Electrophysiological correlates of action observation treatment in children with cerebral palsy: A pilot study.
EEG
action observation treatment
cerebral palsy
mirror neuron system
sensorimotor activation
Journal
Developmental neurobiology
ISSN: 1932-846X
Titre abrégé: Dev Neurobiol
Pays: United States
ID NLM: 101300215
Informations de publication
Date de publication:
11 2019
11 2019
Historique:
received:
31
07
2019
revised:
17
01
2020
accepted:
18
01
2020
pubmed:
26
1
2020
medline:
20
6
2020
entrez:
26
1
2020
Statut:
ppublish
Résumé
Action Observation Treatment (AOT) has been shown to be effective in the functional recovery of several clinical populations. However, little is known about the neural underpinnings of the clinical efficacy of AOT in children with Cerebral Palsy (CP). Using electroencephalography (EEG), we recorded µ rhythm desynchronization as an index of sensorimotor cortex modulation during a passive action observation task before and after AOT. The relationship between sensorimotor modulation and clinical outcomes was also assessed. Eight children with CP entered the present randomized controlled crossover pilot study in which the experimental AOT preceded or followed a control Videogame Observation Treatment (VOT). Results provide further evidence of the clinical efficacy of AOT for improving hand motor function in CP, as assessed with the Assisting Hand Assessment (AHA) and Melbourne Assessment of Unilateral Upper Limb Function Scale (MUUL). The novel finding is that AOT increases µ rhythm desynchronization at scalp locations corresponding to the hand representation areas. This effect is associated to functional improvement assessed with the MUUL. These preliminary findings, although referred to as a small sample, suggest that AOT may affect upper limb motor recovery in children with CP and modulate the activation of sensorimotor areas, offering a potential neurophysiological correlate to support the clinical utility of AOT.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
934-948Informations de copyright
© 2020 Wiley Periodicals, Inc.
Références
Arnstein, D., Cui, F., Keysers, C., Maurits, N. M., & Gazzola, V. (2011). μ-suppression during action observation and execution correlates with BOLD in dorsal premotor, inferior parietal, and SI cortices. Journal of Neuroscience, 31(40), 14243-14249. https://doi.org/10.1523/JNEUROSCI.0963-11.2011
Bellelli, G., Buccino, G., Bernardini, B., Padovani, A., & Trabucchi, M. (2010). Action observation treatment improves recovery of postsurgical orthopedic patients: Evidence for a top-down effect? Archives of Physical Medicine and Rehabilitation, 91(10), 1489-1494. https://doi.org/10.1016/j.apmr.2010.07.013
Bleyenheuft, Y., Arnould, C., Brandao, M. B., Bleyenheuft, C., & Gordon, A. M. (2015). Hand and arm bimanual intensive therapy including lower extremity (HABIT-ILE) in children with unilateral spastic cerebral palsy: A randomized trial. Neurorehabilitation and Neural Repair, 29(7), 645-657. https://doi.org/10.1177/1545968314562109
Bourke-Taylor, H. (2003). Melbourne assessment of unilateral upper limb function: Construct validity and correlation with the pediatric evaluation of disability inventory. Developmental Medicine and Child Neurology, 45(2), 92-96. https://doi.org/10.1111/j.1469-8749.2003.tb00911.x
Boxum, A. G., La Bastide-van Gemert, S., Dijkstra, L. J., Hamer, E. G., Hielkema, T., Reinders-Messelink, H. A., & Hadders-Algra, M. (2017). Development of the quality of reaching in infants with cerebral palsy: A kinematic study. Developmental Medicine & Child Neurology, 59(11), 1164-1173. https://doi.org/10.1111/dmcn.13538
Buccino, G. (2014). Action observation treatment: A novel tool in neurorehabilitation. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1644), 20130185.
Buccino, G., Arisi, D., Gough, P., Aprile, D., Ferri, C., Serotti, L., … Fazzi, E. (2012). Improving upper limb motor functions through action observation treatment: A pilot study in children with cerebral palsy. Developmental Medicine & Child Neurology, 54(9), 822-828. https://doi.org/10.1111/j.1469-8749.2012.04334.x
Buccino, G., Gatti, R., Giusti, M. C., Negrotti, A., Rossi, A., Calzetti, S., & Cappa, S. F. (2011). Action observation treatment improves autonomy in daily activities in Parkinson's disease patients: Results from a pilot study. Movement Disorders, 26(10), 1963-1964. https://doi.org/10.1002/mds.23745
Buccino, G., Molinaro, A., Ambrosi, C., Arisi, D., Mascaro, L., Pinardi, C., …Galli, J. (2018). Action observation treatment improves upper limb motor functions in children with cerebral palsy: A combined clinical and brain imaging study. Neural Plasticity, 2018, 1-11.
