Storti SF, Boscolo Galazzo I, Gandolfi M, Geroin C, Smania N, Fiaschi A, Manganotti P. Time-frequency modulation of ERD and EEG coherence in robot-assisted hand performance. Brain Topogr. 2015;28(2):352–363. doi: 10.1007/s10548-014-0372-8.
    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. 2009;24(8):1139–1143. doi: 10.1002/mds.22491.
    1. Gallagher R, Damodaran H, Werner WG, Powell W, Deutsch JE. Auditory and visual cueing modulate cycling speed of older adults and persons with Parkinson’s disease in a virtual cycling (V-cycle) system. J Neuroeng Rehabil. 2016;13:77. doi: 10.1186/s12984-016-0184-z.
    1. Gao LL, Wu T. The study of brain functional connectivity in Parkinson's disease. Transl Neurodegener. 2016;5:18. doi: 10.1186/s40035-016-0066-0.
    1. Ghai S, Ghai I, Schmitz G, Effenberg AO. Effect of rhythmic auditory cueing on parkinsonian gait: a systematic review and meta-analysis. Sci Rep. 2018;8(1):506. doi: 10.1038/s41598-017-16232-5.
    1. Gómez J, Jesús Marín-Méndez J, Molero P, Atakan Z, Ortuño F. Time perception networks and cognition in schizophrenia: a review and a proposal. Psychiatry Res. 2014;220(3):737–744. doi: 10.1016/j.psychres.2014.07.048.
    1. Gwin JT, Gramann K, Makeig S, Ferris DP. Electrocortical activity is coupled to gait cycle phase during treadmill walking. Neuroimage. 2011;54(2):1289–1296. doi: 10.1016/j.neuroimage.2010.08.066.
    1. Hackett TA. Anatomic organization of the auditory cortex. In: Celesia GG, Hickok G, editors. Handbook of Clinical Neurology. Amsterdam: Elsevier B.V; 2015. pp. 27–53.
    1. Handojoseno AA, Gilat M, Ly QT, Chamtie H, Shine JM, Nguyen TN, et al. Engineering in medicine and biology society (EMBC) 37th annual international conference of the IEEE: IEEE. 2015. An EEG study of turning freeze in Parkinson's disease patients: the alteration of brain dynamic on the motor and visual cortex; pp. 6618–6621.
    1. Hausdorff JM. Gait dynamics in Parkinson's disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. Chaos. 2009;19(2):026113. doi: 10.1063/1.3147408.
    1. Hehenberger L, Seeber M, Scherer R. Estimation of gait parameters from EEG source oscillations. Budapest: IEEE International Conference on Systems, Man, and Cybernetics (SMC); 2016. pp. 004182–004187.
    1. Holtzer R, Mahoney JR, Izzetoglu M, Wang C, England S, Verghese J. Online fronto-cortical control of simple and attention-demanding locomotion in humans. Neuroimage. 2015;112:152–159. doi: 10.1016/j.neuroimage.2015.03.002.
    1. Holtzer R, Schoen C, Demetriou E, Mahoney JR, Izzetoglu M, Wang C, Verghese J. Stress and gender effects on prefrontal cortex oxygenation levels assessed during single and dual-task walking conditions. Eur J Neurosci. 2017;45(5):660–670. doi: 10.1111/ejn.13518.
    1. Holtzer R, Verghese J, Allali G, Izzetoglu M, Wang C, Mahoney JR. Neurological gait abnormalities moderate the functional brain signature of the posture first hypothesis. Brain Topogr. 2016;29(2):334–343. doi: 10.1007/s10548-015-0465-z.
    1. Jankovic J. Gait disorders. Neurol Clin. 2015;33(1):249–268. doi: 10.1016/j.ncl.2014.09.007.
    1. Jenkinson N, Brown P. New insights into the relationship between dopamine, beta oscillations and motor function. Trends Neurosci. 2011;34:611–618. doi: 10.1016/j.tins.2011.09.003.
