Original article
Vol. 147 No. 0708 (2017)
The neuronal correlates of mirror illusion in children with spastic hemiparesis: a study with functional magnetic resonance imaging
Summary
AIM
To investigate the neuronal activation pattern underlying the effects of mirror illusion in children/adolescents with normal motor development and in children/adolescents with hemiparesis and preserved contralateral corticospinal organisation.
METHOD
The type of cortical reorganisation was classified according to results of transcranial magnetic stimulation. Only subjects with congenital lesions and physiological contralateral cortical reorganisation were included. Functional magnetic resonance imaging was performed to investigate neuronal activation patterns with and without a mirror box. Each test consisted of a unimanual and a bimanual motor task.
RESULTS
Seven children/adolescents with congenital hemiparesis (10–20 years old, three boys and four girls) and seven healthy subjects (8–17 years old, four boys and three girls) participated in this study. In the bimanual experiment, children with hemiparesis showed a significant effect of the mirror illusion (p<0.001 at voxel level, family-wise error corrected at cluster level) in the dorsolateral prefrontal cortex and anterior cingulate cortex of the affected and unaffected hemispheres, respectively. No significant effects of the mirror illusion were observed in unimanual experiments and in healthy participants.
INTERPRETATION
Mirror illusion in children/adolescents with hemiparesis leads to activation of brain areas involved in visual conflict detection and cognitive control to resolve this conflict. This effect is observed only in bimanual training. We consider that for mirror therapy in children and adolescents with hemiparesis a bimanual approach is more suitable than a unimanual approach.
References
- Carr LJ, Harrison LM, Evans AL, Stephens JA. Patterns of central motor reorganization in hemiplegic cerebral palsy. Brain. 1993;116(5):1223–47. Published online October 01, 1993. doi:.https://doi.org/10.1093/brain/116.5.1223
- Guzzetta A, Bonanni P, Biagi L, Tosetti M, Montanaro D, Guerrini R, et al. Reorganisation of the somatosensory system after early brain damage. Clin Neurophysiol. 2007;118(5):1110–21. Published online March 27, 2007. doi:.https://doi.org/10.1016/j.clinph.2007.02.014
- Staudt M, Grodd W, Gerloff C, Erb M, Stitz J, Krägeloh-Mann I. Two types of ipsilateral reorganization in congenital hemiparesis: a TMS and fMRI study. Brain. 2002;125(10):2222–37. doi:.https://doi.org/10.1093/brain/awf227
- Ramachandran VS, Rogers-Ramachandran D, Cobb S. Touching the phantom limb. Nature. 1995;377(6549):489–90. Published online October 12, 1995. doi:.https://doi.org/10.1038/377489a0
- Altschuler EL, Wisdom SB, Stone L, Foster C, Galasko D, Llewellyn DM, et al. Rehabilitation of hemiparesis after stroke with a mirror. Lancet. 1999;353(9169):2035–6. Published online June 22, 1999. doi:.https://doi.org/10.1016/S0140-6736(99)00920-4
- Cacchio A, De Blasis E, De Blasis V, Santilli V, Spacca G. Mirror therapy in complex regional pain syndrome type 1 of the upper limb in stroke patients. Neurorehabil Neural Repair. 2009;23(8):792–9. Published online May 26, 2009. doi:.https://doi.org/10.1177/1545968309335977
- Dohle C, Püllen J, Nakaten A, Küst J, Rietz C, Karbe H. Mirror therapy promotes recovery from severe hemiparesis: a randomized controlled trial. Neurorehabil Neural Repair. 2009;23(3):209–17. Published online December 17, 2008. doi:.https://doi.org/10.1177/1545968308324786
