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Published in: Journal of NeuroEngineering and Rehabilitation 1/2019

Open Access 01-12-2019 | Parkinson's Disease | Research

Disentangling stability and flexibility degrees in Parkinson’s disease using a computational postural control model

Authors: Zahra Rahmati, Alfred C. Schouten, Saeed Behzadipour, Ghorban Taghizadeh, Keikhosrow Firoozbakhsh

Published in: Journal of NeuroEngineering and Rehabilitation | Issue 1/2019

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Abstract

Background

Impaired postural control in Parkinson’s disease (PD) seriously compromises life quality. Although balance training improves mobility and postural stability, lack of quantitative studies on the neurophysiological mechanisms of balance training in PD impedes the development of patient-specific therapies. We evaluated the effects of a balance-training program using functional balance and mobility tests, posturography, and a postural control model.

Methods

Center-of-pressure (COP) data of 40 PD patients before and after a 12-session balance-training program, and 20 healthy control subjects were recorded in four conditions with two tasks on a rigid surface (R-tasks) and two on foam. A postural control model was fitted to describe the posturography data. The model comprises a neuromuscular controller, a time delay, and a gain scaling the internal disturbance torque.

Results

Patients’ axial rigidity before training resulted in slower COP velocity in R-tasks; which was reflected as lower internal torque gain. Furthermore, patients exhibited poor stability on foam, remarked by abnormal higher sway amplitude. Lower control parameters as well as higher time delay were responsible for patients’ abnormal high sway amplitude. Balance training improved all clinical scores on functional balance and mobility. Consistently, improved ‘flexibility’ appeared as enhanced sway velocity (increased internal torque gain). Balance training also helped patients to develop the ‘stability degree’ (increase control parameters), and to respond more quickly in unstable condition of stance on foam.