Buccino, G., Perelli, D., Cattaneo, L., Pavesi, G., Ioele, M., Michelotti, V., …Rizzolatti, G. (2002). Motor observation: A new perspective in neuro-rehabilitation. In Eleventh European Stroke Conference. Geneva, Switzerland.
Buccino, G., Solodkin, A., & Small, S. L. (2006). Functions of the mirror neuron system: Implications for neurorehabilitation. Cognitive and Behavioral Neurology, 19(1), 55-63. https://doi.org/10.1097/00146965-200603000-00007
Burzi, V., Tealdi, G., Boyd, R. N., & Guzzetta, A. (2016). Action observation in infancy: Implications for neuro-rehabilitation. Developmental Medicine & Child Neurology, 58, 74-77. https://doi.org/10.1111/dmcn.13048
Cans, C., De-la-Cruz, J., & Mermet, M. A. (2008). Epidemiology of cerebral palsy. Paediatrics and Child Health, 18(9), 393-398. https://doi.org/10.1016/j.paed.2008.05.015
Celnik, P., Webster, B., Glasser, D. M., & Cohen, L. G. (2008). Effects of action observation on physical training after stroke. Stroke, 39(6), 1814-1820. https://doi.org/10.1161/STROKEAHA.107.508184
Csibra, G., Davis, G., Spratling, M. W., & Johnson, M. H. (2000). Gamma oscillations and object processing in the infant brain. Science, 290(5496), 1582-1585. https://doi.org/10.1126/science.290.5496.1582
de Klerk, C. C., Johnson, M. H., & Southgate, V. (2015). An EEG study on the somatotopic organisation of sensorimotor cortex activation during action execution and observation in infancy. Developmental Cognitive Neuroscience, 15, 1-10. https://doi.org/10.1016/j.dcn.2015.08.004
Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134(1), 9-21. https://doi.org/10.1016/j.jneumeth.2003.10.009
Démas, J., Bourguignon, M., Périvier, M., De Tiège, X., Dinomais, M., & Van Bogaert, P. (2019). Mu rhythm: State of the art with special focus on cerebral palsy. Annals of Physical and Rehabilitation Medicine. https://doi.org/10.1016/j.rehab.2019.06.007
di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., & Rizzolatti, G. (1992). Understanding motor events: A neurophysiological study. Experimental Brain Research, 91(1), 176-180. https://doi.org/10.1007/BF00230027
Eliasson, A. C., Krumlinde-Sundholm, L., Rösblad, B., Beckung, E., Arner, M., Öhrvall, A. M., & Rosenbaum, P. (2006). The manual ability classification system (MACS) for children with cerebral palsy: Scale development and evidence of validity and reliability. Developmental Medicine and Child Neurology, 48(7), 549-554. https://doi.org/10.1017/S0012162206001162
Eliasson, A. C., Nordstrand, L., Ek, L., Lennartsson, F., Sjöstrand, L., Tedroff, K., & Krumlinde-Sundholm, L. (2018). The effectiveness of baby-CIMT in infants younger than 12 months with clinical signs of unilateral-cerebral palsy; an explorative study with randomized design. Research in Developmental Disabilities, 72, 191-201. https://doi.org/10.1016/j.ridd.2017.11.006
Elvrum, A. K. G., Zethraeus, B. M., Vik, T., & Krumlinde-Sundholm, L. (2018). Development and validation of the both hands assessment for children with bilateral cerebral palsy. Physical & Occupational Therapy in Pediatrics, 38(2), 113-126. https://doi.org/10.1080/01942638.2017.1318431
Ertelt, D., Small, S., Solodkin, A., Dettmers, C., McNamara, A., Binkofski, F., & Buccino, G. (2007). Action observation has a positive impact on rehabilitation of motor deficits after stroke. NeuroImage, 36, T164-T173. https://doi.org/10.1016/j.neuroimage.2007.03.043
Franceschini, M., Agosti, M., Cantagallo, A., Sale, P., Mancuso, M., & Buccino, G. (2010). Mirror neurons: Action observation treatment as a tool in stroke rehabilitation. European Journal of Physical and Rehabilitation Medicine, 46(4), 517-523.
