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The supplementary motor area syndrome and the cerebellar mutism syndrome: a pathoanatomical relationship?

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Abstract

Purpose

The supplementary motor area (SMA) syndrome affects adults after tumour resection in SMA neighbouring motor cortex. Cerebellar mutism syndrome (CMS) affects children after tumour resection in the posterior fossa. Both syndromes include disturbances in speech and motor function. The causes of the syndromes are unknown; however, surgical damage to the dentato-thalamo-cortical pathway (DTCP) has been associated with CMS. Thus, an anatomical link between the areas associated with the syndromes is possible.

We discuss the syndromes and their possible relationship through the DTCP.

Methods

We identified 61 articles (cohort studies, case reports and reviews) in MEDLINE and Embase searching for CMS, SMA syndrome or DTCP or synonyms and reviewed for evidence linking CMS and SMA.

Results

We found that SMA syndrome and CMS are similar regarding (1) surgical causation; (2) symptoms including speech impairment, disturbance in motor function and facial dysfunction; (3) delayed onset; (4) the courses of the syndromes are transient; and (5) long-term sequelae are seen in both. Relevant differences include age predominance of adults in SMA syndrome versus children in CMS.

Conclusions

The similarities of the two syndromes could be traced back to their mutual connection through the DTCP and their membership to a cerebro-cerebellar circuit. The connectivity network could explain the emotional changes and speech reduction in CMS. The difference in time of post-surgical onset may be related to the anatomical distance between the surgical damage to the cerebellum and the SMA, respectively, and the effector neural loop underpinning symptoms.

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References

  1. Akil H (2006) Re: cerebellar mutism in adults after posterior fossa surgery: a report of 2 cases (Sherman JH et al. Surg Neurol 2005;63:476-9). Surg Neurol 65:424. https://doi.org/10.1016/j.surneu.2005.12.023

    Article  PubMed  Google Scholar 

  2. Akkal D, Dum RP, Strick PL (2007) Supplementary motor area and presupplementary motor area: targets of basal ganglia and cerebellar output. J Neurosci 27:10659–10673. https://doi.org/10.1523/jneurosci.3134-07.2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Avula S, Spiteri M, Kumar R, Lewis E, Harave S, Windridge D, Ong C, Pizer B (2016) Post-operative pediatric cerebellar mutism syndrome and its association with hypertrophic olivary degeneration. Quant Imaging Med Surg 6:535–544. https://doi.org/10.21037/qims.2016.10.11

    Article  PubMed  PubMed Central  Google Scholar 

  4. 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:e00926. https://doi.org/10.1002/brb3.926

    Article  PubMed  PubMed Central  Google Scholar 

  5. Basu AP, Taylor PN, Lowther E, Forsyth EO, Blamire AM, Forsyth RJ (2015) Structural connectivity in a paediatric case of anarchic hand syndrome. BMC Neurol 15:234. https://doi.org/10.1186/s12883-015-0477-z

    Article  PubMed  PubMed Central  Google Scholar 

  6. Cakir Y, Karakisi D, Kocanaogullari O (1994) Cerebellar mutism in an adult: case report. Surg Neurol 41:342–344

    Article  CAS  PubMed  Google Scholar 

  7. Catani M, Dell'acqua F, Vergani F, Malik F, Hodge H, Roy P, Valabregue R, Thiebaut de Schotten M (2012) Short frontal lobe connections of the human brain. Cortex 48:273–291. https://doi.org/10.1016/j.cortex.2011.12.001

    Article  PubMed  Google Scholar 

  8. Crutchfield JS, Sawaya R, Meyers CA, Moore BD 3rd (1994) Postoperative mutism in neurosurgery. Report of two cases. J Neurosurg 81:115–121. https://doi.org/10.3171/jns.1994.81.1.0115

    Article  CAS  PubMed  Google Scholar 

  9. Dailey AT, McKhann GM 2nd, Berger MS (1995) The pathophysiology of oral pharyngeal apraxia and mutism following posterior fossa tumor resection in children. J Neurosurg 83:467–475. https://doi.org/10.3171/jns.1995.83.3.0467

    Article  CAS  PubMed  Google Scholar 

  10. D'Avanzo R, Scuotto A, Natale M, Scotto P, Cioffi FA (1993) Transient "cerebellar" mutism in lesions of the mesencephalic-cerebellar region. Acta Neurol 15:289–296

