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Published in: Journal of NeuroEngineering and Rehabilitation 1/2019

Open Access 01-12-2019 | Dystonia | Research

EMG-based vibro-tactile biofeedback training: effective learning accelerator for children and adolescents with dystonia? A pilot crossover trial

Authors: Claudia Casellato, Emilia Ambrosini, Andrea Galbiati, Emilia Biffi, Ambra Cesareo, Elena Beretta, Francesca Lunardini, Giovanna Zorzi, Terence D. Sanger, Alessandra Pedrocchi

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

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Abstract

Background

This study is aimed at better understanding the role of a wearable and silent ElectroMyoGraphy-based biofeedback on motor learning in children and adolescents with primary and secondary dystonia.

Methods

A crossover study with a wash-out period of at least 1 week was designed; the device provides the patient with a vibration proportional to the activation of an impaired target muscle. The protocol consisted of two 5-day blocks during which subjects were trained and tested on a figure-8 writing task: their performances (at different levels of difficulty) were evaluated in terms of both kinematics and muscular activations on day 1 and day 5, while the other 3 days were purely used as training sessions. The training was performed with and without using the biofeedback device: the week of use was randomized. Data were collected on 14 subjects with primary and secondary (acquired) dystonia (age: 6–19 years).

Results

Results comparing kinematic-based and EMG-based outcome measures pre- and post-training showed learning due to practice for both subjects with primary and secondary dystonia. On top of said learning, an improvement in terms of inter-joint coordination and muscular pattern functionality was recorded only for secondary dystonia subjects, when trained with the aid of the EMG-based biofeedback device.