- Michielsen ME, Selles RW, van der Geest JN, Eckhardt M, Yavuzer G, Stam HJ, et al. Motor recovery and cortical reorganization after mirror therapy in chronic stroke patients: a phase II randomized controlled trial. Neurorehabil Neural Repair. 2011;25(3):223–33. Published online November 06, 2010. doi:.https://doi.org/10.1177/1545968310385127
- Yavuzer G, Selles R, Sezer N, Sütbeyaz S, Bussmann JB, Köseoğlu F, et al. Mirror therapy improves hand function in subacute stroke: a randomized controlled trial. Arch Phys Med Rehabil. 2008;89(3):393–8. Published online February 26, 2008. doi:.https://doi.org/10.1016/j.apmr.2007.08.162
- Hamzei F, Läppchen CH, Glauche V, Mader I, Rijntjes M, Weiller C. Functional plasticity induced by mirror training: the mirror as the element connecting both hands to one hemisphere. Neurorehabil Neural Repair. 2012;26(5):484–96. Published online January 17, 2012. doi:.https://doi.org/10.1177/1545968311427917
- Thieme H, Mehrholz J, Pohl M, Behrens J, Dohle C. Mirror therapy for improving motor function after stroke. Cochrane Database Syst Rev. 2012;3(3):CD008449. Published online March 16, 2012. doi:.https://doi.org/10.1002/14651858.CD008449.pub2
- Wang J, Fritzsch C, Bernarding J, Krause T, Mauritz KH, Brunetti M, et al. Cerebral activation evoked by the mirror illusion of the hand in stroke patients compared to normal subjects. NeuroRehabilitation. 2013;33(4):593–603. Published online September 11, 2013. doi:.https://doi.org/10.3233/NRE-130999
- Wang J, Fritzsch C, Bernarding J, Holtze S, Mauritz KH, Brunetti M, et al. A comparison of neural mechanisms in mirror therapy and movement observation therapy. J Rehabil Med. 2013;45(4):410–3. Published online March 12, 2013. doi:.https://doi.org/10.2340/16501977-1127
- Michielsen ME, Smits M, Ribbers GM, Stam HJ, van der Geest JN, Bussmann JB, et al. The neuronal correlates of mirror therapy: an fMRI study on mirror induced visual illusions in patients with stroke. J Neurol Neurosurg Psychiatry. 2011;82(4):393–8. Published online September 24, 2010. doi:.https://doi.org/10.1136/jnnp.2009.194134
- Fritzsch C, Wang J, Dos Santos LF, Mauritz KH, Brunetti M, Dohle C. Different effects of the mirror illusion on motor and somatosensory processing. Restor Neurol Neurosci. 2014;32(2):269–80. Published online November 19, 2013. doi:.https://doi.org/10.3233/RNN-130343
- Matthys K, Smits M, Van der Geest JN, Van der Lugt A, Seurinck R, Stam HJ, et al. Mirror-induced visual illusion of hand movements: a functional magnetic resonance imaging study. Arch Phys Med Rehabil. 2009;90(4):675–81. Published online April 07, 2009. doi:.https://doi.org/10.1016/j.apmr.2008.09.571
- Gygax MJ, Schneider P, Newman CJ. Mirror therapy in children with hemiplegia: a pilot study. Dev Med Child Neurol. 2011;53(5):473–6. Published online March 18, 2011. doi:.https://doi.org/10.1111/j.1469-8749.2011.03924.x
- Smorenburg AR, Ledebt A, Deconinck FJ, Savelsbergh GJ. Practicing a matching movement with a mirror in individuals with spastic hemiplegia. Res Dev Disabil. 2013;34(9):2507–13. doi:.https://doi.org/10.1016/j.ridd.2013.05.001
- Pasquet T, Gaillard F, Newman CJ, Jequier Gygax M, Le Cornec C, Bonan I, et al. Feasibility of a self-rehabilitation program by mirror therapy in children with hemiplegic cerebral palsy. Ann Phys Rehabil Med. 2016;59S:e9. doi:.https://doi.org/10.1016/j.rehab.2016.07.023