    CAS  Google Scholar 

  11. De Smet HJ, Baillieux H, Wackenier P, De Praeter M, Engelborghs S, Paquier PF, De Deyn PP, Marien P (2009) Long-term cognitive deficits following posterior fossa tumor resection: a neuropsychological and functional neuroimaging follow-up study. Neuropsychology 23:694–704. https://doi.org/10.1037/a0016106

    Article  PubMed  Google Scholar 

  12. De Smet HJ, Paquier P, Verhoeven J, Marien P (2013) The cerebellum: its role in language and related cognitive and affective functions. Brain Lang 127:334–342. https://doi.org/10.1016/j.bandl.2012.11.001

    Article  PubMed  Google Scholar 

  13. Della Sala S, Francescani A, Spinnler H (2002) Gait apraxia after bilateral supplementary motor area lesion. J Neurol Neurosurg Psychiatry 72:77–85

    Article  CAS  PubMed  Google Scholar 

  14. Duffau H (2012) Cortical and subcortical brain mapping. In: Schmidek and sweet - operative neurosurgical techniques, pp 80–93

    Chapter  Google Scholar 

  15. Duffau H, Lopes M, Denvil D, Capelle L (2001) Delayed onset of the supplementary motor area syndrome after surgical resection of the mesial frontal lobe: a time course study using intraoperative mapping in an awake patient. Stereotact Funct Neurosurg 76:74–82. https://doi.org/10.1159/000056496

    Article  CAS  PubMed  Google Scholar 

  16. Dunwoody GW, Alsagoff ZS, Yuan SY (1997) Cerebellar mutism with subsequent dysarthria in an adult: case report. Br J Neurosurg 11:161–163

    Article  CAS  PubMed  Google Scholar 

  17. Fontaine D, Capelle L, Duffau H (2002) Somatotopy of the supplementary motor area: evidence from correlation of the extent of surgical resection with the clinical patterns of deficit. Neurosurgery 50:297–303 discussion 303-295

    PubMed  Google Scholar 

  18. Gedik GK, Sari O, Koktekir E, Akdemir G (2017) Fluorodeoxyglucose positron emission tomography/computed tomography findings in a patient with cerebellar mutism after operation in posterior fossa. Asian J Surg 40:166–170. https://doi.org/10.1016/j.asjsur.2014.01.004

    Article  PubMed  Google Scholar 

  19. Gudrunardottir T, Morgan AT, Lux AL, Walker DA, Walsh KS, Wells EM, Wisoff JH, Juhler M, Schmahmann JD, Keating RF, Catsman-Berrevoets C (2016) Consensus paper on post-operative pediatric cerebellar mutism syndrome: the Iceland Delphi results. Child’s Nervous Syst 32:1195–1203. https://doi.org/10.1007/s00381-016-3093-3

    Article  Google Scholar 

  20. Han S, Wang Z, Wang Y, Wu A (2013) Transcerebellomedullary fissure approach to lesions of the fourth ventricle: less is more? Acta Neurochir 155:1011–1016. https://doi.org/10.1007/s00701-013-1689-x

    Article  PubMed  Google Scholar 

  21. Heiferman DM, Ackerman PD, Hayward DM, Primeau MJ, Anderson DE, Prabhu VC (2014) Bilateral supplementary motor area syndrome causing akinetic mutism following parasagittal meningioma resection. Neurosci Discov 2. https://doi.org/10.7243/2052-6946-2-7

    Article  Google Scholar 

  22. Ildan F, Tuna M, Erman T, Gocer AI, Zeren M, Cetinalp E (2002) The evaluation and comparison of cerebellar mutism in children and adults after posterior fossa surgery: report of two adult cases and review of the literature. Acta Neurochir 144:463–473. https://doi.org/10.1007/s007010200067

    Article  CAS  PubMed  Google Scholar 

  23. 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 70:1152–1168; discussion 1168. https://doi.org/10.1227/NEU.0b013e31823f6001

    Article  PubMed  Google Scholar 

  24. Krainik A, Duffau H, Capelle L, Cornu P, Boch AL, Mangin JF, Le Bihan D, Marsault C, Chiras J, Lehericy S (2004) Role of the healthy hemisphere in recovery after resection of the supplementary motor area. Neurology 62:1323–1332