Conclusions

Our results support the hypothesis that children and adolescents with primary dystonia in which there is intact sensory processing do not benefit from feedback augmentation, whereas children with secondary dystonia, in which sensory deficits are often present, exhibit a higher learning capacity when augmented movement-related sensory information is provided. This study represents a fundamental investigation to address the scarcity of noninvasive therapeutic interventions for young subjects with dystonia.
Literature
1.
go back to reference Sanger TD, Chen D, Fehlings DL, Hallett M, Lang AE, Mink JW, et al. Definition and classification of hyperkinetic movements in childhood. Mov Disord. 2010 Aug 15;25(11):1538–49.PubMedPubMedCentralCrossRef Sanger TD, Chen D, Fehlings DL, Hallett M, Lang AE, Mink JW, et al. Definition and classification of hyperkinetic movements in childhood. Mov Disord. 2010 Aug 15;25(11):1538–49.PubMedPubMedCentralCrossRef
2.
go back to reference Albanese A, Bhatia K, Bressman SB, DeLong MR, Fahn S, Fung VSC, et al. Phenomenology and classification of dystonia: a consensus update. Mov Disord. 2013;28(7):863–73.PubMedPubMedCentralCrossRef Albanese A, Bhatia K, Bressman SB, DeLong MR, Fahn S, Fung VSC, et al. Phenomenology and classification of dystonia: a consensus update. Mov Disord. 2013;28(7):863–73.PubMedPubMedCentralCrossRef
3.
go back to reference Berardelli A, Rothwell JC, Hallett M, Thompson PD, Manfredi M, Marsden CD. The pathophysiology of primary dystonia. Brain. 1998:1195–212.PubMedCrossRef Berardelli A, Rothwell JC, Hallett M, Thompson PD, Manfredi M, Marsden CD. The pathophysiology of primary dystonia. Brain. 1998:1195–212.PubMedCrossRef
4.
go back to reference Roubertie A, Mariani LL, Fernandez-Alvarez E, Doummar D, Roze E. Treatment for dystonia in childhood. Eur J Neurol. 2012;19(10):1292–9.CrossRef Roubertie A, Mariani LL, Fernandez-Alvarez E, Doummar D, Roze E. Treatment for dystonia in childhood. Eur J Neurol. 2012;19(10):1292–9.CrossRef
5.
go back to reference Koy A, Hellmich M, Pauls KAM, Marks W, Lin J-P, Fricke O, et al. Effects of deep brain stimulation in dyskinetic cerebral palsy: a meta-analysis. Mov Disord. 2013;28(5):647–54.PubMedCrossRef Koy A, Hellmich M, Pauls KAM, Marks W, Lin J-P, Fricke O, et al. Effects of deep brain stimulation in dyskinetic cerebral palsy: a meta-analysis. Mov Disord. 2013;28(5):647–54.PubMedCrossRef
7.
go back to reference Bertucco M, Sanger TD. Current and emerging strategies for treatment of childhood dystonia. J Hand Ther. 2015;28(2):185–93 quiz 194.PubMedCrossRef Bertucco M, Sanger TD. Current and emerging strategies for treatment of childhood dystonia. J Hand Ther. 2015;28(2):185–93 quiz 194.PubMedCrossRef
8.
go back to reference Casellato C, Pedrocchi A, Zorzi G, Rizzi G, Ferrigno G, Nardocci N. Error-enhancing robot therapy to induce motor control improvement in childhood onset primary dystonia. J Neuroeng Rehabil. 2012;9(1):46.PubMedPubMedCentralCrossRef Casellato C, Pedrocchi A, Zorzi G, Rizzi G, Ferrigno G, Nardocci N. Error-enhancing robot therapy to induce motor control improvement in childhood onset primary dystonia. J Neuroeng Rehabil. 2012;9(1):46.PubMedPubMedCentralCrossRef
9.
go back to reference Ferrante S, Ambrosini E, Ravelli P, Guanziroli E, Molteni F, Ferrigno G, et al. A biofeedback cycling training to improve locomotion: a case series study based on gait pattern classification of 153 chronic stroke patients. J Neuroeng Rehabil. 2011;8:47.PubMedPubMedCentralCrossRef Ferrante S, Ambrosini E, Ravelli P, Guanziroli E, Molteni F, Ferrigno G, et al. A biofeedback cycling training to improve locomotion: a case series study based on gait pattern classification of 153 chronic stroke patients. J Neuroeng Rehabil. 2011;8:47.PubMedPubMedCentralCrossRef
10.
go back to reference Ambrosini E, Ferrante S, Schauer T, Ferrigno G, Molteni F, Pedrocchi A. Design of a symmetry controller for cycling induced by electrical stimulation: preliminary results on post-acute stroke patients. Artif Organs. 2010;34(8):663–7. Ambrosini E, Ferrante S, Schauer T, Ferrigno G, Molteni F, Pedrocchi A. Design of a symmetry controller for cycling induced by electrical stimulation: preliminary results on post-acute stroke patients. Artif Organs. 2010;34(8):663–7.
11.
