Skip to main content
SpringerLink
Log in

Multimodal assessment of motor pathways and intracortical connections in functional hemispherectomy

  • Original Article
  • Published:
Child's Nervous System Aims and scope Submit manuscript

Abstract

Purpose

For selected children with medically intractable epilepsy, hemispherectomy can be an excellent treatment option and its efficacy in achieving seizure freedom or reduction in seizure frequency has been shown in several studies, but patients’ selection could not be straightforward and often it is taken on subjective basis. We described a multimodal approach to assess patient eligible for hemispherectomy and possibly predicting post-surgical outcomes.

Methods

We describe pre- and post-surgical clinical features along with neuroradiological results by magnetic resonance imaging (MRI), functional magnetic resonance imaging (fMRI), MR-tractography (MRT), and neurophysiological study by single and paired pulses transcranial magnetic stimulation (TMS) in a child with cerebral palsy with epileptic encephalopathy, eligible for epilepsy surgery.

Results

Presurgical TMS evaluation showed a lateralization of motor function on the left motor cortex for both arms, and results were confirmed by MRI studies. Interestingly, after surgery, both epilepsy and motor performances improved and TMS showed enhancement of intracortical inhibition and facilitation activity.

Conclusion

Functional hemispherectomy is an effective treatment for drug-resistant epilepsy, and multimodal presurgical assessment may be a useful approach to guide surgeons in selecting patients. Moreover, pre- and post-surgical evaluation of these patients may enhance our understanding of brain plasticity phenomena.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, Damiano D, Dan B, Jacobsson B (2007) A report: the definition and classification of cerebral palsy April 2006. Dev Med Child Neurol 49:8–14. https://doi.org/10.1111/j.1469-8749.2007.tb12610.x

    Article  Google Scholar 

  2. Blair E (2010) Epidemiology of the cerebral palsies. Orthop Clin North Am 41:441–455. https://doi.org/10.1016/j.ocl.2010.06.004

    Article  PubMed  Google Scholar 

  3. Bax M, Tydeman C, Flodmark O (2006) Clinical and MRI correlates of cerebral palsy: the European cerebral palsy study. JAMA 296:1602–1608. https://doi.org/10.1001/jama.296.13.1602

    Article  CAS  PubMed  Google Scholar 

  4. Riddell M, Kuo H-C, Zewdie E, Kirton A (2019) Mirror movements in children with unilateral cerebral palsy due to perinatal stroke: clinical correlates of plasticity reorganization. Dev Med Child Neurol. https://doi.org/10.1111/dmcn.14155

  5. Rosenbaum P (2007) The natural history of gross motor development in children with cerebral palsy aged 1 to 15 years. Dev Med Child Neurol 49:724. https://doi.org/10.1111/j.1469-8749.2007.00724.x

    Article  PubMed  Google Scholar 

  6. Cross JH, Jayakar P, Nordli D, Delalande O, Duchowny M, Wieser HG, Guerrini R, Mathern GW, International League against Epilepsy, Subcommission for Paediatric Epilepsy Surgery, Commissions of Neurosurgery and Paediatrics (2006) Proposed criteria for referral and evaluation of children for epilepsy surgery: recommendations of the Subcommission for Pediatric Epilepsy Surgery. Epilepsia 47:952–959. https://doi.org/10.1111/j.1528-1167.2006.00569.x

    Article  PubMed  Google Scholar 

  7. Battaglia D, Veggiotti P, Lettori D, Tamburrini G, Tartaglione T, Graziano A, Veredice C, Sacco A, Chieffo D, Pecoraro A, Colosimo C, di Rocco C, Dravet Ch, Guzzetta F (2009) Functional hemispherectomy in children with epilepsy and CSWS due to unilateral early brain injury including thalamus: sudden recovery of CSWS. Epilepsy Res 87:290–298. https://doi.org/10.1016/j.eplepsyres.2009.09.014

    Article  CAS  PubMed  Google Scholar 

  8. Jadhav T, Cross JH (2012) Surgical approaches to treating epilepsy in children. Curr Treat Options Neurol 14:620–629. https://doi.org/10.1007/s11940-012-0203-8

    Article  PubMed  Google Scholar 

  9. Dwivedi R, Ramanujam B, Chandra PS, Sapra S, Gulati S, Kalaivani M, Garg A, Bal CS, Tripathi M, Dwivedi SN, Sagar R, Sarkar C, Tripathi M (2017) Surgery for drug-resistant epilepsy in children. N Engl J Med 377:1639–1647. https://doi.org/10.1056/NEJMoa1615335