    Article  CAS  PubMed  Google Scholar 

  25. 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 34:301–314

    Article  CAS  PubMed  Google Scholar 

  26. Law N, Greenberg M, Bouffet E, Taylor MD, Laughlin S, Strother D, Fryer C, McConnell D, Hukin J, Kaise C, Wang F, Mabbott DJ (2012) Clinical and neuroanatomical predictors of cerebellar mutism syndrome. Neuro-oncology 14:1294–1303. https://doi.org/10.1093/neuonc/nos160

    Article  PubMed  PubMed Central  Google Scholar 

  27. Marien P, De Smet HJ, Wijgerde E, Verhoeven J, Crols R, De Deyn PP (2013) Posterior fossa syndrome in adults: a new case and comprehensive survey of the literature. Cortex 49:284–300. https://doi.org/10.1016/j.cortex.2011.06.018

    Article  PubMed  Google Scholar 

  28. Marien P, Ackermann H, Adamaszek M, Barwood CH, Beaton A, Desmond J, De Witte E, Fawcett AJ, Hertrich I, Kuper M, Leggio M, Marvel C, Molinari M, Murdoch BE, Nicolson RI, Schmahmann JD, Stoodley CJ, Thurling M, Timmann D, Wouters E, Ziegler W (2014) Consensus paper: language and the cerebellum: an ongoing enigma. Cerebellum (London, England) 13:386–410. https://doi.org/10.1007/s12311-013-0540-5

    Article  PubMed Central  Google Scholar 

  29. McEvoy SD, Lee A, Poliakov A, Friedman S, Shaw D, Browd SR, Ellenbogen RG, Ojemann JG, Mac Donald CL (2016) Longitudinal cerebellar diffusion tensor imaging changes in posterior fossa syndrome. NeuroImage Clin 12:582–590. https://doi.org/10.1016/j.nicl.2016.09.007

    Article  PubMed  PubMed Central  Google Scholar 

  30. Miller NG, Reddick WE, Kocak M, Glass JO, Lobel U, Morris B, Gajjar A, Patay Z (2010) Cerebellocerebral diaschisis is the likely mechanism of postsurgical posterior fossa syndrome in pediatric patients with midline cerebellar tumors. AJNR Am J Neuroradiol 31:288–294. https://doi.org/10.3174/ajnr.A1821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Morris EB, Phillips NS, Laningham FH, Patay Z, Gajjar A, Wallace D, Boop F, Sanford R, Ness KK, Ogg RJ (2009) Proximal dentatothalamocortical tract involvement in posterior fossa syndrome. Brain 132:3087–3095. https://doi.org/10.1093/brain/awp241

    Article  PubMed  PubMed Central  Google Scholar 

  32. Moxon-Emre I, Bouffet E, Taylor MD, Laperriere N, Scantlebury N, Law N, Spiegler BJ, Malkin D, Janzen L, Mabbott D (2014) Impact of craniospinal dose, boost volume, and neurologic complications on intellectual outcome in patients with medulloblastoma. J Clin Oncol 32:1760–1768. https://doi.org/10.1200/jco.2013.52.3290

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  34. Palmer SL, Hassall T, Evankovich K, Mabbott DJ, Bonner M, Deluca C, Cohn R, Fisher MJ, Morris EB, Broniscer A, Gajjar A (2010) Neurocognitive outcome 12 months following cerebellar mutism syndrome in pediatric patients with medulloblastoma. Neuro-oncology 12:1311–1317. https://doi.org/10.1093/neuonc/noq094

    Article  PubMed  PubMed Central  Google Scholar 

  35. Patay Z (2015) Postoperative posterior fossa syndrome: unraveling the etiology and underlying pathophysiology by using magnetic resonance imaging. Child’s Nervous Syst 31:1853–1858. https://doi.org/10.1007/s00381-015-2796-1

    Article  Google Scholar 

  36. Patay Z, Enterkin J, Harreld JH, Yuan Y, Lobel U, Rumboldt Z, Khan R, Boop F (2014) MR imaging evaluation of inferior olivary nuclei: comparison of postoperative subjects with and without posterior fossa syndrome. AJNR Am J Neuroradiol 35:797–802. https://doi.org/10.3174/ajnr.A3762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Peraud A, Meschede M, Eisner W, Ilmberger J, Reulen HJ (2002) Surgical resection of grade II astrocytomas in the superior frontal gyrus. Neurosurgery 50:966–975 discussion 975-967