Gerson, S. A., & Woodward, A. L. (2014). Learning from their own actions: The unique effect of producing actions on infants' action understanding. Child Development, 85(1), 264-277. https://doi.org/10.1111/cdev.12115
Gordon, A. M., Schneider, J. A., Chinnan, A., & Charles, J. R. (2007). Efficacy of a hand-arm bimanual intensive therapy (HABIT) in children with hemiplegic cerebral palsy: A randomized control trial. Developmental Medicine & Child Neurology, 49(11), 830-838. https://doi.org/10.1111/j.1469-8749.2007.00830.x
Hoare, B. J., Wasiak, J., Imms, C., & Carey, L. (2007). Constraint-induced movement therapy in the treatment of the upper limb in children with hemiplegic cerebral palsy. Cochrane Database of Systematic Reviews, 2, 1-25. https://doi.org/10.1002/14651858.CD004149.pub2
Hunnius, S., & Bekkering, H. (2014). What are you doing? How active and observational experience shape infants' action understanding. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1644), 20130490. https://doi.org/10.1098/rstb.2013.0490
Johnson, A. (2002). Prevalence and characteristics of children with cerebral palsy in Europe. Developmental Medicine and Child Neurology, 44(9), 633-640. https://doi.org/10.1017/S0012162201002675
Keysers, C., & Gazzola, V. (2010). Social neuroscience: Mirror neurons recorded in humans. Current Biology, 20(8), R353-R354. https://doi.org/10.1016/j.cub.2010.03.013
Kirkpatrick, E., Pearse, J., James, P., & Basu, A. (2016). Effect of parent-delivered action observation therapy on upper limb function in unilateral cerebral palsy: A randomized controlled trial. Developmental Medicine & Child Neurology, 58(10), 1049-1056. https://doi.org/10.1111/dmcn.13109
Klingels, K., De Cock, P., Desloovere, K., Huenaerts, C., Molenaers, G., Van Nuland, I., … Feys, H. (2008). Comparison of the Melbourne assessment of unilateral upper limb function and the quality of upper extremity skills test in hemiplegic CP. Developmental Medicine & Child Neurology, 50(12), 904-909. https://doi.org/10.1111/j.1469-8749.2008.03123.x
Krumlinde-Sundholm, L., Holmefur, M., Kottorp, A., & Eliasson, A. C. (2007). The Assisting Hand Assessment: Current evidence of validity, reliability, and responsiveness to change. Developmental Medicine & Child Neurology, 49(4), 259-264. https://doi.org/10.1111/j.1469-8749.2007.00259.x
Lee, N. G., Kang, S. K., Lee, D. R., Hwang, H. J., Jung, J. H., You, J. S. H., … Kim, K. S. (2012). Feasibility and test-retest reliability of an electroencephalography based brain mapping system in children with cerebral palsy: A preliminary investigation. Archives of Physical Medicine and Rehabilitation, 93(5), 882-888. https://doi.org/10.1016/j.apmr.2011.10.028
Lepage, J. F., & Théoret, H. (2006). EEG evidence for the presence of an action observation-execution matching system in children. European Journal of Neuroscience, 23(9), 2505-2510. https://doi.org/10.1111/j.1460-9568.2006.04769.x
Loo, S. K., Lenartowicz, A., & Makeig, S. (2016). Research review: Use of EEG biomarkers in child psychiatry research-current state and future directions. Journal of Child Psychology and Psychiatry, 57(1), 4-17.
Manzoor, N., Kashif, M., Haroon, B., Dastgir, A., & Iram, H. (2019). Parent’s perception of constraint induced movement therapy in cerebral palsy management in rehabilitation centers of Lahore. Innovation, 69(3).
Marshall, P. J., & Meltzoff, A. N. (2011). Neural mirroring systems: Exploring the EEG mu rhythm in human infancy. Developmental Cognitive Neuroscience, 1(2), 110-123. https://doi.org/10.1016/j.dcn.2010.09.001
Marshall, P. J., & Meltzoff, A. N. (2014). Neural mirroring mechanisms and imitation in human infants. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1644), 20130620. https://doi.org/10.1098/rstb.2013.0620
Mattar, A. A., & Gribble, P. L. (2005). Motor learning by observing. Neuron, 46(1), 153-160. https://doi.org/10.1016/j.neuron.2005.02.009
McLoughlin, G., Makeig, S., & Tsuang, M. T. (2014). In search of biomarkers in psychiatry: EEG-based measures of brain function. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 165(2), 111-121.
