Skip to main content

Advertisement

SpringerLink
Log in

Epilepsy surgery in the supplementary motor area

Epilepsiechirurgie im supplementär motorischen Areal

  • Übersichten
  • Published:
Zeitschrift für Epileptologie Aims and scope Submit manuscript

Abstract

The supplementary motor area (SMA) is a critical modulating hub of the large-scale bihemispherical motor network; however, there is evidence that resective surgery for otherwise intractable mediofrontal epilepsy of lesional and nonlesional origins is possible with an acceptable neurological risk. Neurosurgical resection of this region to treat epilepsy does not result in permanent neurological deficits. A transient SMA syndrome including severe akinesia on the contralateral side with preserved muscle tone occurs in the early postoperative period. The symptoms, however, disappear after the first postoperative weeks according to most reports. The underlying mechanism of these transient deficits and the subsequent functional recovery remains to be elucidated. Recent observations point to the role of the callosal fibers and the frontal aslant tract in the recovery process. The aim of this review is to give a short summary of current knowledge on surgery in the supplementary motor area with a focus on the literature on epilepsy surgery.

Zusammenfassung

Das supplementär motorische Areal (SMA) stellt einen entscheidenden modulierenden Schaltpunkt des großräumigen bihemisphärischen motorischen Netzes dar, es gibt jedoch Hinweise darauf, dass für ansonsten nicht erfolgreich behandelbare mediofrontale Epilepsie läsionalen und nichtläsionalen Ursprungs ein resektiver chirurgischer Eingriff mit einem akzeptablen neurologischen Risiko möglich ist. Die neurochirurgische Resektion dieser Region zur Therapie der Epilepsie führt nicht zu permanenten neurologischen Defiziten. In der frühen postoperativen Phase tritt ein transientes SMA-Syndrom mit schwerer Akinesie auf der kontralateralen Seite bei erhaltenem Muskeltonus auf. Jedoch bilden sich den meisten Publikationen zufolge die Symptome nach den ersten postoperativen Wochen zurück. Der diesen transienten Defiziten und der anschließenden funktionellen Wiederherstellung zugrunde liegende Mechanismus bleibt zu eruieren. Kürzlich erfolgte Beobachtungen weisen auf die Bedeutung der kallosalen Fasern und des frontalen Aslant-Trakts im Wiederherstellungsprozess hin. Das Ziel der vorliegenden Übersichtsarbeit ist es, eine kurze Zusammenfassung des derzeitigen Wissens zur Chirurgie im SMA mit Fokus auf die Literatur zur Epilepsiechirurgie zu geben.

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

Similar content being viewed by others

References

  1. Penfield W (1954) Mechanisms of voluntary movement. Brain 77(1):1–17. https://doi.org/10.1093/brain/77.1.1

    Article  CAS  PubMed  Google Scholar 

  2. Penfield W, Welch K (1951) The supplementary motor area of the cerebral cortex; a clinical and experimental study. AMA Arch Neurol Psychiatry 66(3):289–317. https://doi.org/10.1001/archneurpsyc.1951.02320090038004

    Article  CAS  PubMed  Google Scholar 

  3. Nachev P, Kennard C, Husain M (2008) Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9(11):856–869. https://doi.org/10.1038/nrn2478

    Article  CAS  PubMed  Google Scholar 

  4. Fried I, Katz A, McCarthy G, Sass KJ, Williamson P, Spencer SS, Spencer DD (1991) Functional organization of human supplementary motor cortex studied by electrical stimulation. J Neurosci 11(11):3656–3666. https://doi.org/10.1523/JNEUROSCI.11-11-03656.1991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Chauvel PY, Rey M, Buser P, Bancaud J (1996) What stimulation of the supplementary motor area in humans tells about its functional organization. Adv Neurol 70:199–209

    CAS  PubMed  Google Scholar 

  6. Uematsu S, Lesser R, Fisher RS, Gordon B, Hara K, Krauss GL, Vining EP, Webber RW (1992) Motor and sensory cortex in humans: topography studied with chronic subdural stimulation. Neurosurgery 31(1):59–71. https://doi.org/10.1227/00006123-199207000-00009 (discussion 71–2)

    Article  CAS  PubMed  Google Scholar 

  7. Lüders HO, Lesser RP, Dinner DS, Morris HH, Wyllie E, Godoy J, Hahn JH (1992) A negative motor response elicited by electrical stimulation of the human frontal cortex. Adv Neurol 57:149–157