    PubMed  Google Scholar 

  38. Pitsika M, Tsitouras V (2013) Cerebellar mutism. J Neurosurg Pediatr 12:604–614. https://doi.org/10.3171/2013.8.peds13168

    Article  PubMed  Google Scholar 

  39. Pollack IF, Polinko P, Albright AL, Towbin R, Fitz C (1995) Mutism and pseudobulbar symptoms after resection of posterior fossa tumors in children: incidence and pathophysiology. Neurosurgery 37:885–893

    Article  CAS  PubMed  Google Scholar 

  40. Potgieser AR, de Jong BM, Wagemakers M, Hoving EW, Groen RJ (2014) Insights from the supplementary motor area syndrome in balancing movement initiation and inhibition. Front Hum Neurosci 8:960. https://doi.org/10.3389/fnhum.2014.00960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Radman N, Cacioppo S, Spierer L, Schmidlin E, Mayer E, Annoni JM (2013) Posterior SMA syndrome following subcortical stroke: contralateral akinesia reversed by visual feedback. Neuropsychologia 51:2605–2610. https://doi.org/10.1016/j.neuropsychologia.2013.08.004

    Article  PubMed  Google Scholar 

  42. Ramnani N (2006) The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci 7:511–522. https://doi.org/10.1038/nrn1953

    Article  CAS  PubMed  Google Scholar 

  43. Reed-Berendt R, Phillips B, Picton S, Chumas P, Warren D, Livingston JH, Hughes E, Morrall MC (2014) Cause and outcome of cerebellar mutism: evidence from a systematic review. Child's Nervous Syst 30:375–385. https://doi.org/10.1007/s00381-014-2356-0

    Article  Google Scholar 

  44. Robertson PL, Muraszko KM, Holmes EJ, Sposto R, Packer RJ, Gajjar A, Dias MS, Allen JC (2006) Incidence and severity of postoperative cerebellar mutism syndrome in children with medulloblastoma: a prospective study by the Children’s Oncology Group. J Neurosurg 105:444–451. https://doi.org/10.3171/ped.2006.105.6.444

    Article  PubMed  Google Scholar 

  45. Rostomily RC, Berger MS, Ojemann GA, Lettich E (1991) Postoperative deficits and functional recovery following removal of tumors involving the dominant hemisphere supplementary motor area. J Neurosurg 75:62–68. https://doi.org/10.3171/jns.1991.75.1.0062

    Article  CAS  PubMed  Google Scholar 

  46. 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 52:506–516 discussiom 515-506

    Article  PubMed  Google Scholar 

  47. Ryu JS, Chun MH, You DS (2013) Supplementary motor area syndrome and flexor synergy of the lower extremities. Ann Rehabil Med 37:735–739. https://doi.org/10.5535/arm.2013.37.5.735

    Article  PubMed  PubMed Central  Google Scholar 

  48. Salvati M, Missori P, Lunardi P, Orlando ER (1991) Transient cerebellar mutism after posterior cranial fossa surgery in an adult. Case report and review of the literature. Clin Neurol Neurosurg 93:313–316

    Article  CAS  PubMed  Google Scholar 

  49. Sherman JH, Sheehan JP, Elias WJ, Jane JA Sr (2005) Cerebellar mutism in adults after posterior fossa surgery: a report of 2 cases. Surg Neurol 63:476–479. https://doi.org/10.1016/j.surneu.2004.06.015

    Article  PubMed  Google Scholar 

  50. Strata P (2015) The emotional cerebellum. Cerebellum (London, England) 14:570–577. https://doi.org/10.1007/s12311-015-0649-9

    Article  Google Scholar 

  51. Tellmann S, Bludau S, Eickhoff S, Mohlberg H, Minnerop M, Amunts K (2015) Cytoarchitectonic mapping of the human brain cerebellar nuclei in stereotaxic space and delineation of their co-activation patterns. Front Neuroanat 9:54. https://doi.org/10.3389/fnana.2015.00054

    Article  PubMed  PubMed Central  Google Scholar 

  52. Tomasello F, Conti A, Angileri FF, Cardali S (2015) Telo-velar approach to fourth-ventricle tumours: how I do it. Acta Neurochir 157:607–610. https://doi.org/10.1007/s00701-015-2358-z