    Article  PubMed  Google Scholar 

  10. Spencer S, Huh L (2008) Outcomes of epilepsy surgery in adults and children. Lancet Neurol 7:525–537. https://doi.org/10.1016/S1474-4422(08)70109-1

    Article  PubMed  Google Scholar 

  11. Zsoter A, Pieper T, Kudernatsch M, Staudt M (2012) Predicting hand function after hemispherotomy: TMS versus fMRI in hemispheric polymicrogyria. Epilepsia 53:e98–e101. https://doi.org/10.1111/j.1528-1167.2012.03452.x

    Article  PubMed  Google Scholar 

  12. Pilato F, Profice P, Ranieri F, Capone F, di Iorio R, Florio L, di Lazzaro V (2012) Synaptic plasticity in neurodegenerative diseases evaluated and modulated by in vivo neurophysiological techniques. Mol Neurobiol 46:563–571. https://doi.org/10.1007/s12035-012-8302-9

    Article  CAS  PubMed  Google Scholar 

  13. Pilato F, Dileone M, Capone F, Profice P, Caulo M, Battaglia D, Ranieri F, Oliviero A, Florio L, Graziano A, di Rocco C, Massimi L, di Lazzaro V (2009) Unaffected motor cortex remodeling after hemispherectomy in an epileptic cerebral palsy patient. A TMS and fMRI study. Epilepsy Res 85:243–251. https://doi.org/10.1016/j.eplepsyres.2009.03.016

    Article  PubMed  Google Scholar 

  14. Di Lazzaro V, Profice P, Pilato F et al (2012) The level of cortical afferent inhibition in acute stroke correlates with long-term functional recovery in humans. Stroke 43:250–252. https://doi.org/10.1161/STROKEAHA.111.631085

    Article  PubMed  Google Scholar 

  15. Di Lazzaro V, Profice P, Pilato F et al (2010) Motor cortex plasticity predicts recovery in acute stroke. Cereb Cortex N Y N 1991 20:1523–1528. https://doi.org/10.1093/cercor/bhp216

    Article  Google Scholar 

  16. Di Pino G, Pellegrino G, Assenza G et al (2014) Modulation of brain plasticity in stroke: a novel model for neurorehabilitation. Nat Rev Neurol 10:597–608. https://doi.org/10.1038/nrneurol.2014.162

    Article  PubMed  Google Scholar 

  17. Stinear CM, Barber AP, Smale PR et al (2007) Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain 130:170–180. https://doi.org/10.1093/brain/awl333

    Article  PubMed  Google Scholar 

  18. Tassinari CA, Rubboli G (2019) Encephalopathy related to status epilepticus during slow sleep: current concepts and future directions. Epileptic Disord Int Epilepsy J Videotape 21:82–87. https://doi.org/10.1684/epd.2019.1062

    Article  Google Scholar 

  19. Bourke-Taylor H (2003) Melbourne assessment of unilateral upper limb function: construct validity and correlation with the pediatric evaluation of disability inventory. Dev Med Child Neurol 45:92–96

    Article  PubMed  Google Scholar 

  20. Maegaki Y, Maeoka Y, Seki A et al (1997) Facilitation of ipsilateral motor pathways during recovery from hemiplegia in two adolescent patients. Eur J Paediatr Neurol EJPN Off J Eur Paediatr Neurol Soc 1:79–84

    Article  CAS  Google Scholar 

  21. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501–519. https://doi.org/10.1113/jphysiol.1993.sp019912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Di Lazzaro V, Pilato F, Oliviero A et al (2006) Origin of facilitation of motor-evoked potentials after paired magnetic stimulation: direct recording of epidural activity in conscious humans. J Neurophysiol 96:1765–1771. https://doi.org/10.1152/jn.00360.2006

    Article  PubMed  Google Scholar 

  23. Smith SM (2004) Overview of fMRI analysis. Br J Radiol 77(2):S167–S175. https://doi.org/10.1259/bjr/33553595

    Article  PubMed  Google Scholar 

  24. Blatow M, Reinhardt J, Riffel K, Nennig E, Wengenroth M, Stippich C (2011) Clinical functional MRI of sensorimotor cortex using passive motor and sensory stimulation at 3 tesla. J Magn Reson Imaging JMRI 34:429–437. https://doi.org/10.1002/jmri.22629

