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Research Article

Mu Rhythm during Standing and Walking Is Altered in Children with Unilateral Cerebral Palsy Compared to Children with Typical Development

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 8-17 | Received 25 Oct 2019, Accepted 12 Apr 2020, Published online: 06 May 2020

References

  • Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, Damiano D, Dan B, Jacobsson B. A report: the definition and classification of cerebral palsy April 2006. Dev Med Child Neurol Suppl. 2007;109:8–14.
  • Arneson CL, Durkin MS, Benedict RE, Kirby RS, Yeargin-Allsopp M, Braun KV, Doernberg NS. Prevalence of cerebral palsy: autism and developmental disabilities monitoring network, three sites, United States, 2004. Disabil Health J. 2009;2(1):45–48. doi:10.1016/j.dhjo.2008.08.001.
  • Damiano DL, Alter KE, Chambers H. New clinical and research trends in lower extremity management for ambulatory children with cerebral palsy. Phys Med Rehabil Clin N Am. 2009;20(3):469–91. doi:10.1016/j.pmr.2009.04.005.
  • Corbetta D, Friedman DR, Bell MA. Brain reorganization as a function of walking experience in 12-month-old infants: implications for the development of manual laterality. Front Psychol. 2014;5:245. doi:10.3389/fpsyg.2014.00245.
  • Bell MA, Fox NA. Crawling experience is related to changes in cortical organization during infancy: evidence from EEG coherence. Dev Psychobiol. 1996;29(7):551–61. doi:10.1002/(SICI)1098-2302(199611)29:7<551::AID-DEV1>3.0.CO;2-T.
  • Cannon EN, Simpson EA, Fox NA, Vanderwert RE, Woodward AL, Ferrari PF. Relations between infants’ emerging reach-grasp competence and event-related desynchronization in EEG. Dev Sci. 2015;19(1):50–62. doi:10.1111/desc.12295.
  • Gonzalez SL, Reeb-Sutherland BC, Nelson EL. Quantifying motor experience in the infant brain: EEG power, coherence, and mu desynchronization. Front Psychol. 2016;7:216.
  • Pfurtscheller G. Lopes da Silva FH. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol. 1999;110:1842–57.
  • Pfurtscheller G, Aranibar A. Evaluation of event-related desynchronization (ERD) preceding and following voluntary self-paced movement. Electroencephalogr Clin Neurophysiol. 1979;46:138–46.
  • Berchicci M, Zhang T, Romero L, Peters A, Annett R, Teuscher U, Bertollo M, Okada Y, Stephen J, Comani S, et al. Development of mu rhythm in infants and preschool children. Dev Neurosci. 2011;33(2):130–43. doi:10.1159/000329095.
  • Hagne I. Development of the EEG in normal infants during the first year of life. A longitudinal study. Acta Paediatr Scand Suppl. 1972;232:1–53.
  • Marshall PJ, Bar-Haim Y, Fox NA. Development of the EEG from 5 months to 4 years of age. Clin Neurophysiol. 2002;113(8):1199–208. doi:10.1016/S1388-2457(02)00163-3.
  • Muthukumaraswamy SD, Johnson BW. Changes in rolandic mu rhythm during observation of a precision grip. Psychophysiology. 2004;41(1):152–56. doi:10.1046/j.1469-8986.2003.00129.x.
  • Warreyn P, Ruysschaert L, Wiersema JR, Handl A, Pattyn G, Roeyers H. Infants’ mu suppression during the observation of real and mimicked goal-directed actions. Dev Sci. 2013;16(2):173–85. doi:10.1111/desc.12014.
  • Thorpe SG, Cannon EN, Fox NA. Spectral and source structural development of mu and alpha rhythms from infancy through adulthood. Clin Neurophysiol. 2015;127(1):254–69. doi:10.1016/j.clinph.2015.03.004.
  • Xiao R, Qi X, Patino A, Fagg AH, Kolobe THA, Miller DP, Ding L. Characterization of infant mu rhythm immediately before crawling: A high-resolution EEG study. NeuroImage. 2017;146:47–57. doi:10.1016/j.neuroimage.2016.11.007.
  • Demas J, Bourguignon M, Perivier M, De Tiege X, Dinomais M, Van Bogaert P. Mu rhythm: state of the art with special focus on cerebral palsy. Ann Phys Rehabil Med. 2019. doi:10.1016/j.rehab.2019.06.007.
