Therapeutic benefits of music-based synchronous finger tapping in Parkinson's disease-an fNIRS study protocol for randomized controlled trial in Dalian, China

Lanlan Pu, Nauman Khalid Qureshi, Joanne Ly, Bingwei Zhang, Fengyu Cong, William C Tang, Zhanhua Liang, Lanlan Pu, Nauman Khalid Qureshi, Joanne Ly, Bingwei Zhang, Fengyu Cong, William C Tang, Zhanhua Liang

Abstract

Background: Music therapy improves neuronal activity and connectivity of healthy persons and patients with clinical symptoms of neurological diseases like Parkinson's disease, Alzheimer's disease, and major depression. Despite the plethora of publications that have reported the positive effects of music interventions, little is known about how music improves neuronal activity and connectivity in afflicted patients.

Methods: For patients suffering from Parkinson's disease (PD), we propose a daily 25-min music-based synchronous finger tapping (SFT) intervention for 8 weeks. Eligible participants with PD are split into two groups: an intervention group and a control arm. In addition, a third cohort of healthy controls will be recruited. Assessment of finger tapping performances, the Unified Parkinson's Disease Rating Scale (UPDRS), an n-back test, the Montreal Cognitive Assessment (MoCA), as well as oxygenated hemoglobin (HbO2), deoxygenated hemoglobin (HbR), and total hemoglobin activation collected by functional near-infrared spectroscopy (fNIRS) are measured at baseline, week 4 (during), week 8 (post), and week 12 (retention) of the study. Data collected from the two PD groups are compared to baseline performances from healthy controls.

Discussion: This exploratory prospective trial study investigates the cortical neuronal activity and therapeutic effects associated with an auditory external cue used to induce automatic and implicit synchronous finger tapping in patients diagnosed with PD. The extent to which the intervention is effective may be dependent on the severity of the disease. The study's findings are used to inform larger clinical studies for optimization and further exploration of the therapeutic effects of movement-based music therapy on neural activity in neurological diseases.

Trial registration: ClinicalTrials.gov NCT04212897 . Registered on December 30, 2019. The participant recruitment and study protocol have received ethical approval from the First Affiliated Hospital of Dalian Medical University. The hospital Protocol Record number is PJ-KY-2019-123. The protocol was named "fNIRS Studies of Music Intervention of Parkinson's Disease." The current protocol is version 1.1, revised on September 1, 2020.

Keywords: Explicit and implicit timing; Motor-control; Music therapy; Parkinson’s disease; Randomized controlled trials; Synchronous finger tapping; fNIRS.

Figures

Fig. 1
Fig. 1
Expected trial plan. Not included in the diagram are excluded participants that may stop participation at any time during weeks 0–12 due to various reasons including failure to meet inclusion criteria or inability to continue at-home intervention. The intervention tasks are 25 min total, with two 10-min sets with a 5-min break between each set
Fig. 2
Fig. 2
Standard Protocol Items: Recommendation for Interventional Trials (SPIRIT). W, weeks; SFT, synchronous finger tapping; HC, healthy control; CFT, continuous finger tapping; fNIRS, functional near-infrared spectroscopy; MoCA, Montreal Cognitive Assessment Test; UPDRS, Unified Parkinson’s Disease Rating Scale
Fig. 3
Fig. 3
Schematic of experimental paradigm. BR, baseline rest; SFT, synchronous finger tapping; CFT, continuous finger tapping. In the SFT task, visual stimuli will appear at three different rates 1000 ms, 1500 ms, and 2000 ms respectively

