Experimental Brain Research

, Volume 236, Issue 2, pp 517–527 | Cite as

Ipsilesional functional recruitment within lower mu band in children with unilateral cerebral palsy, an event-related desynchronization study

  • Alberto Inuggi
  • Michela Bassolino
  • Chiara Tacchino
  • Valentina Pippo
  • Valeria Bergamaschi
  • Claudio Campus
  • Valentina De Franchis
  • Thierry Pozzo
  • Paolo Moretti
Research Article

Abstract

Cerebral palsy (CP) is a group of non-progressive developmental movement disorders inducing a strong brain reorganization in primary and secondary motor areas. Nevertheless, few studies have been dedicated to quantify brain pattern changes and correlate them with motor characteristics in CP children. In this context, it is very important to identify feasible and complementary tools able to enrich the description of motor impairments by considering their neural correlates. To this aim, we recorded the electroencephalographic activity and the corresponding event-related desynchronization (ERD) of a group of mild-to-moderate affected unilateral CP children while performing unilateral reach-to-grasp movements with both their paretic and non-paretic arms. During paretic arm movement execution, we found a reduced ERD in the upper µ band (10–12.5 Hz) over central electrodes, preceded by an increased fronto-central ERD in the lower µ band (7.5–10 Hz) during movement preparation. These changes positively correlated, respectively, with the Modified House Classification scale and the Manual Ability Classification System. The fronto-central activation likely represents an ipsilesional plastic compensatory reorganization, confirming that in not-severely affected CP, the lesioned hemisphere is able to compensate part of the damage effects. These results highlight the importance of analyzing different sub-bands within the classical mu band and suggest that in similar CP population, the lesioned hemisphere should be the target of specific intensive rehabilitation programs.

Keywords

Cerebral palsy Event-related desynchronization Reach-to-grasp movement Electroencephalography Brain plasticity 

Notes

Acknowledgements

This work was supported by Fondation Motrice (http://www.lafondationmotrice.org) within the PACE for CP program.

Compliance with ethical standards

Conflict of interest

The authors have stated that they had no interests that might be perceived as posing a conflict or bias.

Supplementary material

221_2017_5149_MOESM1_ESM.pdf (141 kb)
Supplementary material 1 (PDF 140 KB)