    Article  PubMed  Google Scholar 

  53. Van Calenbergh F, Van de Laar A, Plets C, Goffin J, Casaer P (1995) Transient cerebellar mutism after posterior fossa surgery in children. Neurosurgery 37:894–898

    Article  PubMed  Google Scholar 

  54. Vassal M, Charroud C, Deverdun J, Le Bars E, Molino F, Bonnetblanc F, Boyer A, Dutta A, Herbet G, Moritz-Gasser S, Bonafe 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 126:1181–1190. https://doi.org/10.3171/2016.4.jns152484

    Article  PubMed  Google Scholar 

  55. Vergani F, Lacerda L, Martino J, Attems J, Morris C, Mitchell P, Thiebaut de Schotten M, Dell'Acqua F (2014) White matter connections of the supplementary motor area in humans. J Neurol Neurosurg Psychiatry 85:1377–1385. https://doi.org/10.1136/jnnp-2013-307492

    Article  PubMed  Google Scholar 

  56. Wells EM, Khademian ZP, Walsh KS, Vezina G, Sposto R, Keating RF, Packer RJ (2010) Postoperative cerebellar mutism syndrome following treatment of medulloblastoma: neuroradiographic features and origin. J Neurosurg Pediatr 5:329–334. https://doi.org/10.3171/2009.11.peds09131

    Article  PubMed  Google Scholar 

  57. Wibroe M, Rochat P, Juhler M (2017) Cerebellar mutism syndrome and other complications following surgery in the posterior fossa in adults: a prospective study. World Neurosurg 110:e738–e746. https://doi.org/10.1016/j.wneu.2017.11.100

    Article  PubMed  Google Scholar 

  58. Wilson TW, Slason E, Asherin R, Kronberg E, Reite ML, Teale PD, Rojas DC (2010) An extended motor network generates beta and gamma oscillatory perturbations during development. Brain Cogn 73:75–84. https://doi.org/10.1016/j.bandc.2010.03.001

    Article  PubMed  PubMed Central  Google Scholar 

  59. Wolpe N, Ingram JN, Tsvetanov KA, Geerligs L, Kievit RA, Henson RN, Wolpert DM, Rowe JB (2016) Ageing increases reliance on sensorimotor prediction through structural and functional differences in frontostriatal circuits. Nat Commun 7:13034. https://doi.org/10.1038/ncomms13034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Yildiz O, Kabatas S, Yilmaz C, Altinors N, Agaoglu B (2010) Cerebellar mutism syndrome and its relation to cerebellar cognitive and affective function: review of the literature. Ann Indian Acad Neurol 13:23–27. https://doi.org/10.4103/0972-2327.61272

    Article  PubMed  PubMed Central  Google Scholar 

  61. Zaheer SN, Wood M (2010) Experiences with the telovelar approach to fourth ventricular tumors in children. Pediatr Neurosurg 46:340–343. https://doi.org/10.1159/000321539

    Article  PubMed  Google Scholar 

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Funding

This project was partially funded by Danish Cancer Society (Kræftens Bekæmpelse) and Danish Child Cancer Foundation (Børnecancerfonden).

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Authors and Affiliations

  1. Department of Neurosurgery, The University Hospital Rigshospitalet, Copenhagen, Denmark

    Jonathan Grønbæk, Morten Wibroe & Marianne Juhler

  2. Department of Paediatrics and Adolescent Medicine, The University Hospital Rigshospitalet, Copenhagen, Denmark

    Jonathan Grønbæk & Morten Wibroe

  3. Department of Neurology, The Queen Elizabeth University Hospital, University of Glasgow, Glasgow, UK

    Emanuela Molinari

  4. Department of Radiology, Alder Hey Children’s NHS Foundation Trust, Liverpool, UK

    Shivaram Avula

  5. Department of Neurosurgery, Aarhus University Hospital, Aarhus, Denmark

    Gorm Oettingen & Marianne Juhler

  6. Institute of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark

    Marianne Juhler

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  1. Jonathan Grønbæk
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Grønbæk, J., Molinari, E., Avula, S. et al. The supplementary motor area syndrome and the cerebellar mutism syndrome: a pathoanatomical relationship?. Childs Nerv Syst 36, 1197–1204 (2020). https://doi.org/10.1007/s00381-019-04202-3

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