Conclusions

Projection of the common posturography measures on a postural control model provided a quantitative framework for unraveling the neurophysiological factors and different recovery mechanisms in impaired postural control in PD.
Appendix
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Literature
1.
go back to reference Nantel J, McDonald JC, Bronte-Stewart H. Effect of medication and STN-DBS on postural control in subjects with Parkinson’s disease. Parkinsonism Relat Disord. 2012;18(3):285–9.PubMedCrossRef Nantel J, McDonald JC, Bronte-Stewart H. Effect of medication and STN-DBS on postural control in subjects with Parkinson’s disease. Parkinsonism Relat Disord. 2012;18(3):285–9.PubMedCrossRef
2.
go back to reference Diab KS, Hale LA, Waters DL, Skinner MA. Factors contributing to postural instability in patients with idiopathic Parkinson’s disease. Phys Ther Rev. 2014;19(5):302–27.CrossRef Diab KS, Hale LA, Waters DL, Skinner MA. Factors contributing to postural instability in patients with idiopathic Parkinson’s disease. Phys Ther Rev. 2014;19(5):302–27.CrossRef
3.
go back to reference Pasma J, Engelhart D, Schouten A, Van der Kooij H, Maier A, Meskers C. Impaired standing balance: the clinical need for closing the loop. Neuroscience. 2014;267:157–65.PubMedCrossRef Pasma J, Engelhart D, Schouten A, Van der Kooij H, Maier A, Meskers C. Impaired standing balance: the clinical need for closing the loop. Neuroscience. 2014;267:157–65.PubMedCrossRef
4.
go back to reference Benatru I, Vaugoyeau M, Azulay J-P. Postural disorders in Parkinson’s disease. Neurophysiol Clin/Clin Neurophysiol. 2008;38(6):459–65.CrossRef Benatru I, Vaugoyeau M, Azulay J-P. Postural disorders in Parkinson’s disease. Neurophysiol Clin/Clin Neurophysiol. 2008;38(6):459–65.CrossRef
5.
go back to reference Kim SD, Allen NE, Canning CG, Fung VS. Postural instability in patients with Parkinson’s disease. CNS Drugs. 2013;27(2):97–112.PubMedCrossRef Kim SD, Allen NE, Canning CG, Fung VS. Postural instability in patients with Parkinson’s disease. CNS Drugs. 2013;27(2):97–112.PubMedCrossRef
6.
go back to reference Horak F, Frank J, Nutt J. Effects of dopamine on postural control in parkinsonian subjects: scaling, set, and tone. J Neurophysiol. 1996;75(6):2380–96.PubMedCrossRef Horak F, Frank J, Nutt J. Effects of dopamine on postural control in parkinsonian subjects: scaling, set, and tone. J Neurophysiol. 1996;75(6):2380–96.PubMedCrossRef
7.
go back to reference Nardone A, Schieppati M. Balance in Parkinson's disease under static and dynamic conditions. Mov Disord. 2006;21(9):1515–20.PubMedCrossRef Nardone A, Schieppati M. Balance in Parkinson's disease under static and dynamic conditions. Mov Disord. 2006;21(9):1515–20.PubMedCrossRef
8.
go back to reference Wiesmeier IK, Dalin D, Wehrle A, Granacher U, Muehlbauer T, Dietterle J, et al. Balance training enhances vestibular function and reduces overactive proprioceptive feedback in elderly. Front Aging Neurosci. 2017;9:273.PubMedPubMedCentralCrossRef Wiesmeier IK, Dalin D, Wehrle A, Granacher U, Muehlbauer T, Dietterle J, et al. Balance training enhances vestibular function and reduces overactive proprioceptive feedback in elderly. Front Aging Neurosci. 2017;9:273.PubMedPubMedCentralCrossRef
9.
go back to reference Maurer C, Peterka RJ. A new interpretation of spontaneous sway measures based on a simple model of human postural control. J Neurophysiol. 2005;93(1):189–200.PubMedCrossRef Maurer C, Peterka RJ. A new interpretation of spontaneous sway measures based on a simple model of human postural control. J Neurophysiol. 2005;93(1):189–200.PubMedCrossRef
10.
