A training approach to improve stepping automaticity while dual-tasking in Parkinson's disease: A prospective pilot study

Taylor Chomiak, Alexander Watts, Nicole Meyer, Fernando V Pereira, Bin Hu, Taylor Chomiak, Alexander Watts, Nicole Meyer, Fernando V Pereira, Bin Hu

Abstract

Background: Deficits in motor movement automaticity in Parkinson's disease (PD), especially during multitasking, are early and consistent hallmarks of cognitive function decline, which increases fall risk and reduces quality of life. This study aimed to test the feasibility and potential efficacy of a wearable sensor-enabled technological platform designed for an in-home music-contingent stepping-in-place (SIP) training program to improve step automaticity during dual-tasking (DT).

Methods: This was a 4-week prospective intervention pilot study. The intervention uses a sensor system and algorithm that runs off the iPod Touch which calculates step height (SH) in real-time. These measurements were then used to trigger auditory (treatment group, music; control group, radio podcast) playback in real-time through wireless headphones upon maintenance of repeated large amplitude stepping. With small steps or shuffling, auditory playback stops, thus allowing participants to use anticipatory motor control to regain positive feedback. Eleven participants were recruited from an ongoing trial (Trial Number: ISRCTN06023392). Fear of falling (FES-I), general cognitive functioning (MoCA), self-reported freezing of gait (FOG-Q), and DT step automaticity were evaluated.

Results: While we found no significant effect of training on FES-I, MoCA, or FOG-Q, we did observe a significant group (music vs podcast) by training interaction in DT step automaticity (P<0.01).

Conclusion: Wearable device technology can be used to enable musically-contingent SIP training to increase motor automaticity for people living with PD. The training approach described here can be implemented at home to meet the growing demand for self-management of symptoms by patients.

Conflict of interest statement

The authors have no conflicts of interest to disclose.

Figures

Figure 1
Figure 1
Overview of study design. Schematic of the study design (Panel A). Participants were tested before (“pre”) and after (“post”) a 4-week in-home Ambulosono intervention program. Participants were asked to use the device in-home a minimum of 3 times per week, for 10 to 20 minutes per training session. Pre- and post assessments included The Falls Efficacy Scale International (FES-I) survey for fear of falling, the Freezing of Gait Questionnaire (FOG-Q) for freezing, and The Montreal Cognitive Assessment (MoCA) for general cognitive functioning. The dual-tasking test (DT test) consisted of measuring step-height decrement while SIP and simultaneously performing cognitive tasks (shown in Panel B). The order was standardized as done previously.[4] The control group was identical to the Ambulosono music group with the exception that instead of contingent music playback, they received contingent auditory feedback in the form of a CBC podcast (CBC Quirks and Quarks segment: The Sloth's Pharmaceutical Fur).
Figure 2
Figure 2
Basic concept of Ambulosono Music-Contingent Training. The basic concept of the Ambulosono technological platform is to computationally link auditory musical reward stimulation to scalable motor action. Based on an individuals’ mono-task SIP step height, a predefined step-height training threshold (red dotted line) can be set for auditory feedback. Therefore, during training, if step height (black trace) is above the threshold (red dotted line), music will play (green regions), while if step height is below the threshold, music does not play. This allows participants to use real-time step measurements and analytics that provide biofeedback to help self-motivate and self-activate reward networks with training.
Figure 3
Figure 3
Improvements in Dual-Tasking Step Automaticity Following Ambulosono Training. Plotted are the fixed effects parameter estimates (i.e., mean and standard error) from the linear mixed-effect model. Colors represent average changes in automaticity ratio (DT/MT) for each DT condition (i.e., immediate word recall, red; delayed word recall, green; serial subtract 5, yellow; serial subtract 7, purple). While there was no significant DT condition by training interaction (F(3,69) = 0.07, P = 0.98), there was a significant group (i.e., music vs podcast) by training interaction (F(1,69) = 9.20, P = 0.003).