go back to reference Sanger TD. Failure of motor learning for large initial errors. Neural Comput. 2004;16(9):1873–86.CrossRef Sanger TD. Failure of motor learning for large initial errors. Neural Comput. 2004;16(9):1873–86.CrossRef
12.
go back to reference Molloy FM, Carr TD, Zeuner KE, Dambrosia JM, Hallett M. Abnormalities of spatial discrimination in focal and generalized dystonia. Brain. 2003;126(10):2175–82.PubMedCrossRef Molloy FM, Carr TD, Zeuner KE, Dambrosia JM, Hallett M. Abnormalities of spatial discrimination in focal and generalized dystonia. Brain. 2003;126(10):2175–82.PubMedCrossRef
13.
go back to reference Sanger TD, Kukke SN. Abnormalities of tactile sensory function in children with dystonic and diplegic cerebral palsy. J Child Neurol. 2007;22(3):289–93.CrossRef Sanger TD, Kukke SN. Abnormalities of tactile sensory function in children with dystonic and diplegic cerebral palsy. J Child Neurol. 2007;22(3):289–93.CrossRef
14.
go back to reference Abbruzzese G, Berardelli A. Sensorimotor integration in movement disorders. Mov Disord. 2003;18(3):231–40.PubMedCrossRef Abbruzzese G, Berardelli A. Sensorimotor integration in movement disorders. Mov Disord. 2003;18(3):231–40.PubMedCrossRef
15.
go back to reference Auld ML, Boyd R, Moseley GL, Ware R, Johnston LM. Tactile function in children with unilateral cerebral palsy compared to typically developing children. Disabil Rehabil. 2012;34(17):1488–94.PubMedCrossRef Auld ML, Boyd R, Moseley GL, Ware R, Johnston LM. Tactile function in children with unilateral cerebral palsy compared to typically developing children. Disabil Rehabil. 2012;34(17):1488–94.PubMedCrossRef
16.
go back to reference Cuppone AV, Cappagli G, Gori M. Audio feedback associated with body movement enhances audio and somatosensory spatial representation. Front Integr Neurosci. 2018;12:37.PubMedCentralCrossRef Cuppone AV, Cappagli G, Gori M. Audio feedback associated with body movement enhances audio and somatosensory spatial representation. Front Integr Neurosci. 2018;12:37.PubMedCentralCrossRef
17.
go back to reference Cuppone AV, Squeri V, Semprini M, Masia L, Konczak J. Robot-Assisted Proprioceptive Training with Added Vibro-Tactile Feedback Enhances Somatosensory and Motor Performance. Bensmaia SJ, editor. PLoS One. 2016;11(10):e0164511. Cuppone AV, Squeri V, Semprini M, Masia L, Konczak J. Robot-Assisted Proprioceptive Training with Added Vibro-Tactile Feedback Enhances Somatosensory and Motor Performance. Bensmaia SJ, editor. PLoS One. 2016;11(10):e0164511.
18.
go back to reference Cappagli G, Finocchietti S, Cocchi E, Giammari G, Zumiani R, Cuppone AV, et al. Audio motor training improves mobility and spatial cognition in visually impaired children. Sci Rep. 2019;9(1):3303.PubMedPubMedCentralCrossRef Cappagli G, Finocchietti S, Cocchi E, Giammari G, Zumiani R, Cuppone AV, et al. Audio motor training improves mobility and spatial cognition in visually impaired children. Sci Rep. 2019;9(1):3303.PubMedPubMedCentralCrossRef
19.
go back to reference Yoo JW, Lee DR, Sim YJ, You JH, Kim CJ. Effects of innovative virtual reality game and EMG biofeedback on neuromotor control in cerebral palsy. Biomed Mater Eng. 2014;24(6):3613–8. Yoo JW, Lee DR, Sim YJ, You JH, Kim CJ. Effects of innovative virtual reality game and EMG biofeedback on neuromotor control in cerebral palsy. Biomed Mater Eng. 2014;24(6):3613–8.
20.
go back to reference Golomb MR, McDonald BC, Warden SJ, Yonkman J, Saykin AJ, Shirley B, et al. In-Home Virtual Reality Videogame Telerehabilitation in Adolescents With Hemiplegic Cerebral Palsy. Arch Phys Med Rehabil. 2010;91(1):1–8 e1.PubMedCrossRef Golomb MR, McDonald BC, Warden SJ, Yonkman J, Saykin AJ, Shirley B, et al. In-Home Virtual Reality Videogame Telerehabilitation in Adolescents With Hemiplegic Cerebral Palsy. Arch Phys Med Rehabil. 2010;91(1):1–8 e1.PubMedCrossRef
21.
go back to reference Young SJ, van Doornik J, Sanger TD. Visual feedback reduces co-contraction in children with dystonia. J Child Neurol. 2011 Jan 1;26(1):37–43.PubMedCrossRef Young SJ, van Doornik J, Sanger TD. Visual feedback reduces co-contraction in children with dystonia. J Child Neurol. 2011 Jan 1;26(1):37–43.PubMedCrossRef
22.