go back to reference Mancini M, Salarian A, Carlson-Kuhta P, Zampieri C, King L, Chiari L, et al. ISway: a sensitive, valid and reliable measure of postural control. J Neuroeng Rehabil. 2012;9(1):59.PubMedPubMedCentralCrossRef Mancini M, Salarian A, Carlson-Kuhta P, Zampieri C, King L, Chiari L, et al. ISway: a sensitive, valid and reliable measure of postural control. J Neuroeng Rehabil. 2012;9(1):59.PubMedPubMedCentralCrossRef
11.
go back to reference Maurer C, Mergner T, Xie J, Faist M, Pollak P, Lücking C. Effect of chronic bilateral subthalamic nucleus (STN) stimulation on postural control in Parkinson’s disease. Brain. 2003;126(5):1146–63.PubMedCrossRef Maurer C, Mergner T, Xie J, Faist M, Pollak P, Lücking C. Effect of chronic bilateral subthalamic nucleus (STN) stimulation on postural control in Parkinson’s disease. Brain. 2003;126(5):1146–63.PubMedCrossRef
12.
go back to reference Rocchi L, Chiari L, Horak F. Effects of deep brain stimulation and levodopa on postural sway in Parkinson's disease. J Neurol Neurosurg Psychiatry. 2002;73(3):267–74.PubMedPubMedCentralCrossRef Rocchi L, Chiari L, Horak F. Effects of deep brain stimulation and levodopa on postural sway in Parkinson's disease. J Neurol Neurosurg Psychiatry. 2002;73(3):267–74.PubMedPubMedCentralCrossRef
13.
go back to reference Maurer C, Mergner T, Peterka R. Abnormal resonance behavior of the postural control loop in Parkinson’s disease. Exp Brain Res. 2004;157(3):369–76.PubMedCrossRef Maurer C, Mergner T, Peterka R. Abnormal resonance behavior of the postural control loop in Parkinson’s disease. Exp Brain Res. 2004;157(3):369–76.PubMedCrossRef
14.
go back to reference Frenklach A, Louie S, Koop MM, Bronte-Stewart H. Excessive postural sway and the risk of falls at different stages of Parkinson's disease. Mov Disord. 2009;24(3):377–85.PubMedCrossRef Frenklach A, Louie S, Koop MM, Bronte-Stewart H. Excessive postural sway and the risk of falls at different stages of Parkinson's disease. Mov Disord. 2009;24(3):377–85.PubMedCrossRef
15.
go back to reference Singh NB, Taylor WR, Madigan ML, Nussbaum MA. The spectral content of postural sway during quiet stance: influences of age, vision and somatosensory inputs. J Electromyogr Kinesiol. 2012;22(1):131–6.PubMedCrossRef Singh NB, Taylor WR, Madigan ML, Nussbaum MA. The spectral content of postural sway during quiet stance: influences of age, vision and somatosensory inputs. J Electromyogr Kinesiol. 2012;22(1):131–6.PubMedCrossRef
16.
go back to reference Schmit JM, Riley MA, Dalvi A, Sahay A, Shear PK, Shockley KD, et al. Deterministic center of pressure patterns characterize postural instability in Parkinson’s disease. Exp Brain Res. 2006;168(3):357–67.PubMedCrossRef Schmit JM, Riley MA, Dalvi A, Sahay A, Shear PK, Shockley KD, et al. Deterministic center of pressure patterns characterize postural instability in Parkinson’s disease. Exp Brain Res. 2006;168(3):357–67.PubMedCrossRef
17.
go back to reference Engelhart D, Boonstra TA, Aarts RG, Schouten AC, van der Kooij H. Comparison of closed-loop system identification techniques to quantify multi-joint human balance control. Annu Rev Control. 2016;41:58–70.CrossRef Engelhart D, Boonstra TA, Aarts RG, Schouten AC, van der Kooij H. Comparison of closed-loop system identification techniques to quantify multi-joint human balance control. Annu Rev Control. 2016;41:58–70.CrossRef
18.
19.
go back to reference Boonstra TA, Schouten AC, van Vugt JP, Bloem BR, van der Kooij H. Parkinson's disease patients compensate for balance control asymmetry. J Neurophysiol. 2014;112(12):3227–39.PubMedCrossRef Boonstra TA, Schouten AC, van Vugt JP, Bloem BR, van der Kooij H. Parkinson's disease patients compensate for balance control asymmetry. J Neurophysiol. 2014;112(12):3227–39.PubMedCrossRef
20.
go back to reference Mehdizadeh M. The effect of sensory re-weighting as a method of balance exercise on postural control in people with Parkinson's disease: MSc Thesis, Iran University of Medical Science; 2016. Mehdizadeh M. The effect of sensory re-weighting as a method of balance exercise on postural control in people with Parkinson's disease: MSc Thesis, Iran University of Medical Science; 2016.