Molenberghs, P., Cunnington, R., & Mattingley, J. B. (2012). Brain regions with mirror properties: A meta-analysis of 125 human fMRI studies. Neuroscience & Biobehavioral Reviews, 36(1), 341-349. https://doi.org/10.1016/j.neubiorev.2011.07.004
Muthukumaraswamy, S. D., Johnson, B. W., & McNair, N. A. (2004). Mu rhythm modulation during observation of an object-directed grasp. Cognitive Brain Research, 19(2), 195-201. https://doi.org/10.1016/j.cogbrainres.2003.12.001
Natale, E., Senna, I., Bolognini, N., Quadrelli, E., Addabbo, M., Cassia, V. M., & Turati, C. (2014). Predicting others’ intention involves motor resonance: EMG evidence from 6-and 9-month-old infants. Developmental Cognitive Neuroscience, 7, 23-29. https://doi.org/10.1016/j.dcn.2013.10.004
Oberman, L. M., Hubbard, E. M., McCleery, J. P., Altschuler, E. L., Ramachandran, V. S., & Pineda, J. A. (2005). EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Cognitive Brain Research, 24(2), 190-198. https://doi.org/10.1016/j.cogbrainres.2005.01.014
Parise, E., & Csibra, G. (2013). Neural responses to multimodal ostensive signals in 5-month-old infants. PLoS One, 8(8), e72360. https://doi.org/10.1371/journal.pone.0072360
Pelosin, E., Avanzino, L., Bove, M., Stramesi, P., Nieuwboer, A., & Abbruzzese, G. (2010). Action observation improves freezing of gait in patients with Parkinson's disease. Neurorehabilitation and Neural Repair, 24(8), 746-752. https://doi.org/10.1177/1545968310368685
Pfurtscheller, G., Brunner, C., Schlögl, A., & Da Silva, F. L. (2006). Mu rhythm (de) synchronization and EEG single-trial classification of different motor imagery tasks. NeuroImage, 31(1), 153-159. https://doi.org/10.1016/j.neuroimage.2005.12.003
Pineda, J. A., Grichanik, M., Williams, V., Trieu, M., Chang, H., & Keysers, C. (2013). EEG sensorimotor correlates of translating sounds into actions. Frontiers in Neuroscience, 7, 203. https://doi.org/10.3389/fnins.2013.00203
Pomiechowska, B., & Csibra, G. (2017). Motor activation during action perception depends on action interpretation. Neuropsychologia, 105, 84-91. https://doi.org/10.1016/j.neuropsychologia.2017.01.032
Quadrelli, E., Geangu, E., & Turati, C. (2019). Human action sounds elicit sensorimotor activation early in life. Cortex, 117, 323-335. https://doi.org/10.1016/j.cortex.2019.05.009
Quadrelli, E., Roberti, E., Turati, C., & Craighero, L. (2019). Observation of the Point-Light animation of a grasping hand activates sensorimotor cortex in nine-month-old infants. Cortex, 119, 373-385. https://doi.org/10.1016/j.cortex.2019.07.006
Quadrelli, E., & Turati, C. (2016). Origins and development of mirroring mechanisms: A neuroconstructivist framework. British Journal of Developmental Psychology, 34(1), 6-23.
Rabinoff, M., Kitchen, C. M. R., Cook, I. A., & Leuchter, A. F. (2011). Evaluation of quantitative EEG by classification and regression trees to characterize responders to antidepressant and placebo treatment. The Open Medical Informatics Journal, 5, 1.
Ramachandran, V. S., & Altschuler, E. L. (2009). The use of visual feedback, in particular mirror visual feedback, in restoring brain function. Brain, 132(7), 1693-1710. https://doi.org/10.1093/brain/awp135
Rosenbaum, P., Paneth, N., Leviton, A., Goldstein, M., Bax, M., Damiano, D., … Jacobsson, B. (2007). A report: The definition and classification of cerebral palsy April 2006. Developmental Medicine and Child Neurology Supplement, 109(suppl 109), 8-14.
Saby, J. N., Meltzoff, A. N., & Marshall, P. J. (2013). Infants' somatotopic neural responses to seeing human actions: I've got you under my skin. PLoS One, 8(10), e77905. https://doi.org/10.1371/journal.pone.0077905
Sakzewski, L., Ziviani, J., & Boyd, R. N. (2014). Efficacy of upper limb therapies for unilateral cerebral palsy: A meta-analysis. Pediatrics, 133(1), e175-e204.
Sgandurra, G., Ferrari, A., Cossu, G., Guzzetta, A., Fogassi, L., & Cioni, G. (2013). Randomized trial of observation and execution of upper extremity actions versus action alone in children with unilateral cerebral palsy. Neurorehabilitation and Neural Repair, 27(9), 808-815. https://doi.org/10.1177/1545968313497101
Small, S. L., Buccino, G., & Solodkin, A. (2012). The mirror neuron system and treatment of stroke. Developmental Psychobiology, 54(3), 293-310.
Thorpe, S. G., Cannon, E. N., & Fox, N. A. (2016). Spectral and source structural development of mu and alpha rhythms from infancy through adulthood. Clinical Neurophysiology, 127(1), 254-269. https://doi.org/10.1016/j.clinph.2015.03.004
Wechsler, D. (2003). Wechsler intelligence scale for children-WISC-IV. San Antonio, TX: Psychological Corporation.