References

  1. Accardo J, Kammann H, Hoon AH et al (2012) NIH public access. Neuroimage 6:290–301.  https://doi.org/10.1016/j.bbr.2012.08.038 Google Scholar
  2. Arnfield E, Guzzetta A, Boyd R (2013) Relationship between brain structure on magnetic resonance imaging and motor outcomes in children with cerebral palsy: a systematic review. Res Dev Disabil 34:2234–2250.  https://doi.org/10.1016/j.ridd.2013.03.031 CrossRefPubMedGoogle Scholar
  3. Bax M, Goldstein M, Rosenbaum P et al (2005) Proposed definition and classification of cerebral palsy. Dev Med Child Neurol 47:571–576.  https://doi.org/10.1017/S001216220500112X CrossRefPubMedGoogle Scholar
  4. Canivez GL, Watkins MW (1998) Long-term stability of the Wechsler Intelligence Scale for Children—Third Edition. Psychol Assess 10:285–291.  https://doi.org/10.1037/1040-3590.10.3.285 CrossRefGoogle Scholar
  5. Cans C (2000) Surveillance of cerebral palsy in Europe: a collaboration of cerebral palsy surveys and registers. Surveillance of Cerebral Palsy in Europe (SCPE). Dev Med Child Neurol 42:816–824.  https://doi.org/10.1111/j.1469-8749.2000.tb00695.x CrossRefGoogle Scholar
  6. Carr LJ, Harrison LM, Evans AL, Stephens JA (1993) Patterns of central motor reorganization in hemiplegic cerebral palsy. Brain 116 (Pt 5):1223–1247.  https://doi.org/10.1093/brain/116.5.1223 CrossRefPubMedGoogle Scholar
  7. Cebolla AM, Palmero-Soler E, Dan B, Cheron G (2014) Modulation of the N30 generators of the somatosensory evoked potentials by the mirror neuron system. Neuroimage 95:48–60.  https://doi.org/10.1016/j.neuroimage.2014.03.039 CrossRefPubMedGoogle Scholar
  8. Chouinard PA , Paus T (2006) The primary motor and premotor areas of the human cerebral cortex. Neuroscientist 12:143–152.  https://doi.org/10.1177/1073858405284255 CrossRefPubMedGoogle Scholar
  9. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21.  https://doi.org/10.1016/j.jneumeth.2003.10.009 CrossRefPubMedGoogle Scholar
  10. Duff SV, Gordon AM (2003) Learning of grasp control in children with hemiplegic cerebral palsy. Dev Med Child Neurol 45:746–757.  https://doi.org/10.1017/S0012162203001397 CrossRefPubMedGoogle Scholar
  11. Eliasson A-C, Krumlinde-Sundholm L, Rösblad B et al (2006) The Manual Ability Classification System (MACS) for children with cerebral palsy: scale development and evidence of validity and reliability. Dev Med Child Neurol 48:549–554.  https://doi.org/10.1017/S0012162206001162 CrossRefPubMedGoogle Scholar
  12. Eliasson AC, Krumlinde-Sundholm L, Gordon AM et al (2014) Guidelines for future research in constraint-induced movement therapy for children with unilateral cerebral palsy: an expert consensus. Dev Med Child Neurol 56:125–137CrossRefPubMedGoogle Scholar
  13. Eyre J (2007) Corticospinal tract development and its plasticity after perinatal injury. Neurosci Biobehav Rev 31:1136–1149.  https://doi.org/10.1016/j.neubiorev.2007.05.011 CrossRefPubMedGoogle Scholar
  14. Fennell EB, Dikel TN (2001) Cognitive and neuropsychological functioning in children with cerebral palsy. J Child Neurol 16:58–63.  https://doi.org/10.1177/088307380101600110 CrossRefPubMedGoogle Scholar
  15. Fiori S, Cioni G, Klingels K et al (2014) Reliability of a novel, semi-quantitative scale for classification of structural brain magnetic resonance imaging in children with cerebral palsy. Dev Med Child Neurol 56:839–845.  https://doi.org/10.1111/dmcn.12457 CrossRefPubMedGoogle Scholar
  16. Gainsborough M, Surman G, Maestri G et al (2008) Validity and reliability of the guidelines of the surveillance of cerebral palsy in Europe for the classification of cerebral palsy. Dev Med Child Neurol 50:828–831CrossRefPubMedGoogle Scholar
  17. Grandchamp R, Delorme A (2011) Single-trial normalization for event-related spectral decomposition reduces sensitivity to noisy trials. Front Psychol 2:236.  https://doi.org/10.3389/fpsyg.2011.00236 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Holmefur M, Krumlinde-Sundholm L, Eliasson A-C (2007) Interrater and intrarater reliability of the assisting hand assessment. Am J Occup Ther 61:79–84CrossRefPubMedGoogle Scholar