21.
go back to reference Rahmati Z, Behzadipour S, Schouten AC, Taghizadeh G, editors. A postural control model to assess the improvement of balance rehabilitation in Parkinson's disease. In: 2018 7th IEEE International Conference on Biomedical Robotics and Biomechatronics (Biorob); 2018: pp. 1019-1024. IEEE. Rahmati Z, Behzadipour S, Schouten AC, Taghizadeh G, editors. A postural control model to assess the improvement of balance rehabilitation in Parkinson's disease. In: 2018 7th IEEE International Conference on Biomedical Robotics and Biomechatronics (Biorob); 2018: pp. 1019-1024. IEEE.
22.
go back to reference Scoppa F, Capra R, Gallamini M, Shiffer R. Clinical stabilometry standardization: basic definitions–acquisition interval–sampling frequency. Gait Posture. 2013;37(2):290–2.PubMedCrossRef Scoppa F, Capra R, Gallamini M, Shiffer R. Clinical stabilometry standardization: basic definitions–acquisition interval–sampling frequency. Gait Posture. 2013;37(2):290–2.PubMedCrossRef
23.
go back to reference Carpenter MG, Frank JS, Winter DA, Peysar GW. Sampling duration effects on Centre of pressure summary measures. Gait Posture. 2001;13(1):35–40.PubMedCrossRef Carpenter MG, Frank JS, Winter DA, Peysar GW. Sampling duration effects on Centre of pressure summary measures. Gait Posture. 2001;13(1):35–40.PubMedCrossRef
24.
go back to reference van der Kooij H, Campbell AD, Carpenter MG. Sampling duration effects on Centre of pressure descriptive measures. Gait Posture. 2011;34(1):19–24.PubMedCrossRef van der Kooij H, Campbell AD, Carpenter MG. Sampling duration effects on Centre of pressure descriptive measures. Gait Posture. 2011;34(1):19–24.PubMedCrossRef
25.
go back to reference Paillard T, Noé F. Techniques and methods for testing the postural function in healthy and pathological subjects. Biomed Res Int. 2015;2015:891390.PubMedPubMedCentral Paillard T, Noé F. Techniques and methods for testing the postural function in healthy and pathological subjects. Biomed Res Int. 2015;2015:891390.PubMedPubMedCentral
26.
go back to reference Prieto TE, Myklebust JB, Hoffmann RG, Lovett EG, Myklebust BM. Measures of postural steadiness: differences between healthy young and elderly adults. IEEE Trans Biomed Eng. 1996;43(9):956–66.PubMedCrossRef Prieto TE, Myklebust JB, Hoffmann RG, Lovett EG, Myklebust BM. Measures of postural steadiness: differences between healthy young and elderly adults. IEEE Trans Biomed Eng. 1996;43(9):956–66.PubMedCrossRef
27.
go back to reference Ruhe A, Fejer R, Walker B. The test–retest reliability of Centre of pressure measures in bipedal static task conditions–a systematic review of the literature. Gait Posture. 2010;32(4):436–45.PubMedCrossRef Ruhe A, Fejer R, Walker B. The test–retest reliability of Centre of pressure measures in bipedal static task conditions–a systematic review of the literature. Gait Posture. 2010;32(4):436–45.PubMedCrossRef
28.
go back to reference Collins JJ, De Luca CJ. Open-loop and closed-loop control of posture: a random-walk analysis of center-of-pressure trajectories. Exp Brain Res. 1993;95(2):308–18.PubMedCrossRef Collins JJ, De Luca CJ. Open-loop and closed-loop control of posture: a random-walk analysis of center-of-pressure trajectories. Exp Brain Res. 1993;95(2):308–18.PubMedCrossRef
29.
30.
go back to reference Winter DA. Biomechanics and motor control of human movement. Wiley; 2009. Winter DA. Biomechanics and motor control of human movement. Wiley; 2009.
31.
go back to reference Wiesmeier IK, Dalin D, Maurer C. Elderly use proprioception rather than visual and vestibular cues for postural motor control. Front Aging Neurosci. 2015;7:97.PubMedPubMedCentralCrossRef Wiesmeier IK, Dalin D, Maurer C. Elderly use proprioception rather than visual and vestibular cues for postural motor control. Front Aging Neurosci. 2015;7:97.PubMedPubMedCentralCrossRef