    1. Kadivar Z, Corcos DM, Foto J, Hondzinski JM. Effect of step training and rhythmic auditory stimulation on functional performance in Parkinson patients. Neurorehabil Neural Repair. 2011;25:626–635. doi: 10.1177/1545968311401627.
    1. Koshimori Y, Strafella AP, Valli M, et al. Motor synchronization to rhythmic auditory stimulation (RAS) attenuates dopaminergic responses in ventral striatum in young healthy adults: [11C]-(+)-PHNO PET study. Front Neurosci. 2019;13:106. doi: 10.3389/fnins.2019.00106.
    1. Koshimori Y, Thaut MH. Future perspectives on neural mechanisms underlying rhythm and music based neurorehabilitation in Parkinson's disease. Ageing Res Rev. 2018;47:133–139. doi: 10.1016/j.arr.2018.07.001.
    1. Lee MM, Cho HY, Song CH. The mirror therapy program enhances upper-limb motor recovery and motor function in acute stroke patients. Am J Phys Med Rehabil. 2012;91(8):689–696. doi: 10.1097/PHM.0b013e31824fa86d.
    1. Lee SJ, Yoo JY, Ryu JS, Park HK, Chung SJ. The effects of visual and auditory cues on freezing of gait in patients with Parkinson disease. Am J Phys Med Rehabil. 2012;91:2–11. doi: 10.1097/PHM.0b013e31823c7507.
    1. Leocani L, Toro C, Manganotti P, Zhuang P, Hallett M. Event-related coherence and event-related desynchronization/synchronization in the 10 Hz and 20 Hz EEG during self-paced movements. Electroencephalogr Clin Neurophysiol. 1997;104(3):199–206. doi: 10.1016/S0168-5597(96)96051-7.
    1. Leow LA, Grahn JA. Neural mechanisms of rhythm perception: present findings and future directions. Adv Exp Med Biol. 2014;829:325–338. doi: 10.1007/978-1-4939-1782-2_17.
    1. Leow LA, Parrott T, Grahn JA. Individual differences in beat perception affect gait responses to low- and high-groove music. Front Hum Neurosci. 2014;8:811. doi: 10.3389/fnhum.2014.00811.
    1. Leow LA, Rinchon C, Grahn J. Familiarity with music increases walking speed in rhythmic auditory cuing. Ann N Y Acad Sci. 2015;1337:53–61. doi: 10.1111/nyas.12658.
    1. Lim I, van Wegen E, de Goede C, Deutekom M, Nieuwboer A, Willems A, Jones D, Rochester L, Kwakkel G. Effects of external rhythmical cueing on gait in patients with Parkinson's disease: a systematic review. Clin Rehabil. 2005;19(7):695–713. doi: 10.1191/0269215505cr906oa.
    1. Little S, Brown P. The functional role of beta oscillations in Parkinson's disease. Parkinsonism Relat Disord. 2014;20(Suppl 1):S44–S48. doi: 10.1016/S1353-8020(13)70013-0.
    1. Ly QT, Handojoseno AA, Gilat M, Nguyen N, Chai R, Tran Y, et al. Engineering in medicine and biology society (EMBC), 2016 IEEE 38th annual international conference of the: IEEE. 2016. Detection of gait initiation failure in Parkinson’s disease patients using EEG signals; pp. 1599–1602.
    1. Magrinelli F, Picelli A, Tocco P, Federico A, Roncari L, Smania N, Zanette G, Tamburin S. Pathophysiology of motor dysfunction in Parkinson’s disease as theRationale for drug treatment and rehabilitation. Parkinsons Dis. 2016;2016:9832839.
    1. Manganotti P, Gerloff C, Toro C, Katsuta H, Sadato N, Zhuang Leocani L, Hallett M. Task-related coherence and task-related spectral power changes during sequential finger movements. Electroencephalogr Clin Neurophysiol. 1998;109(1):50–62. doi: 10.1016/S0924-980X(97)00074-X.
    1. McIntosh GC, Brown SH, Rice RR, Thaut MH. Rhythmic auditory-motor facilitation of gait patterns in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry. 1997;62:22–26. doi: 10.1136/jnnp.62.1.22.