References

    1. Beitz JM. Parkinson’s disease: a review. Front Biosci. 2014;6:65–74. doi: 10.2741/S415.
    1. Auksztulewicz R, Myers NE, Schnupp JW, Nobre AC. Rhythmic temporal expectation boosts neural activity by increasing neural gain. J Neurosci. 2019;39(49):9806–9817. doi: 10.1523/JNEUROSCI.0925-19.2019.
    1. Nessler JA, De Leone CJ, Gilliland S. Nonlinear time series analysis of knee and ankle kinematics during side by side treadmill walking. Chaos. 2009;19(2):026104. doi: 10.1063/1.3125762.
    1. Nessler JA, McMillan D, Schoulten M, Shallow T, Stewart B, De Leone C. Side by side treadmill walking with intentionally desynchronized gait. Ann Biomed Eng. 2013;41(8):1680–1691. doi: 10.1007/s10439-012-0657-6.
    1. Zivotofsky AZ, Hausdorff JM. The sensory feedback mechanisms enabling couples to walk synchronously: an initial investigation. J Neuroeng Rehabil. 2007;4:28. doi: 10.1186/1743-0003-4-28.
    1. Thaut MH, Miller RA, Schauer LM. Multiple synchronization strategies in rhythmic sensorimotor tasks: phase vs period correction. Biol Cybern. 1998;79(3):241–250. doi: 10.1007/s004220050474.
    1. Large EW, Fink P, Kelso JAS. Tracking simple and complex sequences. Psychol Res. 2002;66:3–17. doi: 10.1007/s004260100069.
    1. Thaut M, McIntosh GC, Hoemberg V. Neurobiological foundations of neurologic music therapy: rhythmic entrainment and the motor system. Front Psychol. 2015;5:1185. doi: 10.3389/fpsyg.2014.01185.
    1. Hickey P, Stacy M. Deep brain stimulation: a paradigm shifting approach to treat Parkinson’s disease. Front Neurosci. 2016;10:173. doi: 10.3389/fnins.2016.00173.
    1. Malapani C, Rakitin B, Levy R, Meck WH, Deweer B, Dubois B, et al. Coupled temporal memories in Parkinson’s disease: a dopamine-related dysfunction. J Cogn Neurosci. 1998;10(3):316–331. doi: 10.1162/089892998562762.
    1. Pascual-Sedano B, Kulisevsky J, Barbanoj M, García-Sánchez C, Campolongo A, Gironell A, et al. Levodopa and executive performance in Parkinson’s disease: a randomized study. J Int Neuropsychol Soc. 2008;14(5):832–841. doi: 10.1017/S1355617708081010.
    1. Collomb-Clerc A, Welter ML. Effects of deep brain stimulation on balance and gait in patients with Parkinson’s disease: a systematic neurophysiological review. Neurophysiol Clin. 2015;45(4–5):371–388. doi: 10.1016/j.neucli.2015.07.001.
    1. Cancela J, Moreno EM, Arredondo MT, Bonato P. 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society. 2014. Designing auditory cues for Parkinson’s disease gait rehabilitation; pp. 5852–5855.
    1. Braun T, Haase M, Thaut MH. Rhythmic priming across effector systems: a randomized controlled trial with Parkinson’s disease patients. Hum Mov Sci. 2019;64:355–365. doi: 10.1016/j.humov.2019.03.001.
    1. Meck WH, Benson AM. Dissecting the brain’s internal clock: how frontal-striatal circuitry keeps time and shifts attention. Brain Cogn. 2002;48(1):195–211. doi: 10.1006/brcg.2001.1313.
    1. Lewis PA, Miall RC. Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging. Curr Opin Neurobiol. 2003;13(2):250–255. doi: 10.1016/S0959-4388(03)00036-9.
    1. Avanzino L, Pelosin E, Vicario CM, Lagravinese G, Abbruzzese G, Martino D. Time processing and motor control in movement disorders. Front Hum Neurosci. 2016;10:631. doi: 10.3389/fnhum.2016.00631.
    1. Wiener M, Turkeltaub P, Coslett HB. The image of time: a voxel-wise meta-analysis. Neuroimage. 2010;49(2):1728–1740. doi: 10.1016/j.neuroimage.2009.09.064.
    1. Repp BH, Su YH. Sensorimotor synchronization: a review of recent research (2006-2012) Psychon Bull Rev. 2013;20(3):403–452. doi: 10.3758/s13423-012-0371-2.
    1. Beudel M, Galama S, Leenders KL, De Jong BM. Time estimation in Parkinson’s disease and degenerative cerebellar disease. Neuroreport. 2008;19(10):1055–1059. doi: 10.1097/WNR.0b013e328303b7b9.
    1. Merchant H, Grahn J, Trainor L, Rohrmeier M, Fitch WT. Finding the beat: a neural perspective across humans and non-human primates. Philos Trans R Soc B Biol Sci. 2015;370(1664):20140093. doi: 10.1098/rstb.2014.0093.
    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. O’Boyle DJ, Freeman JS, Cody FW. The accuracy and precision of timing of self-paced, repetitive movements in subjects with Parkinson’s disease. Brain. 1996;119(1):51–70. doi: 10.1093/brain/119.1.51.