32.
go back to reference Nagy E, Feher-Kiss A, Barnai M, Domján-Preszner A, Angyan L, Horvath G. Postural control in elderly subjects participating in balance training. Eur J Appl Physiol. 2007;100(1):97–104.PubMedCrossRef Nagy E, Feher-Kiss A, Barnai M, Domján-Preszner A, Angyan L, Horvath G. Postural control in elderly subjects participating in balance training. Eur J Appl Physiol. 2007;100(1):97–104.PubMedCrossRef
33.
go back to reference Esculier J-F, Vaudrin J, Bériault P, Gagnon K, Tremblay LE. Home-based balance training programme using Wii fit with balance board for Parkinson's disease: a pilot study. J Rehabil Med. 2012;44(2):144–50.PubMedCrossRef Esculier J-F, Vaudrin J, Bériault P, Gagnon K, Tremblay LE. Home-based balance training programme using Wii fit with balance board for Parkinson's disease: a pilot study. J Rehabil Med. 2012;44(2):144–50.PubMedCrossRef
34.
go back to reference Johnson L, Putrino D, James I, Rodrigues J, Stell R, Thickbroom G, et al. The effects of a supervised Pilates training program on balance in Parkinson’s disease. Adv Park Dis. 2013;2(02):58–61. Johnson L, Putrino D, James I, Rodrigues J, Stell R, Thickbroom G, et al. The effects of a supervised Pilates training program on balance in Parkinson’s disease. Adv Park Dis. 2013;2(02):58–61.
35.
go back to reference Bello O, Sánchez JA, Lopez-Alonso V, Márquez G, Morenilla L, Castro X, et al. The effects of treadmill or overground walking training program on gait in Parkinson's disease. Gait Posture. 2013;38(4):590–5.PubMedCrossRef Bello O, Sánchez JA, Lopez-Alonso V, Márquez G, Morenilla L, Castro X, et al. The effects of treadmill or overground walking training program on gait in Parkinson's disease. Gait Posture. 2013;38(4):590–5.PubMedCrossRef
36.
go back to reference Hue OA, Seynnes O, Ledrole D, Colson SS, Bernard P-L. Effects of a physical activity program on postural stability in older people. Aging Clin Exp Res. 2004;16(5):356–62.PubMedCrossRef Hue OA, Seynnes O, Ledrole D, Colson SS, Bernard P-L. Effects of a physical activity program on postural stability in older people. Aging Clin Exp Res. 2004;16(5):356–62.PubMedCrossRef
37.
go back to reference Strang AJ, Haworth J, Hieronymus M, Walsh M, Smart LJ. Structural changes in postural sway lend insight into effects of balance training, vision, and support surface on postural control in a healthy population. Eur J Appl Physiol. 2011;111(7):1485–95.PubMedCrossRef Strang AJ, Haworth J, Hieronymus M, Walsh M, Smart LJ. Structural changes in postural sway lend insight into effects of balance training, vision, and support surface on postural control in a healthy population. Eur J Appl Physiol. 2011;111(7):1485–95.PubMedCrossRef
38.
go back to reference Carpenter M, Allum J, Honegger F, Adkin A, Bloem B. Postural abnormalities to multidirectional stance perturbations in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2004;75(9):1245–54.PubMedPubMedCentralCrossRef Carpenter M, Allum J, Honegger F, Adkin A, Bloem B. Postural abnormalities to multidirectional stance perturbations in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2004;75(9):1245–54.PubMedPubMedCentralCrossRef
39.
go back to reference Raymakers J, Samson M, Verhaar H. The assessment of body sway and the choice of the stability parameter (s). Gait Posture. 2005;21(1):48–58.PubMedCrossRef Raymakers J, Samson M, Verhaar H. The assessment of body sway and the choice of the stability parameter (s). Gait Posture. 2005;21(1):48–58.PubMedCrossRef
40.