- Smorenburg AR, Ledebt A, Feltham MG, Deconinck FJ, Savelsbergh GJ. The positive effect of mirror visual feedback on arm control in children with spastic hemiparetic cerebral palsy is dependent on which arm is viewed. Exp Brain Res. 2011;213(4):393–402. doi:.https://doi.org/10.1007/s00221-011-2789-6
- Feltham MG, Ledebt A, Deconinck FJ, Savelsbergh GJ. Mirror visual feedback induces lower neuromuscular activity in children with spastic hemiparetic cerebral palsy. Res Dev Disabil. 2010;31(6):1525–35. doi:.https://doi.org/10.1016/j.ridd.2010.06.004
- Bruchez R, Jequier Gygax M, Roches S, Fluss J, Jacquier D, Ballabeni P, et al. Mirror therapy in children with hemiparesis: a randomized observer-blinded trial. Dev Med Child Neurol. 2016;58(9):970–8. doi:.https://doi.org/10.1111/dmcn.13117
- Grunt S, Newman CJ, Saxer S, Steinlin M, Weisstanner C, Kaelin-Lang A. The Mirror Illusion Increases Motor Cortex Excitability in Children With and Without Hemiparesis. Neurorehabil Neural Repair. 2016:1545968316680483. [e-pub ahead of print.] doi:.https://doi.org/10.1177/1545968316680483
- Eliasson AC, Krumlinde-Sundholm L, Rösblad B, Beckung E, Arner M, Ohrvall AM, et al. The Manual Ability Classification System (MACS) for children with cerebral palsy: scale development and evidence of validity and reliability. Dev Med Child Neurol. 2006;48(7):549–54. Published online June 20, 2006. doi:.https://doi.org/10.1017/S0012162206001162
- Z’Graggen WJ, Conforto AB, Wiest R, Remonda L, Hess CW, Kaelin-Lang A. Mapping of direction and muscle representation in the human primary motor cortex controlling thumb movements. J Physiol. 2009;587(9):1977–87. Published online March 18, 2009. doi:.https://doi.org/10.1113/jphysiol.2009.171066
- Kaelin-Lang A, Cohen LG. Enhancing the quality of studies using transcranial magnetic and electrical stimulation with a new computer-controlled system. J Neurosci Methods. 2000;102(1):81–9. Published online September 23, 2000. doi:.https://doi.org/10.1016/S0165-0270(00)00284-3
- Brasil-Neto JP, Cohen LG, Panizza M, Nilsson J, Roth BJ, Hallett M. Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse, and stimulus intensity. J Clin Neurophysiol. 1992;9(1):132–6. Published online January 01, 1992. doi:.https://doi.org/10.1097/00004691-199201000-00014
- Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol. 1994;91(2):79–92. Published online August 01, 1994. doi:.https://doi.org/10.1016/0013-4694(94)90029-9
- Dinomais M, Lignon G, Chinier E, Richard I, Ter Minassian A, Tich SN. Effect of observation of simple hand movement on brain activations in patients with unilateral cerebral palsy: an fMRI study. Res Dev Disabil. 2013;34(6):1928–37. doi:.https://doi.org/10.1016/j.ridd.2013.03.020
- Deconinck FJ, Smorenburg AR, Benham A, Ledebt A, Feltham MG, Savelsbergh GJ. Reflections on mirror therapy: a systematic review of the effect of mirror visual feedback on the brain. Neurorehabil Neural Repair. 2015;29(4):349–61. doi:.https://doi.org/10.1177/1545968314546134
- Shinoura N, Suzuki Y, Watanabe Y, Yamada R, Tabei Y, Saito K, et al. Mirror therapy activates outside of cerebellum and ipsilateral M1. NeuroRehabilitation. 2008;23(3):245–52. Published online June 19, 2008.
- Merians AS, Tunik E, Fluet GG, Qiu Q, Adamovich SV. Innovative approaches to the rehabilitation of upper extremity hemiparesis using virtual environments. Eur J Phys Rehabil Med. 2009;45(1):123–33.