    1. Craig C, Pepping GJ, Grealy M. Intercepting beats in predesignated target zones. Exp Brain Res. 2005;165(4):490–504. doi: 10.1007/s00221-005-2322-x.
    1. Tokushige SI, Terao Y, Matsuda S, Furubayashi T, Sasaki T, Inomata-Terada S, et al. Does the clock tick slower or faster in Parkinson’s disease? - Insights gained from the synchronized tapping task. Front Psychol. 2018;9:1178. doi: 10.3389/fpsyg.2018.01178.
    1. Grahn JA, Brett M. Rhythm perception in motor areas of the brain. J Cogn Neurosci. 2007;19(5):893–906. doi: 10.1162/jocn.2007.19.5.893.
    1. Grahn JA, Rowe JB. Feeling the beat: premotor and striatal interactions in musicians and nonmusicians during beat perception. 2009;29(23):7540-8.
    1. Lewis MM, Slagle CG, Smith AB, Truong Y, Bai P, McKeown MJ, et al. Task specific influences of Parkinson’s disease on the striato-thalamo-cortical and cerebello-thalamo-cortical motor circuitries. Neuroscience. 2007;147(1):224–235. doi: 10.1016/j.neuroscience.2007.04.006.
    1. Nombela C, Hughes LE, Owen AM, Grahn JA. Into the groove: can rhythm influence Parkinson’s disease? Neurosci Biobehav Rev. 2013;37(10):2564–2570. doi: 10.1016/j.neubiorev.2013.08.003.
    1. Mahoney JR, Holtze R, Izzetoglu M, Zemon V, Verghese J, Allali G. The role of prefrontal cortex during postural control in Parkinsonian syndromes a functional near-infrared spectroscopy study. Brain Res. 2015;1633:126–138. doi: 10.1016/j.brainres.2015.10.053.
    1. Maidan I, Bernad-Elazari H, Gazit E, Giladi N, Hausdorff JM, Mirelman A. Changes in oxygenated hemoglobin link freezing of gait to frontal activation in patients with Parkinson disease: an fNIRS study of transient motor-cognitive failures. J Neurol. 2015;262(4):899–908. doi: 10.1007/s00415-015-7650-6.
    1. Thumm PC, Maidan I, Brozgol M, Shustak S, Gazit E, Shema Shiratzki S, et al. Treadmill walking reduces pre-frontal activation in patients with Parkinson’s disease. Gait Posture. 2018;62:384–387. doi: 10.1016/j.gaitpost.2018.03.041.
    1. Nieuwhof F, Reelick MF, Maidan I, Mirelman A, Hausdorff JM, Olde Rikkert MGM, et al. Measuring prefrontal cortical activity during dual task walking in patients with Parkinson’s disease: feasibility of using a new portable fNIRS device. Pilot Feasibility Stud. 2016;2:59. doi: 10.1186/s40814-016-0099-2.
    1. Klempir O, Krupicka R, Mehnert J, Cejka V, Polakova K, Brozova H, et al. Reshaping cortical activity with subthalamic stimulation in Parkinson’s disease during finger tapping and gait mapped by near infrared spectroscopy. J Appl Biomed. 2019;17(3):157–166. doi: 10.32725/jab.2019.014.
    1. Gervain J, Mehler J, Werker JF, Nelson CA, Csibra G, Lloyd-Fox S, et al. Near-infrared spectroscopy: a report from the McDonnell infant methodology consortium. Dev Cogn Neurosci. 2011;1(1):22–46. doi: 10.1016/j.dcn.2010.07.004.
    1. Schreppel T, Egetemeir J, Schecklmann M, Plichta MM, Pauli P, Ellgring H, et al. Activation of the prefrontal cortex in working memory and interference resolution processes assessed with near-infrared spectroscopy. Neuropsychobiology. 2008;57(4):188–193. doi: 10.1159/000147473.
    1. Qureshi NK, Naseer N, Noori FM, Nazeer H, Khan RA, Saleem S. Enhancing classification performance of functional near-infrared spectroscopy-brain-computer interface using adaptive estimation of general linear model coefficients. Front Neurorobot. 2017;11:33. doi: 10.3389/fnbot.2017.00033.
    1. Naseer N, Hong K-S. fNIRS-based brain-computer interfaces: a review. Front Hum Neurosci. 2015;9:3.
    1. Goetz CG. The Unified Parkinson’s Disease Rating Scale (UPDRS).pdf. Mov Disord. 2003;18(7):738–750. doi: 10.1002/mds.10473.
    1. Beato R, Levy R, Pillon B, Vidal C, Du Montcel ST, Deweer B, et al. Working memory in Parkinson’s disease patients: clinical features and response to levodopa. Arq Neuropsiquiatr. 2008;66(2A):147–151. doi: 10.1590/S0004-282X2008000200001.
    1. Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53(4):695–699. doi: 10.1111/j.1532-5415.2005.53221.x.
    1. Ziad Nasreddine MD. MoCA Montreal cognitive assessment [Internet]. Available from: .
    1. Bienkiewicz MMN, Craig CM. Parkinson’s is time on your side? Evidence for difficulties with sensorimotor synchronization. Front Neurol. 2015;6:249. doi: 10.3389/fneur.2015.00249.

Source: PubMed

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