go back to reference Błaszczyk J, Orawiec R, Duda-Kłodowska D, Opala G. Assessment of postural instability in patients with Parkinson’s disease. Exp Brain Res. 2007;183(1):107–14.PubMedCrossRef Błaszczyk J, Orawiec R, Duda-Kłodowska D, Opala G. Assessment of postural instability in patients with Parkinson’s disease. Exp Brain Res. 2007;183(1):107–14.PubMedCrossRef
41.
go back to reference Holmes J, Jenkins M, Johnson AM, Adams S, Spaulding S. Dual-task interference: the effects of verbal cognitive tasks on upright postural stability in Parkinson's disease. Park Dis. 2010;2010:696492. Holmes J, Jenkins M, Johnson AM, Adams S, Spaulding S. Dual-task interference: the effects of verbal cognitive tasks on upright postural stability in Parkinson's disease. Park Dis. 2010;2010:696492.
42.
go back to reference Termoz N, Halliday SE, Winter DA, Frank JS, Patla AE, Prince F. The control of upright stance in young, elderly and persons with Parkinson's disease. Gait Posture. 2008;27(3):463–70.PubMedCrossRef Termoz N, Halliday SE, Winter DA, Frank JS, Patla AE, Prince F. The control of upright stance in young, elderly and persons with Parkinson's disease. Gait Posture. 2008;27(3):463–70.PubMedCrossRef
43.
go back to reference King L, Salarian A, Mancini M, Priest K, Nutt J, Serdar A, et al. Exploring outcome measures for exercise intervention in people with Parkinson’s disease. Parkinson’s Dis. 2013;2013:572134. King L, Salarian A, Mancini M, Priest K, Nutt J, Serdar A, et al. Exploring outcome measures for exercise intervention in people with Parkinson’s disease. Parkinson’s Dis. 2013;2013:572134.
44.
go back to reference Ni M, Signorile JF, Mooney K, Balachandran A, Potiaumpai M, Luca C, et al. Comparative effect of power training and high-speed yoga on motor function in older patients with Parkinson disease. Arch Phys Med Rehabil. 2016;97(3):345–54. e15.PubMedCrossRef Ni M, Signorile JF, Mooney K, Balachandran A, Potiaumpai M, Luca C, et al. Comparative effect of power training and high-speed yoga on motor function in older patients with Parkinson disease. Arch Phys Med Rehabil. 2016;97(3):345–54. e15.PubMedCrossRef
45.
go back to reference Rocchi L, Chiari L, Cappello A, Horak FB. Identification of distinct characteristics of postural sway in Parkinson's disease: a feature selection procedure based on principal component analysis. Neurosci Lett. 2006;394(2):140–5.PubMedCrossRef Rocchi L, Chiari L, Cappello A, Horak FB. Identification of distinct characteristics of postural sway in Parkinson's disease: a feature selection procedure based on principal component analysis. Neurosci Lett. 2006;394(2):140–5.PubMedCrossRef
46.
go back to reference Nallegowda M, Singh U, Handa G, Khanna M, Wadhwa S, Yadav SL, et al. Role of sensory input and muscle strength in maintenance of balance, gait, and posture in Parkinson’s disease: a pilot study. Am J Phys Med Rehabil. 2004;83(12):898–908.PubMedCrossRef Nallegowda M, Singh U, Handa G, Khanna M, Wadhwa S, Yadav SL, et al. Role of sensory input and muscle strength in maintenance of balance, gait, and posture in Parkinson’s disease: a pilot study. Am J Phys Med Rehabil. 2004;83(12):898–908.PubMedCrossRef
47.
go back to reference Panyakaew P, Anan C, Bhidayasiri R. Visual deprivation elicits subclinical postural inflexibilities in early Parkinson's disease. J Neurol Sci. 2015;349(1–2):214–9.PubMedCrossRef Panyakaew P, Anan C, Bhidayasiri R. Visual deprivation elicits subclinical postural inflexibilities in early Parkinson's disease. J Neurol Sci. 2015;349(1–2):214–9.PubMedCrossRef
Metadata
Title
Disentangling stability and flexibility degrees in Parkinson’s disease using a computational postural control model
Authors
Zahra Rahmati
Alfred C. Schouten
Saeed Behzadipour
Ghorban Taghizadeh
Keikhosrow Firoozbakhsh
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of NeuroEngineering and Rehabilitation / Issue 1/2019
Electronic ISSN: 1743-0003
DOI
https://doi.org/10.1186/s12984-019-0574-0

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