    PubMed  Google Scholar 

  8. Penfield W, Welch K (1949) Instability of response to stimulation of the sensorimotor cortex of man. J Physiol 109(3–4):358–365. https://doi.org/10.1113/jphysiol.1949.sp004399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP, Bitar A, Fohanno D (2002) Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 125(Pt 1):199–214. https://doi.org/10.1093/brain/awf016

    Article  PubMed  Google Scholar 

  10. Tachibana N, Shinde A, Ikeda A, Akiguchi I, Kimura J, Shibasaki H (1996) Supplementary motor area seizure resembling sleep disorder. Sleep 19(10):811–816. https://doi.org/10.1093/sleep/19.10.811

    Article  CAS  PubMed  Google Scholar 

  11. Morris HH 3rd, Dinner DS, Lüders H, Wyllie E, Kramer R (1988) Supplementary motor seizures: clinical and electroencephalographic findings. Neurology 38(7):1075–1082. https://doi.org/10.1212/wnl.38.7.1075

    Article  PubMed  Google Scholar 

  12. Alonso-Vanegas MA, San-Juan D, Buentello García RM, Castillo-Montoya C, Sentíes-Madrid H, Mascher EB, Bialik PS, Trenado C (2017) Long-term surgical results of supplementary motor area epilepsy surgery. J Neurosurg 127(5):1153–1159. https://doi.org/10.3171/2016.8.JNS16333

    Article  PubMed  Google Scholar 

  13. Zentner J, Hufnagel A, Pechstein U, Wolf HK, Schramm J (1996) Functional results after resective procedures involving the supplementary motor area. J Neurosurg 85(4):542–549. https://doi.org/10.3171/jns.1996.85.4.0542

    Article  CAS  PubMed  Google Scholar 

  14. Peraud A, Meschede M, Eisner W, Ilmberger J, Reulen HJ (2002) Surgical resection of grade II astrocytomas in the superior frontal gyrus. Neurosurgery 50(5):966–975. https://doi.org/10.1097/00006123-200205000-00009 (discussion 975–7)

    Article  PubMed  Google Scholar 

  15. Kasasbeh AS, Yarbrough CK, Limbrick DD, Steger-May K, Leach JL, Mangano FT, Smyth MD (2012) Characterization of the supplementary motor area syndrome and seizure outcome after medial frontal lobe resections in pediatric epilepsy surgery. Neurosurgery 70(5):1152–1168. https://doi.org/10.1227/NEU.0b013e31823f6001 (discussion 1168)

    Article  PubMed  Google Scholar 

  16. Klitsinikos D, Ekert JO, Carels A, Samandouras G (2021) Mapping and anatomo-surgical techniques for SMA-cingulum-corpus callosum gliomas; how I do it. Acta Neurochir 163(5):1239–1246. https://doi.org/10.1007/s00701-021-04774-7

    Article  PubMed  Google Scholar 

  17. Young JS, Gogos AJ, Aabedi AA, Morshed RA, Pereira MP, Lashof-Regas S, Mansoori Z, Luks T, Hervey-Jumper SL, Villanueva-Meyer JE, Berger MS (2021) Resection of supplementary motor area gliomas: revisiting supplementary motor syndrome and the role of the frontal aslant tract. J Neurosurg 1(34598138):1–7. https://doi.org/10.3171/2021.4.JNS21187

    Article  Google Scholar 

  18. Schramm S, Albers L, Ille S, Schröder A, Meyer B, Sollmann N, Krieg SM (2019) Navigated transcranial magnetic stimulation of the supplementary motor cortex disrupts fine motor skills in healthy adults. Sci Rep 9(1):17744. https://doi.org/10.1038/s41598-019-54302-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Schramm S, Sollmann N, Ille S, Meyer B, Krieg SM (2020) Application of navigated transcranial magnetic stimulation to map the supplementary motor area in healthy subjects. J Clin Neurophysiol 37(2):140–149. https://doi.org/10.1097/WNP.0000000000000530

    Article  PubMed  Google Scholar 

  20. Russell SM, Kelly PJ (2003) Incidence and clinical evolution of postoperative deficits after volumetric stereotactic resection of glial neoplasms involving the supplementary motor area. Neurosurgery 52(3):506–516. https://doi.org/10.1227/01.neu.0000047670.56996.53 (discussion 515–6)