go back to reference Casellato C, Pedrocchi A, Zorzi G, Vernisse L, Ferrigno G, Nardocci N. EMG-based visual-haptic biofeedback: a tool to improve motor control in children with primary dystonia. IEEE Trans Neural Syst Rehabil Eng. 2013;21(3):474–80.PubMedCrossRef Casellato C, Pedrocchi A, Zorzi G, Vernisse L, Ferrigno G, Nardocci N. EMG-based visual-haptic biofeedback: a tool to improve motor control in children with primary dystonia. IEEE Trans Neural Syst Rehabil Eng. 2013;21(3):474–80.PubMedCrossRef
23.
go back to reference Bloom R, Przekop A, Sanger TD. Prolonged electromyogram biofeedback improves upper extremity function in children with cerebral palsy. J Child Neurol. 2010 Dec;25(12):1480–4.PubMedCrossRef Bloom R, Przekop A, Sanger TD. Prolonged electromyogram biofeedback improves upper extremity function in children with cerebral palsy. J Child Neurol. 2010 Dec;25(12):1480–4.PubMedCrossRef
24.
go back to reference Lunardini F, Cesareo A, Biffi E, Casellato C, Aless PR, et al. EMG-based vibro-tactile biofeedback improves motor control in children with secondary dystonia: two case reports. Neuropsychiatry (London). 2016;6(6). Lunardini F, Cesareo A, Biffi E, Casellato C, Aless PR, et al. EMG-based vibro-tactile biofeedback improves motor control in children with secondary dystonia: two case reports. Neuropsychiatry (London). 2016;6(6).
25.
go back to reference Lunardini F, Bertucco M, Casellato C, Bhanpuri N, Pedrocchi A, Sanger TD. Speed-accuracy trade-off in a trajectory-constrained self-feeding task: a quantitative index of unsuppressed motor noise in children with dystonia. J Child Neurol. 2015;30(12):1676–85.PubMedPubMedCentralCrossRef Lunardini F, Bertucco M, Casellato C, Bhanpuri N, Pedrocchi A, Sanger TD. Speed-accuracy trade-off in a trajectory-constrained self-feeding task: a quantitative index of unsuppressed motor noise in children with dystonia. J Child Neurol. 2015;30(12):1676–85.PubMedPubMedCentralCrossRef
26.
go back to reference Lunardini F, Maggioni S, Casellato C, Bertucco M, Pedrocchi ALG, Sanger TD. Increased task-uncorrelated muscle activity in childhood dystonia. J Neuroeng Rehabil. 2015;12(1):52.PubMedPubMedCentralCrossRef Lunardini F, Maggioni S, Casellato C, Bertucco M, Pedrocchi ALG, Sanger TD. Increased task-uncorrelated muscle activity in childhood dystonia. J Neuroeng Rehabil. 2015;12(1):52.PubMedPubMedCentralCrossRef
27.
28.
go back to reference Harris CM, Wolpert DM. Signal-dependent noise determines motor planning. Nature. 1998;394(6695):780–4.PubMedCrossRef Harris CM, Wolpert DM. Signal-dependent noise determines motor planning. Nature. 1998;394(6695):780–4.PubMedCrossRef
29.
30.
go back to reference Casellato C, Zorzi G, Pedrocchi A, Ferrigno G, Nardocci N. Reaching and writing movements: sensitive and reliable tools to measure genetic dystonia in children. J Child Neurol. 2011;26(7):822–9.PubMedCrossRef Casellato C, Zorzi G, Pedrocchi A, Ferrigno G, Nardocci N. Reaching and writing movements: sensitive and reliable tools to measure genetic dystonia in children. J Child Neurol. 2011;26(7):822–9.PubMedCrossRef
31.
go back to reference Liyanagamage SA, Bertucco M, Bhanpuri NH, Sanger TD. Scaled vibratory feedback can Bias muscle use in children with dystonia during a redundant, 1-dimensional Myocontrol task. J Child Neurol. 2017;32(2):161–9.PubMedCrossRef Liyanagamage SA, Bertucco M, Bhanpuri NH, Sanger TD. Scaled vibratory feedback can Bias muscle use in children with dystonia during a redundant, 1-dimensional Myocontrol task. J Child Neurol. 2017;32(2):161–9.PubMedCrossRef
32.
go back to reference Grand KF, Bruzi AT, Dyke FB, Godwin MM, Leiker AM, Thompson AG, et al. Why self-controlled feedback enhances motor learning: answers from electroencephalography and indices of motivation. Hum Mov Sci. 2015;43:23–32.PubMedCrossRef Grand KF, Bruzi AT, Dyke FB, Godwin MM, Leiker AM, Thompson AG, et al. Why self-controlled feedback enhances motor learning: answers from electroencephalography and indices of motivation. Hum Mov Sci. 2015;43:23–32.PubMedCrossRef
Metadata
Title
EMG-based vibro-tactile biofeedback training: effective learning accelerator for children and adolescents with dystonia? A pilot crossover trial
Authors
Claudia Casellato
Emilia Ambrosini
Andrea Galbiati
Emilia Biffi
Ambra Cesareo
Elena Beretta
Francesca Lunardini
Giovanna Zorzi
Terence D. Sanger
Alessandra Pedrocchi
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/s12984-019-0620-y

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