  • Bulea TC, Lerner ZF, Gravunder AJ, Damiano DL. Exergaming with a pediatric exoskeleton: facilitating rehabilitation and research in children with cerebral palsy. IEEE Int Conf Rehabil Robot. 2017;2017:1087–93. doi:10.1109/ICORR.2017.8009394.
  • Koeda T, Takeshita K. Electroencephalographic coherence abnormalities in preterm diplegia. Pediatr Neurol. 1998;18(1):51–56. doi:10.1016/S0887-8994(97)00155-0.
  • Rigoldi C, Molteni E, Rozbaczylo C, Morante M, Albertini G, Bianchi AM, Galli M. Movement analysis and EEG recordings in children with hemiplegic cerebral palsy. Exp Brain Res. 2012;223(4):517–24. doi:10.1007/s00221-012-3278-2.
  • Kukke SN, de Campos AC, Damiano D, Alter KE, Patronas N, Hallett M. Cortical activation and inter-hemispheric sensorimotor coherence in individuals with arm dystonia due to childhood stroke. Clin Neurophysiol. 2015;126(8):1589–98. doi:10.1016/j.clinph.2014.11.002.
  • Inuggi A, Bassolino M, Tacchino C, Pippo V, Bergamaschi V, Campus C, De Franchis V, Pozzo T, Moretti P. Ipsilesional functional recruitment within lower mu band in children with unilateral cerebral palsy, an event-related desynchronization study. Exp Brain Res. 2018;236(2):517–27. doi:10.1007/s00221-017-5149-3.
  • Weinstein M, Green D, Rudisch J, Zielinski IM, Benthem-Muñiz M, Jongsma MLA, McClelland V, Steenbergen B, Shiran S, Ben Bashat D, et al. Understanding the relationship between brain and upper limb function in children with unilateral motor impairments: A multimodal approach. Eur J Paediatr Neuro. 2018;22(1):143–54. doi:10.1016/j.ejpn.2017.09.012.
  • Simon-Martinez C, Jaspers E, Alaerts K, Ortibus E, Balsters J, Mailleux L, Blommaert J, Sleurs C, Klingels K, Amant F, et al. Influence of the corticospinal tract wiring pattern on sensorimotor functional connectivity and clinical correlates of upper limb function in unilateral cerebral palsy. Sci Rep. 2019;9(1):8230. doi:10.1038/s41598-019-44728-9.
  • de Campos AC, Sukal-Moulton T, Huppert T, Alter K, Damiano DL. Brain activation patterns underlying upper limb bilateral motor coordination in unilateral cerebral palsy: an fNIRS study. Dev Med Child Neurol. 2020. doi:10.1111/dmcn.14458.
  • Surkar SM, Hoffman RM, Harbourne R, Kurz MJ. Neural activation within the prefrontal cortices during the goal-directed motor actions of children with hemiplegic cerebral palsy. Neurophotonics. 2018;5:011021.
  • Kurz MJ, Wilson TW, Arpin DJ. An fNIRS exploratory investigation of the cortical activity during gait in children with spastic diplegic cerebral palsy. Brain Dev. 2014;36(10):870–77. doi:10.1016/j.braindev.2014.01.003.
  • Miyai I, Suzuki M, Hatakenaka M, Kubota K. Effect of body weight support on cortical activation during gait in patients with stroke. Exp Brain Res. 2006;169(1):85–91. doi:10.1007/s00221-005-0123-x.
  • Castermans T, Duvinage M, Cheron G, Dutoit T. About the cortical origin of the low-delta and high-gamma rhythms observed in EEG signals during treadmill walking. Neurosci Lett. 2014;561:166–70. doi:10.1016/j.neulet.2013.12.059.
  • Kline JE, Huang HJ, Snyder KL, Ferris DP. Isolating gait-related movement artifacts in electroencephalography during human walking. J Neural Eng. 2015;12(4):046022. doi:10.1088/1741-2560/12/4/046022.
  • Bulea TC, Kim J, Damiano DL, Stanley CJ, Park HS. Prefrontal, posterior parietal and sensorimotor network activity underlying speed control during walking. Front Hum Neurosci. 2015;9:247. doi:10.3389/fnhum.2015.00247.