    Article  PubMed  Google Scholar 

  21. Ulu MO, Tanriöver N, Ozlen F, Sanus GZ, Tanriverdi T, Ozkara C, Uzan M (2008) Surgical treatment of lesions involving the supplementary motor area: clinical results of 12 patients. Turk Neurosurg 18(3):286–293

    PubMed  Google Scholar 

  22. Rosenberg K, Nossek E, Liebling R, Fried I, Shapira-Lichter I, Hendler T, Ram Z (2010) Prediction of neurological deficits and recovery after surgery in the supplementary motor area: a prospective study in 26 patients. J Neurosurg 113(6):1152–1163. https://doi.org/10.3171/2010.6.JNS1090

    Article  PubMed  Google Scholar 

  23. Kim YH, Kim CH, Kim JS, Lee SK, Han JH, Kim CY, Chung CK (2013) Risk factor analysis of the development of new neurological deficits following supplementary motor area resection. J Neurosurg 119(1):7–14. https://doi.org/10.3171/2013.3.JNS121492

    Article  PubMed  Google Scholar 

  24. Ibe Y, Tosaka M, Horiguchi K, Sugawara K, Miyagishima T, Hirato M, Yoshimoto Y (2016) Resection extent of the supplementary motor area and post-operative neurological deficits in glioma surgery. Br J Neurosurg 30(3):323–329. https://doi.org/10.3109/02688697.2015.1133803

    Article  PubMed  Google Scholar 

  25. Nakajima R, Kinoshita M, Yahata T, Nakada M (2019) Recovery time from supplementary motor area syndrome: relationship to postoperative day 7 paralysis and damage of the cingulum. J Neurosurg 132(3):865–874. https://doi.org/10.3171/2018.10.JNS182391

    Article  PubMed  Google Scholar 

  26. Laplane D, Talairach J, Meininger V, Bancaud J, Orgogozo JM (1977) Clinical consequences of corticectomies involving the supplementary motor area in man. J Neurol Sci 34(3):301–314. https://doi.org/10.1016/0022-510x(77)90148-4

    Article  CAS  PubMed  Google Scholar 

  27. Krainik A, Lehéricy S, Duffau H, Vlaicu M, Poupon F, Capelle L, Cornu P, Clemenceau S, Sahel M, Valery CA, Boch AL, Mangin JF, Bihan DL, Marsault C (2001) Role of the supplementary motor area in motor deficit following medial frontal lobe surgery. Neurology 57(5):871–878. https://doi.org/10.1212/wnl.57.5.871

    Article  CAS  PubMed  Google Scholar 

  28. Endo Y, Saito Y, Otsuki T, Takahashi A, Nakata Y, Okada K, Hirozane M, Kaido T, Kaneko Y, Takada E, Okazaki T, Enokizno T, Saito T, Komaki H, Nakagawa E, Sugai K, Sasaki M (2014) Persistent verbal and behavioral deficits after resection of the left supplementary motor area in epilepsy surgery. Brain Dev 36(1):74–79. https://doi.org/10.1016/j.braindev.2013.01.002. Epub 2013 Feb 8. PMID: 24370003

    Article  PubMed  Google Scholar 

  29. Lim SH, Dinner DS, Pillay PK, Lüders H, Morris HH, Klem G, Wyllie E, Awad IA (1994) Functional anatomy of the human supplementary sensorimotor area: results of extraoperative electrical stimulation. Electroencephalogr Clin Neurophysiol 91(3):179–193. https://doi.org/10.1016/0013-4694(94)90068-x

    Article  CAS  PubMed  Google Scholar 

  30. Mayka MA, Corcos DM, Leurgans SE, Vaillancourt DE (2006) Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: a meta-analysis. Neuroimage 31(4):1453–1474. https://doi.org/10.1016/j.neuroimage.2006.02.004

    Article  PubMed  Google Scholar 

  31. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain: 3‑Dimensional proportional system: an approach to cerebral imaging. Thieme, New York

    Google Scholar 

  32. Dum RP, Strick PL (1991) The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci 11(3):667–689. https://doi.org/10.1523/JNEUROSCI.11-03-00667.1991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Oda K, Yamaguchi F, Enomoto H, Higuchi T, Morita A (2018) Prediction of recovery from supplementary motor area syndrome after brain tumor surgery: preoperative diffusion tensor tractography analysis and postoperative neurological clinical course. Neurosurg Focus 44(6):E3–29852764. https://doi.org/10.3171/2017.12.FOCUS17564