References

    1. Kelly VE, Eusterbrock AJ, Shumway-Cook A. A review of dual-task walking deficits in people with Parkinson's disease: motor and cognitive contributions, mechanisms, and clinical implications. Parkinsons Dis 2012;2012:918719.
    1. Holtzer R, Wang C, Verghese J. The relationship between attention and gait in aging: facts and fallacies. Motor Control 2012;16:64–80.
    1. Yogev-Seligmann G, Hausdorff JM, Giladi N. The role of executive function and attention in gait. Mov Disord 2008;23:329–42. quiz 472.
    1. Chomiak T, Pereira FV, Meyer N, et al. A new quantitative method for evaluating freezing of gait and dual-attention task deficits in Parkinson's disease. J Neural Transm (Vienna) 2015;122:1523–31.
    1. Chomiak T, Meyer N, Cihal A, et al. Correlation between midline gait function performance and verbal fluency in patients with Parkinson's disease. Aging Clin Exp Res 2016;28:469–73.
    1. Speelman AD, van de Warrenburg BP, van Nimwegen M, et al. How might physical activity benefit patients with Parkinson disease? Nat Rev Neurol 2011;7:528–34.
    1. Chomiak T, Pereira FV, Clark TW, et al. Concurrent arm swing-stepping (CASS) can reveal gait start hesitation in Parkinson's patients with low self-efficacy and fear of falling. Aging Clin Exp Res 2015;27:457–63.
    1. Jones G, Federick JAB. The Canadian Centre for Activity and Aging's Home Support Exercise Program. Geriatr Aging 2003;6:48–9.
    1. Fraix V, Bastin J, David O, et al. Pedunculopontine nucleus area oscillations during stance, stepping and freezing in Parkinson's disease. PLoS ONE 2013;8:e83919.
    1. Chomiak T, Pereira FV, Hu B. The single-leg-stance test in Parkinson's disease. J Clin Med Res 2015;7:182–5.
    1. Petzinger GM, Fisher BE, McEwen S, et al. Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson's disease. Lancet Neurol 2013;12:716–26.
    1. Brauer SG, Morris ME. Can people with Parkinson's disease improve dual tasking when walking? Gait Posture 2010;31:229–33.
    1. Yogev-Seligmann G, Giladi N, Brozgol M, et al. A training program to improve gait while dual tasking in patients with Parkinson's disease: a pilot study. Arch Phys Med Rehabil 2012;93:176–81.
    1. Fernandes A, Rocha N, Santos R, et al. Effects of dual-task training on balance and executive functions in Parkinson's disease: a pilot study. Somatosens Mot Res 2015;32:122–7.
    1. de Vries NM, Nonnekes J, Bloem BR. Toward affordable falls prevention in Parkinson's disease. Mov Disord 2016;31:3–6.
    1. Avin KG, Hanke TA, Kirk-Sanchez N, et al. Management of falls in community-dwelling older adults: clinical guidance statement from the Academy of Geriatric Physical Therapy of the American Physical Therapy Association. Phys Ther 2015;95:815–34.
    1. Montero-Odasso M, Bherer L, Studenski S, et al. Mobility and Cognition in Seniors. Report from the 2008 Institute of Aging (CIHR) Mobility and Cognition Workshop. Can Geriatr J 2015;18:159–67.
    1. Salimpoor VN, Zald DH, Zatorre RJ, et al. Predictions and the brain: how musical sounds become rewarding. Trends Cogn Sci 2015;19:86–91.
    1. Ashby FG, Turner BO, Horvitz JC. Cortical and basal ganglia contributions to habit learning and automaticity. Trends Cogn Sci 2010;14:208–15.
    1. Norman G. Likert scales, levels of measurement and the “laws” of statistics. Adv Health Sci Educ Theory Pract 2010;15:625–32.
    1. Wu T, Hallett M, Chan P. Motor automaticity in Parkinson's disease. Neurobiol Dis 2015;82:226–34.
    1. Nantel J, de Solages C, Bronte-Stewart H. Repetitive stepping in place identifies and measures freezing episodes in subjects with Parkinson's disease. Gait Posture 2011;34:329–33.
    1. Giladi N, Shabtai H, Simon ES, et al. Construction of freezing of gait questionnaire for patients with Parkinsonism. Parkinsonism Relat Disord 2000;6:165–70.
    1. Jonasson SB, Nilsson MH, Lexell J. Psychometric properties of four fear of falling rating scales in people with Parkinson's disease. BMC Geriatr 2014;14:66.
    1. Hu B, Cihal A, Meyer N, et al. AmbuloSono: a sensorimotor contingent musical walking program for Parkinsons disease rehabilitation. J Parkinson Dis 2013;3:146.
    1. Cihal A, Clark TW, Luan K, et al. Validation of a novel GaitReminder Apple iPod application to measure real-time stride data and control music play in a gait rehabilitation program for people with Parkinson's disease. Mov Disord 213;28:S164.
    1. Friedmann PD, Rose JS, Swift R, et al. Trazodone for sleep disturbance after alcohol detoxification: a double-blind, placebo-controlled trial. Alcohol Clin Exp Res 2008;32:1652–60.
    1. Meireles J, Massano J. Cognitive impairment and dementia in Parkinson's disease: clinical features, diagnosis, and management. Front Neurol 2012;3:88.
    1. Mirelman A, Giladi N, Hausdorff JM. Body-fixed sensors for Parkinson disease. JAMA 2015;314:873–4.
    1. Kucinski A, Paolone G, Bradshaw M, et al. Modeling fall propensity in Parkinson's disease: deficits in the attentional control of complex movements in rats with cortical-cholinergic and striatal-dopaminergic deafferentation. J Neurosci 2013;33:16522–39.
    1. Polston JE, Rubbinaccio HY, Morra JT, et al. Music and methamphetamine: conditioned cue-induced increases in locomotor activity and dopamine release in rats. Pharmacol Biochem Behav 2010;98:54–61.
    1. Blood AJ, Zatorre RJ. Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc Natl Acad Sci USA 2001;98:11818–23.
    1. Boso M, Politi P, Barale F, et al. Neurophysiology and neurobiology of the musical experience. Funct Neurol 2006;21:187–91.
    1. Koelsch S. Towards a neural basis of music-evoked emotions. Trends Cogn Sci 2010;14:131–7.
    1. Schultz W. Reward functions of the basal ganglia. J Neural Transm (Vienna) 2016;123:679–93.
    1. MacInnes JJ, Dickerson KC, Chen NK, et al. Cognitive neurostimulation: learning to volitionally sustain ventral tegmental area activation. Neuron 2016;89:1331–42.
    1. Dobryakova E, Genova HM, DeLuca J, et al. The dopamine imbalance hypothesis of fatigue in multiple sclerosis and other neurological disorders. Front Neurol 2015;6:52.
    1. Hu B. Functional organization of lemniscal and nonlemniscal auditory thalamus. Exp Brain Res 2003;153:543–9.
    1. Bayona NA, Bitensky J, Salter K, et al. The role of task-specific training in rehabilitation therapies. Top Stroke Rehabil 2005;12:58–65.
    1. Steeves JA, Thompson DL, Bassett DR., Jr Energy cost of stepping in place while watching television commercials. Med Sci Sports Exerc 2012;44:330–5.

Source: PubMed

3
Subscribe