    Article  PubMed  Google Scholar 

  25. Staudt M, Grodd W, Gerloff C et al (2002) Two types of ipsilateral reorganization in congenital hemiparesis: a TMS and fMRI study. Brain J Neurol 125:2222–2237

    Article  Google Scholar 

  26. Kirton A (2013) Modeling developmental plasticity after perinatal stroke: defining central therapeutic targets in cerebral palsy. Pediatr Neurol 48:81–94. https://doi.org/10.1016/j.pediatrneurol.2012.08.001

    Article  PubMed  Google Scholar 

  27. Zewdie E, Damji O, Ciechanski P, Seeger T, Kirton A (2017) Contralesional corticomotor neurophysiology in hemiparetic children with perinatal stroke. Neurorehabil Neural Repair 31:261–271. https://doi.org/10.1177/1545968316680485

    Article  PubMed  Google Scholar 

  28. Di Lazzaro V, Pilato F, Dileone M et al (2006) GABAA receptor subtype specific enhancement of inhibition in human motor cortex. J Physiol 575:721–726. https://doi.org/10.1113/jphysiol.2006.114694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Eyre JA (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

    Article  CAS  PubMed  Google Scholar 

  30. Grefkes C, Nowak DA, Eickhoff SB, Dafotakis M, Küst J, Karbe H, Fink GR (2008) Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann Neurol 63:236–246. https://doi.org/10.1002/ana.21228

    Article  PubMed  Google Scholar 

  31. Puig J, Blasco G, Schlaug G, Stinear CM, Daunis-I-Estadella P, Biarnes C, Figueras J, Serena J, Hernández-Pérez M, Alberich-Bayarri A, Castellanos M, Liebeskind DS, Demchuk AM, Menon BK, Thomalla G, Nael K, Wintermark M, Pedraza S (2017) Diffusion tensor imaging as a prognostic biomarker for motor recovery and rehabilitation after stroke. Neuroradiology 59:343–351. https://doi.org/10.1007/s00234-017-1816-0

    Article  PubMed  Google Scholar 

  32. Puig J, Blasco G, Terceño M et al (2019) Predicting motor outcome in acute intracerebral hemorrhage. AJNR Am J Neuroradiol. https://doi.org/10.3174/ajnr.A6038

Download references

Author information

Authors and Affiliations

  1. UOC Neurologia, Dipartimento di scienze dell’invecchiamento, neurologiche, ortopediche e della testa-collo, Fondazione Policlinico Universitario A. Gemelli—IRCCS, 00168, Rome, Italy

    Fabio Pilato

  2. Neurocenter of Southern Switzerland, Neuroradiology Department, Ospedale Regionale di Lugano, via Tesserete 46, 6901, Lugano, Switzerland

    Emanuele Pravatà

  3. UOC Neuropsichiatria infantile, Fondazione Policlinico Universitario A. Gemelli—IRCCS, Rome, Italy

    Domenica Battaglia

  4. Istituto Neurochirurgia, Università Cattolica del Sacro Cuore, Rome, Italy

    Domenica Battaglia & Luca Massimi

  5. UOC Radiologia e Neuroradiologia, Dipartimento di diagnostica per immagini, radioterapia oncologica ed ematologia, Fondazione Policlinico Universitario A. Gemelli—IRCCS, Rome, Italy

    Rosalinda Calandrelli

  6. UOC Neurochirurgia, Dipartimento di scienze dell’invecchiamento, neurologiche, ortopediche e della testa-collo, Fondazione Policlinico Universitario A. Gemelli—IRCCS, Rome, Italy

    Luca Massimi

  7. International Neuroscience Institute, Hannover, Germany

    Concezio Di Rocco

  8. Neurology, Neurophysiology and Neurobiology Unit, Department of Medicine, Università Campus Bio-Medico di Roma, Rome, Italy

    Vincenzo Di Lazzaro

Authors
  1. Fabio Pilato
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emanuele Pravatà
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Domenica Battaglia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rosalinda Calandrelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luca Massimi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Concezio Di Rocco
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vincenzo Di Lazzaro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fabio Pilato.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pilato, F., Pravatà, E., Battaglia, D. et al. Multimodal assessment of motor pathways and intracortical connections in functional hemispherectomy. Childs Nerv Syst 36, 3085–3093 (2020). https://doi.org/10.1007/s00381-020-04617-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00381-020-04617-3

Keywords

Search

Navigation