    Article  PubMed  Google Scholar 

  34. Otten ML, Mikell CB, Youngerman BE, Liston C, Sisti MB, Bruce JN, Small SA, McKhann GM 2nd (2012) Motor deficits correlate with resting state motor network connectivity in patients with brain tumours. Brain 135(Pt 4):1017–1026. https://doi.org/10.1093/brain/aws041

    Article  PubMed  PubMed Central  Google Scholar 

  35. Vassal M, Charroud C, Deverdun J, Le Bars E, Molino F, Bonnetblanc F, Boyer A, Dutta A, Herbet G, Moritz-Gasser S, Bonafé A, Duffau H, de Champfleur NM (2017) Recovery of functional connectivity of the sensorimotor network after surgery for diffuse low-grade gliomas involving the supplementary motor area. J Neurosurg 126(4):1181–1190. https://doi.org/10.3171/2016.4.JNS152484

    Article  PubMed  Google Scholar 

  36. Krainik A, Duffau H, Capelle L, Cornu P, Boch AL, Mangin JF, Le Bihan D, Marsault C, Chiras J, Lehéricy S (2004) Role of the healthy hemisphere in recovery after resection of the supplementary motor area. Neurology 62(8):1323–1332. https://doi.org/10.1212/01.wnl.0000120547.83482.b1

    Article  CAS  PubMed  Google Scholar 

  37. Catani M, Mesulam MM, Jakobsen E, Malik F, Martersteck A, Wieneke C, Thompson CK, Thiebaut de Schotten M, Dell’Acqua F, Weintraub S, Rogalski E (2013) A novel frontal pathway underlies verbal fluency in primary progressive aphasia. Brain 136(Pt 8):2619–2628. https://doi.org/10.1093/brain/awt163

    Article  PubMed  PubMed Central  Google Scholar 

  38. Dick AS, Bernal B, Tremblay P (2014) The language connectome: new pathways, new concepts. Neuroscientist 20(5):453–467. https://doi.org/10.1177/1073858413513502 (Erratum in: Neuroscientist. 2017 Feb. 23(1):95. PMID: 24342910)

    Article  PubMed  Google Scholar 

  39. Dick AS, Garic D, Graziano P, Tremblay P (2019) The frontal aslant tract (FAT) and its role in speech, language and executive function. Cortex 111:148–163. https://doi.org/10.1016/j.cortex.2018.10.015

    Article  PubMed  Google Scholar 

  40. Pinson H, Van Lerbeirghe J, Vanhauwaert D, Van Damme O, Hallaert G, Kalala JP (2021) The supplementary motor area syndrome: a neurosurgical review. Neurosurg Rev. https://doi.org/10.1007/s10143-021-01566-6

    Article  PubMed  Google Scholar 

  41. Young JS, Morshed RA, Mansoori Z, Cha S, Berger MS (2020) Disruption of frontal aslant tract is not associated with long-term postoperative language deficits. World Neurosurg 133:192–195. https://doi.org/10.1016/j.wneu.2019.09.128

    Article  PubMed  Google Scholar 

  42. Baker CM, Burks JD, Briggs RG, Smitherman AD, Glenn CA, Conner AK, Wu DH, Sughrue ME (2018) The crossed frontal aslant tract: a possible pathway involved in the recovery of supplementary motor area syndrome. Brain Behav 8(3):e926. https://doi.org/10.1002/brb3.926

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Geneva University Hospitals, Rue Gabrielle-Perret-Gentil 4, 1205, Geneva, Switzerland

    Daniel Kiss-Bodolay, Andrea Bartoli & Karl Schaller

  2. Faculty of Medicine, University of Geneva, Rue Gabrielle-Perret-Gentil 4, 1205, Geneva, Switzerland

    Daniel Kiss-Bodolay, Andrea Bartoli & Karl Schaller

Authors
  1. Daniel Kiss-Bodolay
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea Bartoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karl Schaller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel Kiss-Bodolay.

Ethics declarations

Conflict of interest

D. Kiss-Bodolay, A. Bartoli and K. Schaller declare that they have no competing interests.

For this article no studies with human participants or animals were performed by any of the authors. Research Ethics Board Approval was not required.

Additional information

figure qr

Scan QR code & read article online

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kiss-Bodolay, D., Bartoli, A. & Schaller, K. Epilepsy surgery in the supplementary motor area. Z. Epileptol. 35, 46–50 (2022). https://doi.org/10.1007/s10309-021-00465-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10309-021-00465-6

Keywords

Schlüsselwörter

Search

Navigation