    1. McKinlay A, Grace RC, Dalrymple-Alford JC, Roger D. Characteristics of executive function impairment in Parkinson's disease patients without dementia. J Int Neuropsychol Soc. 2010;16(2):268–277. doi: 10.1017/S1355617709991299.
    1. Miller RA, Thaut MH, McIntosh GC, Rice RR. Components of EMG symmetry and variability in parkinsonian and healthy elderly gait. Electroencephalogr Clin Neurophysiol. 1996;101(1):1–7. doi: 10.1016/0013-4694(95)00209-X.
    1. Miller RA, Thaut MH, McIntosh GC, Rice RR. Components of EMG symmetry and variability in parkinsonian and healthy elderly gait. Electroencephalogr Clin Neurophysiol Electromyogr Mot Control. 1996;101:1–7. doi: 10.1016/0013-4694(95)00209-X.
    1. Mirdamadi JL. Cerebellar role in Parkinson's disease. J Neurophysiol. 2016;116(3):917–919. doi: 10.1152/jn.01132.2015.
    1. Morris ME, Iansek R, Matyas TA, Summers JJ. Stride length regulation in Parkinson’s disease. Normalization strategies and underlying mechanisms. Brain. 1996;119(Pt 2):551–568. doi: 10.1093/brain/119.2.551.
    1. Nakayashiki K, Saeki M, Takata Y, Hayashi Y, Kondo T. Modulation of event-related desynchronization during kinematic and kinetic hand movements. J Neuroeng Rehabil. 2014;11:90. doi: 10.1186/1743-0003-11-90.
    1. Naro A, Leo A, Cannavò A, Buda A, Bruno R, Salviera C, Bramanti P, Calabrò RS. Audiomotor integration in minimally conscious state: proof of concept! Neural Plast. 2015;2015:391349. doi: 10.1155/2015/391349.
    1. Naro A, Leo A, Russo M, Cannavò A, Milardi D, Bramanti P, Calabrò RS. Does transcranial alternating current stimulation induce cerebellum plasticity? Feasibility, safety and efficacy of a novel electrophysiological approach. Brain Stimul. 2016;9(3):388–395. doi: 10.1016/j.brs.2016.02.005.
    1. Naro A, Russo M, Leo A, Cannavò A, Manuli A, Bramanti A, Bramanti P, Calabrò RS. Cortical connectivity modulation induced by cerebellar oscillatory transcranial direct current stimulation in patients with chronic disorders of consciousness: a marker of covert cognition? Clin Neurophysiol. 2016;127(3):1845–1854. doi: 10.1016/j.clinph.2015.12.010.
    1. Nieuwboer A, Kwakkel G, Rochester L, Jones D, van Wegen E, Willems AM, Chavret F, Hetherington V, Baker K, Lim I. Cueing training in the home improves gait-related mobility in Parkinson’s disease: the RESCUE trial. J Neurol Neurosurg Psychiatry. 2007;78(2):134–40. Erratum in: J Neurol Neurosurg Psychiatry. 2010;81(12):1414. J Neurol Neurosurg Psychiatry. 2010;81(1):126.
    1. Parker KL, Lamichhane D, Caetano MS, Narayanan NS. Executive dysfunction in Parkinson's disease and timing deficits. Front Integr Neurosci. 2013;7:75. doi: 10.3389/fnint.2013.00075.
    1. Parsons BD, Novich SD, Eagleman DM. Motor-sensory recalibration modulates perceived simultaneity of cross-modal events at different distances. Front Psychol. 2013;4:46. doi: 10.3389/fpsyg.2013.00046.
    1. Pelzer EA, Hintzen A, Goldau M, von Cramon DY, Timmermann L, Tittgemeyer M. Cerebellar networks with basal ganglia: feasibility for tracking cerebello-pallidal and subthalamo-cerebellar projections in the human brain. Eur J Neurosci. 2013;38:3106–3114. doi: 10.1111/ejn.12314.