  19. Hoon AH, Vasconcellos Faria A, Faria AV (2010) Pathogenesis, neuroimaging and management in children with cerebral palsy born preterm. Dev Disabil Res Rev 16:302–312.  https://doi.org/10.1002/ddrr.127 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Inuggi A, Amato N, Magnani G et al (2011a) Cortical control of unilateral simple movement in healthy aging. Neurobiol Aging 32:524–538.  https://doi.org/10.1016/j.neurobiolaging.2009.02.020 CrossRefPubMedGoogle Scholar
  21. Inuggi A, Riva N, González-Rosa JJ et al (2011b) Compensatory movement-related recruitment in amyotrophic lateral sclerosis patients with dominant upper motor neuron signs: an EEG source analysis study. Brain Res 1425:37–46.  https://doi.org/10.1016/j.brainres.2011.09.007 CrossRefPubMedGoogle Scholar
  22. Johansen-Berg H, Rushworth MFS, Bogdanovic MD et al (2002) The role of ipsilateral premotor cortex in hand movement after stroke. Proc Natl Acad Sci USA 99:14518–14523.  https://doi.org/10.1073/pnas.222536799 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Krumlinde-Sundholm L, Holmefur M, Kottorp A, Eliasson AC (2007) The assisting hand assessment: current evidence of validity, reliability, and responsiveness to change. Dev Med Child Neurol 49:259–264.  https://doi.org/10.1111/j.1469-8749.2007.00259.x CrossRefPubMedGoogle Scholar
  24. Kurz MJ, Becker KM, Heinrichs-Graham E, Wilson TW (2014) Neurophysiological abnormalities in the sensorimotor cortices during the motor planning and movement execution stages of children with cerebral palsy. Dev Med Child Neurol 56:1072–1077.  https://doi.org/10.1111/dmcn.12513 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Law MC, Darrah J, Pollock N et al (2011) Focus on function: a cluster, randomized controlled trial comparing child-versus context-focused intervention for young children with cerebral palsy. Dev Med Child Neurol 53:621–629.  https://doi.org/10.1111/j.1469-8749.2011.03962.x CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lu MK, Arai N, Tsai CH, Ziemann U (2012) Movement related cortical potentials of cued versus self-initiated movements: Double dissociated modulation by dorsal premotor cortex versus supplementary motor area rTMS. Hum Brain Mapp 33:824–839.  https://doi.org/10.1002/hbm.21248 CrossRefPubMedGoogle Scholar
  27. Makeig S (1993) Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. Electroencephalogr Clin Neurophysiol 86:283–293CrossRefPubMedGoogle Scholar
  28. McConnell K, Johnston L, Kerr C (2011) Upper limb function and deformity in cerebral palsy: a review of classification systems. Dev Med Child Neurol 53:799–805.  https://doi.org/10.1111/j.1469-8749.2011.03953.x CrossRefPubMedGoogle Scholar
  29. Morris C (2007) Definition and classification of cerebral palsy: a historic perspective. Dev Med Child Neurol 49:1–44.  https://doi.org/10.1111/j.1469-8749.2007.00201.x Google Scholar
  30. Muthukumaraswamy SD, Johnson BW (2004) Changes in rolandic mu rhythm during observation of a precision grip. Psychophysiology 41:152–156.  https://doi.org/10.1046/j.1469-8986.2003.00129.x CrossRefPubMedGoogle Scholar
  31. Mutsaarts M, Steenbergen B, Bekkering H (2006) Anticipatory planning deficits and task context effects in hemiparetic cerebral palsy. Exp Brain Res 172:151–162.  https://doi.org/10.1007/s00221-005-0327-0 CrossRefPubMedGoogle Scholar
  32. Neuper C, Pfurtscheller G (2001) Event-related dynamics of cortical rhythms: frequency-specific features and functional correlates. Int J Psychophysiol 43:41–58.  https://doi.org/10.1016/S0167-8760(01)00178-7 CrossRefPubMedGoogle Scholar
  33. Novak I, McIntyre S, Morgan C et al (2013) A systematic review of interventions for children with cerebral palsy: state of the evidence. Dev Med Child Neurol 55:885–910.  https://doi.org/10.1111/dmcn.12246 CrossRefPubMedGoogle Scholar
  34. Nunez PL, Srinivasan R, Westdorp AF et al (1997) EEG coherency. Electroencephalogr Clin Neurophysiol 103:499–515.  https://doi.org/10.1016/S0013-4694(97)00066-7 CrossRefPubMedGoogle Scholar
  35. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113.  https://doi.org/10.1016/0028-3932(71)90067-4 CrossRefPubMedGoogle Scholar
  36. Pfurtscheller G, Lopes da Silva FHH (1999) Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110:1842–1857.  https://doi.org/10.1016/S1388-2457(99)00141-8 CrossRefPubMedGoogle Scholar
  37. Puzzo I, Cooper NR, Vetter P, Russo R (2010) EEG activation differences in the pre-motor cortex and supplementary motor area between normal individuals with high and low traits of autism. Brain Res 1342:104–110.  https://doi.org/10.1016/j.brainres.2010.04.060 CrossRefPubMedGoogle Scholar