  • Kilicarslan A, Grossman RG, Contreras-Vidal JL. A robust adaptive denoising framework for real-time artifact removal in scalp EEG measurements. J Neural Eng. 2016;13(2):026013. doi:10.1088/1741-2560/13/2/026013.
  • Blum S, Jacobsen NSJ, Bleichner MG, Debener S. A Riemannian modification of artifact subspace reconstruction for EEG artifact handling. Front Hum Neurosci. 2019;13:141. doi:10.3389/fnhum.2019.00141.
  • Wagner J, Solis-Escalante T, Grieshofer P, Neuper C, Muller-Putz G, Scherer R. Level of participation in robotic-assisted treadmill walking modulates midline sensorimotor EEG rhythms in able-bodied subjects. NeuroImage. 2012;63(3):1203–11. doi:10.1016/j.neuroimage.2012.08.019.
  • Gwin JT, Gramann K, Makeig S, Ferris DP. Electrocortical activity is coupled to gait cycle phase during treadmill walking. NeuroImage. 2011;54(2):1289–96. doi:10.1016/j.neuroimage.2010.08.066.
  • Seeber M, Scherer R, Wagner J, Solis-Escalante T, Muller-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.
  • Wagner J, Makeig S, Gola M, Neuper C, Muller-Putz G. Distinct beta band oscillatory networks subserving motor and cognitive control during gait adaptation. J Neurosci. 2016;36(7):2212–26. doi:10.1523/JNEUROSCI.3543-15.2016.
  • Mima T, Matsuoka T, Hallett M. Functional coupling of human right and left cortical motor areas demonstrated with partial coherence analysis. Neurosci Lett. 2000;287(2):93–96. doi:10.1016/S0304-3940(00)01165-4.
  • Andrew C, Pfurtscheller G. Event-related coherence as a tool for studying dynamic interaction of brain regions. Electroencephalogr Clin Neurophysiol. 1996;98(2):144–48. doi:10.1016/0013-4694(95)00228-6.
  • Lau TM, Gwin JT, Ferris DP. Walking reduces sensorimotor network connectivity compared to standing. J Neuroeng Rehabil. 2014;11:14. doi:10.1186/1743-0003-11-14.
  • Mullen TR, Kothe CA, Chi YM, Ojeda A, Kerth T, Makeig S, Jung T-P, Cauwenberghs G. Real-time neuroimaging and cognitive monitoring using wearable dry EEG. IEEE Trans Biomed Eng. 2015;62(11):2553–67. doi:10.1109/TBME.2015.2481482.
  • Nordin AD, Hairston WD, Ferris DP. Faster gait speeds reduce alpha and beta EEG spectral power from human sensorimotor cortex. IEEE Trans Biomed Eng. 2020;67(3):842–53. doi:10.1109/TBME.2019.2921766.
  • Cuevas K, Cannon EN, Yoo K, Fox NA. The infant EEG mu rhythm: methodological considerations and best practices. Dev Rev. 2014;34(1):26–43. doi:10.1016/j.dr.2013.12.001.
  • Bulea TC, Prasad S, Kilicarslan A, Contreras-Vidal JL. Sitting and standing intention can be decoded from scalp EEG recorded prior to movement execution. Front Neurosci-Switz. 2014;8:376.
  • Lee PJ, Kukke SN. Neurophysiological features of tactile versus visual guidance of ongoing movement. Exp Brain Res. 2017;235(9):2615–25. doi:10.1007/s00221-017-4999-z.
  • Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39(4):214–23. doi:10.1111/j.1469-8749.1997.tb07414.x.
  • Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113. doi:10.1016/0028-3932(71)90067-4.
  • Beckung E, Carlsson G, Carlsdotter S, Uvebrant P. The natural history of gross motor development in children with cerebral palsy aged 1 to 15 years. Dev Med Child Neurol. 2007;49(10):751–56. doi:10.1111/j.1469-8749.2007.00751.x.
  • Hanna SE, Rosenbaum PL, Bartlett DJ, Palisano RJ, Walter SD, Avery L, Russell DJ. Stability and decline in gross motor function among children and youth with cerebral palsy aged 2 to 21 years. Dev Med Child Neurol. 2009;51(4):295–302. doi:10.1111/j.1469-8749.2008.03196.x.