    1. Petter EA, Lusk NA, Hesslow G, Meck WH. Interactive roles of the cerebellum and striatum in sub-second and supra-second timing: support for an initiation, continuation, adjustment, and termination (ICAT) model of temporal processing. Neurosci Biobehav Rev. 2016;71:739–755. doi: 10.1016/j.neubiorev.2016.10.015.
    1. Petzinger GM, Holschneider DP, Fisher BE, et al. The effects of exercise on dopamine neurotransmission in Parkinson’s disease: targeting neuroplasticity to modulate basal ganglia circuitry. Brain Plasticity. 2015;1(1):29–39. doi: 10.3233/BPL-150021.
    1. Pfurtscheller G, Aranibar A. Event-related cortical desynchronization detected by power measurements of scalp EEG. Electroencephalogr Clin Neurophysiol. 1977;42:817–826. doi: 10.1016/0013-4694(77)90235-8.
    1. Pfurtscheller G, Lopes da Silva FH. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol. 1999;110:1842–1857. doi: 10.1016/S1388-2457(99)00141-8.
    1. Pizzamiglio S, Abdalla H, Naeem U, Turner DL. Neural predictors of gait stability when walking freely in the real-world. J Neuroeng Rehabil. 2018;15(1):11. doi: 10.1186/s12984-018-0357-z.
    1. Rappelsberger P. The reference problem and mapping of coherence: a stimulation study. Brain Topogr. 1989;2:63–72. doi: 10.1007/BF01128844.
    1. Rocha PA, Porfírio GM, Ferraz HB, Trevisani VF. Effects of external cues on gait parameters of Parkinson's disease patients: a systematic review. Clin Neurol Neurosurg. 2014;124:127–134. doi: 10.1016/j.clineuro.2014.06.026.
    1. Rochester L, Baker K, Nieuwboer A, Burn D. Targeting dopa-sensitive and dopa-resistant gait dysfunction in Parkinson's disease: selective responses to internal and external cues. Mov Disord. 2011;26(3):430–5. doi: 10.1002/mds.23450.
    1. Rubinstein TC, Giladi N, Hausdorff JM. The power of cueing to circumvent dopamine deficits: a review of physical therapy treatment of gait disturbances in Parkinson’s disease. Mov Disord. 2002;17:1148–1160. doi: 10.1002/mds.10259.
    1. Seeber M, Scherer R, Wagner J, Solis-Escalante T, Müller-Putz GR. EEG beta suppression and low gamma modulation are different elements of human upright walking. Front Hum Neurosci. 2014;8:485. doi: 10.3389/fnhum.2014.00485.
    1. Seeber M, Scherer R, Wagner J, Solis-Escalante T, Müller-Putz GR. High and low gamma EEG oscillations in central sensorimotor areas are conversely modulated during the human gait cycle. Neuroimage. 2015;112:318–326. doi: 10.1016/j.neuroimage.2015.03.045.
    1. Sen S, Kawaguchi A, Truong Y, Lewis MM, Huang X. Dynamic changes in cerebello-thalamo-cortical motor circuitry during progression of Parkinson’s disease. Neuroscience. 2010;166(2):712–719. doi: 10.1016/j.neuroscience.2009.12.036.
    1. Senhadji L, Wendling F. Epileptic transient detection: wavelets and time-frequency approaches. Neurophysiol Clin. 2002;32:175–192. doi: 10.1016/S0987-7053(02)00304-0.
    1. Shine JM, Matar E, Ward PB, Frank MJ, Moustafa AA, Pearson M, Naismith SL, Lewis SJ. Freezing of gait in Parkinson’s disease is associated with functional decoupling between the cognitive control network and the basal ganglia. Brain. 2013;136:3671–3681. doi: 10.1093/brain/awt272.
    1. Spaulding SJ, Barber B, Colby M, Cormack B, Mick T, Jenkins ME. Cueing and gait improvement among people with Parkinson’s disease: a meta-analysis. Arch Phys Med Rehabil. 2013;94(3):562–570. doi: 10.1016/j.apmr.2012.10.026.