  38. Raimondo F, Kamienkowski JE, Sigman M, Fernandez Slezak D (2012) CUDAICA: GPU optimization of Infomax-ICA EEG analysis. Comput Intell Neurosci 2012:206972.  https://doi.org/10.1155/2012/206972 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Randall M, Carlin JB, Chondros P, Reddihough D (2001) Reliability of the Melbourne assessment of unilateral upper limb function. Dev Med Child Neurol 43:761–767CrossRefPubMedGoogle Scholar
  40. Reid LB, Rose SE, Boyd RN (2015) Rehabilitation and neuroplasticity in children with unilateral cerebral palsy. Nat Rev Neurol 11:390–400.  https://doi.org/10.1038/nrneurol.2015.97 CrossRefPubMedGoogle Scholar
  41. Rigoldi C, Molteni E, Rozbaczylo C et al (2012) Movement analysis and EEG recordings in children with hemiplegic cerebral palsy. Exp Brain Res 223:517–524.  https://doi.org/10.1007/s00221-012-3278-2 CrossRefPubMedGoogle Scholar
  42. Rönnqvist L, Rösblad B (2007) Kinematic analysis of unimanual reaching and grasping movements in children with hemiplegic cerebral palsy. Clin Biomech 22:165–175.  https://doi.org/10.1016/j.clinbiomech.2006.09.004 CrossRefGoogle Scholar
  43. Rosenbaum P, Paneth N, Leviton A et al (2007) The definition and classification of cerebral palsy. Dev Med Child Neurol 49:1–44.  https://doi.org/10.1111/j.1469-8749.2007.00001.x Google Scholar
  44. Sakzewski L, Ziviani J, Boyd R (2010) The relationship between unimanual capacity and bimanual performance in children with congenital hemiplegia. Dev Med Child Neurol 52:811–816.  https://doi.org/10.1111/j.1469-8749.2009.03588.x CrossRefPubMedGoogle Scholar
  45. Sakzewski L, Carlon S, Shields N et al (2012) Impact of intensive upper limb rehabilitation on quality of life: a randomized trial in children with unilateral cerebral palsy. Dev Med Child Neurol 54:415–423.  https://doi.org/10.1111/j.1469-8749.2012.04272.x CrossRefPubMedGoogle Scholar
  46. Sanger TD (2003) Pediatric movement disorders. Curr Opin Neurol 16:529–535.  https://doi.org/10.1097/01.wco.0000084233.82329.0e PubMedGoogle Scholar
  47. Sgandurra G, Ferrari A, Cossu G et al (2013) Randomized trial of observation and execution of upper extremity actions versus action alone in children with unilateral cerebral palsy. Neurorehabilit Neural Repair 27:808–815.  https://doi.org/10.1177/1545968313497101 CrossRefGoogle Scholar
  48. Staudt M (2010) Reorganization after pre- and perinatal brain lesions. J Anat 217:469–474.  https://doi.org/10.1111/j.1469-7580.2010.01262.x CrossRefPubMedPubMedCentralGoogle Scholar
  49. Staudt M, Grodd W, Gerloff C et al (2002) Two types of ipsilateral reorganization in congenital hemiparesis: a TMS and fMRI study. Brain 125:2222–2237.  https://doi.org/10.1093/brain/awf227 CrossRefPubMedGoogle Scholar
  50. Van Der Heide JC, Fock JM, Otten B et al (2005) Kinematic characteristics of reaching movements in preterm children with cerebral palsy. Pediatr Res 57:883–889.  https://doi.org/10.1203/01.PDR.0000157771.20683.14 CrossRefPubMedGoogle Scholar
  51. Wagner LV, Davids JR (2012) Assessment tools and classification systems used for the upper extremity in children with cerebral palsy. Clin Orthop Relat Res 470:1257–1271.  https://doi.org/10.1007/s11999-011-2065-x CrossRefPubMedGoogle Scholar
  52. Ward NS (2006) Compensatory mechanisms in the aging motor system. Ageing Res Rev 5:239–254.  https://doi.org/10.1016/j.arr.2006.04.003 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Alberto Inuggi
    • 1
  • Michela Bassolino
    • 2
    • 3
  • Chiara Tacchino
    • 4
  • Valentina Pippo
    • 1
  • Valeria Bergamaschi
    • 4
  • Claudio Campus
    • 1
  • Valentina De Franchis
    • 2
  • Thierry Pozzo
    • 1
    • 5
    • 6
  • Paolo Moretti
    • 4
  1. 1.Robotics, Brain and Cognitive Sciences UnitIstituto Italiano di Tecnologia, Center for Human TechnologiesGenoaItaly
  2. 2.Laboratory of Cognitive Neuroscience, Brain Mind InstituteEcole Polytechnique Fédérale de LausanneGenevaSwitzerland
  3. 3.Center for NeuroprostheticsÉcole Polytechnique Fédérale de LausanneGeneveSwitzerland
  4. 4.Physical Medicine and RehabilitationInstitute G. GasliniGenoaItaly
  5. 5.Centro di Neurofisiologia traslazionaleIstituto Italiano di TecnologiaFerraraItaly
  6. 6.INSERM-U1093, Cognition-Action-Plasticité sensorimotriceDijonFrance

Personalised recommendations