  • Weersink JB, Maurits NM, de Jong BM. EEG time-frequency analysis provides arguments for arm swing support in human gait control. Gait Posture. 2019;70:71–78. doi:10.1016/j.gaitpost.2019.02.017.
  • Enzinger C, Dawes H, Johansen-Berg H, Wade D, Bogdanovic M, Collett J, Guy C, Kischka U, Ropele S, Fazekas F, et al. Brain activity changes associated with treadmill training after stroke. Stroke. 2009;40(7):2460–67. doi:10.1161/STROKEAHA.109.550053.
  • Suzuki M, Miyai I, Ono T, Oda I, Konishi I, Kochiyama T, Kubota K. Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study. NeuroImage. 2004;23(3):1020–26. doi:10.1016/j.neuroimage.2004.07.002.
  • Koenraadt KL, Roelofsen EG, Duysens J, Keijsers NL. Cortical control of normal gait and precision stepping: an fNIRS study. NeuroImage. 2014;85(Pt 1):415–22. doi:10.1016/j.neuroimage.2013.04.070.
  • Kurz MJ, Wilson TW, Arpin DJ. Stride-time variability and sensorimotor cortical activation during walking. NeuroImage. 2012;59(2):1602–07. doi:10.1016/j.neuroimage.2011.08.084.
  • Pannek K, Boyd RN, Fiori S, Guzzetta A, Rose SE. Assessment of the structural brain network reveals altered connectivity in children with unilateral cerebral palsy due to periventricular white matter lesions. Neuroimage-Clin. 2014;5:84–92. doi:10.1016/j.nicl.2014.05.018.
  • Jain KK, Paliwal VK, Yadav A, Roy B, Goel P, Chaturvedi S, Chaurasia A, Garg R, Rathore R, Gupta R, et al. Cerebral Blood Flow and DTI metrics changes in children with cerebral palsy following therapy. J Pediatr Neuroradio. 2014;3(2):63–73. doi:10.3233/PNR-14088.
  • Mailleux L, Franki I, Emsell L, Peedima ML, Fehrenbach A, Feys H, Ortibus E. The relationship between neuroimaging and motor outcome in children with cerebral palsy: A systematic review-Part B diffusion imaging and tractography. Res Dev Disabil. 2020;97:103569. doi:10.1016/j.ridd.2019.103569.
  • Meyns P, Van Gestel L, Leunissen I, De Cock P, Sunaert S, Feys H, Duysens J, Desloovere K, Ortibus E. Macrostructural and microstructural brain lesions relate to gait pathology in children with cerebral palsy. Neurorehabil Neural Repair. 2016;30(9):817–33. doi:10.1177/1545968315624782.
  • Englander ZA, Sun J, Case L, Mikati MA, Kurtzberg J, Song AW. Brain structural connectivity increases concurrent with functional improvement: evidence from diffusion tensor MRI in children with cerebral palsy during therapy. Neuroimage-Clin. 2015;7:315–24. doi:10.1016/j.nicl.2015.01.002.
  • Lee JD, Park HJ, Park ES, Oh M-K, Park B, Rha D-W, Cho S-R, Kim EY, Park JY, Kim CH, et al. Motor pathway injury in patients with periventricular leucomalacia and spastic diplegia. Brain. 2011;134:1199–210. doi:10.1093/brain/awr021.
  • Trivedi R, Agarwal S, Shah V, Goyel P, Paliwal VK, Rathore RKS, Gupta RK. Correlation of quantitative sensorimotor tractography with clinical grade of cerebral palsy. Neuroradiology. 2010;52(8):759–65. doi:10.1007/s00234-010-0703-8.
  • Yoshida S, Hayakawa K, Yamamoto A, Okano S, Kanda T, Yamori Y, Yoshida N, Hirota H. Quantitative diffusion tensor tractography of the motor and sensory tract in children with cerebral palsy. Dev Med Child Neurol. 2010;52(10):935–40.
  • Woodward KE, Carlson HL, Kuczynski A, Saunders J, Hodge J, Kirton A. Sensory-motor network functional connectivity in children with unilateral cerebral palsy secondary to perinatal stroke. Neuroimage Clin. 2019;21:101670.
  • Aisen ML, Kerkovich D, Mast J, Mulroy S, Wren TA, Kay RM, Rethlefsen SA. Cerebral palsy: clinical care and neurological rehabilitation. Lancet Neurol. 2011;10(9):844–52.

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