- Wasaka T, Kakigi R. Conflict caused by visual feedback modulates activation in somatosensory areas during movement execution. Neuroimage. 2012;59(2):1501–7. doi:.https://doi.org/10.1016/j.neuroimage.2011.08.024
- Wasaka T, Kakigi R. The effect of unpredicted visual feedback on activation in the secondary somatosensory cortex during movement execution. BMC Neurosci. 2012;13(1):138. doi:.https://doi.org/10.1186/1471-2202-13-138
- Dohle C, Stephan KM, Valvoda JT, Hosseiny O, Tellmann L, Kuhlen T, et al. Representation of virtual arm movements in precuneus. Exp Brain Res. 2011;208(4):543–55. doi:.https://doi.org/10.1007/s00221-010-2503-0
- Fink GR, Marshall JC, Halligan PW, Frith CD, Driver J, Frackowiak RS, et al. The neural consequences of conflict between intention and the senses. Brain. 1999;122(3):497–512. doi:.https://doi.org/10.1093/brain/122.3.497
- Mehnert J, Brunetti M, Steinbrink J, Niedeggen M, Dohle C. Effect of a mirror-like illusion on activation in the precuneus assessed with functional near-infrared spectroscopy. J Biomed Opt. 2013;18(6):066001. doi:.https://doi.org/10.1117/1.JBO.18.6.066001
- Carson RG, Ruddy KL. Vision modulates corticospinal suppression in a functionally specific manner during movement of the opposite limb. J Neurosci. 2012;32(2):646–52. doi:.https://doi.org/10.1523/JNEUROSCI.4435-11.2012
- Garry MI, Loftus A, Summers JJ. Mirror, mirror on the wall: viewing a mirror reflection of unilateral hand movements facilitates ipsilateral M1 excitability. Exp Brain Res. 2005;163(1):118–22. doi:.https://doi.org/10.1007/s00221-005-2226-9
- Fukumura K, Sugawara K, Tanabe S, Ushiba J, Tomita Y. Influence of mirror therapy on human motor cortex. Int J Neurosci. 2007;117(7):1039–48. doi:.https://doi.org/10.1080/00207450600936841
- Dohle C, Kleiser R, Seitz RJ, Freund HJ. Body scheme gates visual processing. J Neurophysiol. 2004;91(5):2376–9. Published online December 19, 2003. doi:.https://doi.org/10.1152/jn.00929.2003
- Paus T. Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci. 2001;2(6):417–24. doi:.https://doi.org/10.1038/35077500
- Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 2001;24(1):167–202. Published online April 03, 2001. doi:.https://doi.org/10.1146/annurev.neuro.24.1.167
- Heekeren HR, Marrett S, Ungerleider LG. The neural systems that mediate human perceptual decision making. Nat Rev Neurosci. 2008;9(6):467–79. doi:.https://doi.org/10.1038/nrn2374
- Iacoboni M, Dapretto M. The mirror neuron system and the consequences of its dysfunction. Nat Rev Neurosci. 2006;7(12):942–51. Published online November 23, 2006. doi:.https://doi.org/10.1038/nrn2024
- Bertenthal BI, Longo MR. Is there evidence of a mirror system from birth? Dev Sci. 2007;10(5):526–9. doi:.https://doi.org/10.1111/j.1467-7687.2007.00633.x
- Simpson EA, Murray L, Paukner A, Ferrari PF. The mirror neuron system as revealed through neonatal imitation: presence from birth, predictive power and evidence of plasticity. Philos Trans R Soc Lond B Biol Sci. 2014;369(1644):20130289. doi:.https://doi.org/10.1098/rstb.2013.0289
- Van de Winckel A, Klingels K, Bruyninckx F, Wenderoth N, Peeters R, Sunaert S, et al. How does brain activation differ in children with unilateral cerebral palsy compared to typically developing children, during active and passive movements, and tactile stimulation? An fMRI study. Res Dev Disabil. 2013;34(1):183–97. doi:.https://doi.org/10.1016/j.ridd.2012.07.030