    1. Stuart S, Vitorio R, Morris R, Martini DN, Fino PC, Mancini M. Cortical activity during walking and balance tasks in older adults and in people with Parkinson's disease: a structured review. Maturitas. 2018;113:53–72. doi: 10.1016/j.maturitas.2018.04.011.
    1. Szewczyk-Krolikowski K, Menke RA, Rolinski M, Duff E, Salimi-Khorshidi G, Filippini N, Zamboni G, Hu MT, Mackay CE. Functional connectivity in the basal ganglia network differentiates PD patients from controls. Neurology. 2014;83(3):208–214. doi: 10.1212/WNL.0000000000000592.
    1. Thaut MH, Abiru M. Rhythmic auditory stimulation in rehabilitation of movement disorders: a review of the current research. Music Percept. 2010;27:263–269. doi: 10.1525/mp.2010.27.4.263.
    1. Thaut MH, McIntosh GC, Hoemberg V. Neurobiological foundations of neurologic music therapy: rhythmic entrainment and the motor system. Front Psychol. 2014;5:1185.
    1. Thaut MH, Trimarchi PD, Parsons LM. Human brain basis of musical rhythm perception: common and distinct neural substrates for meter, tempo, and pattern. Brain Sci. 2014;4(2):428–452. doi: 10.3390/brainsci4020428.
    1. Thaut MH, Kenyon GP, Schauer ML, McIntosh GC. The connection between rhythmicity and brain function. IEEE Eng Med Biol. 1999;18:101–108. doi: 10.1109/51.752991.
    1. Thaut MH, McIntosh GC, Hoemberg V. Neurobiological foundations of neurologic music therapy: rhythmic entrainment and the motor system. Front Psychol. 2015. 10.3389/fpsyg.2015.01185.
    1. Thaut MH, McIntosh GC, Rice RR, Miller RA, Rathbun J, Brault JM. Rhythmic auditory stimulation in gait training for Parkinson’s disease patients. Mov Disord. 1996;11(2):193–200. doi: 10.1002/mds.870110213.
    1. Thaut MH, Miltner R, Lange HW, Hurt CP, Hoemberg V. Velocity modulation and rhythmic synchronization of gait in Huntington’s disease. Mov Disord. 1999;14(5):808–819. doi: 10.1002/1531-8257(199909)14:5<808::AID-MDS1014>;2-J.
    1. Tononi G, Sporns O, Edelman GM. Measures of degeneracy and redundancy in biological networks. Proc Natl Acad Sci U S A. 1999;96:3257–3262. doi: 10.1073/pnas.96.6.3257.
    1. Wagner J, Solis-Escalante T, Grieshofer P, Neuper C, Müller-Putz GR, Scherer R. Level of participation in robotic-assisted treadmill walking modulates midline sensorimotor EEG rhythms in able-bodied subjects. Neuroimage. 2012;63(3):1203–1211. doi: 10.1016/j.neuroimage.2012.08.019.
    1. Willems AM, Nieuwboer A, Chavret F, Desloovere K, Dom R, Rochester L, Jones D, Kwakkel G, Van Wegen E. 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. 2006;28(11):721–728. doi: 10.1080/09638280500386569.
    1. Wrisley DM, Marchetti GF, Kuharsky DK, Whitney SL. Reliability, internal consistency, and validity of data obtained with the functional gait assessment. Phys Ther. 2004;84(10):906–918.
    1. Wu O, Cloonan L, Mocking SJ, Bouts MJ, Copen WA, Cougo-Pinto PT, Fitzpatrick K, Kanakis A, Schaefer PW, Rosand J, Furie KL, Rost NS. Role of Acute Lesion Topography in Initial Ischemic Stroke Severity and Long-Term Functional Outcomes. Stroke. 2015;46(9):2438–44. doi: 10.1161/STROKEAHA.115.009643.
    1. Yeterian EH, Pandya DN. Corticostriatal connections of the superior temporal region in rhesus monkeys. J Comp Neurol. 1998;399(3):384–402. doi: 10.1002/(SICI)1096-9861(19980928)399:3<384::AID-CNE7>;2-X.

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