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Intraoperative neurophysiology of the cerebellum: a tabula rasa

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Abstract

Purpose

Cerebellar mutism (CM) is a condition that occurs predominantly in children, after posterior fossa surgery (PFS). It is characterized by motor, speech, and behavioral disorders. Despite widespread use of intraoperative neurophysiological monitoring (IONM), little is known about the neurophysiological aspects involved in the pathophysiology of CM. We reviewed the IONM literature to identify working hypotheses aimed to investigate intraoperatively the circuits involved in CM.

Methods

A systematic review of the literature was conducted using PubMed central database. Papers describing the use of IONM techniques in the cerebellum were selected, thoroughly reviewed, and discussed.

Results and discussion

Only two studies reported the use of intraoperative neurophysiology of the cerebellum, suggesting a possible somatotopic motor organization of the cerebellar cortex. In addition, extra-operative studies using transcranial magnetic stimulation showed the possibility to modulate—possibly through the dentato-thalamic-cortical (DTC) pathway—primary motor cortex output using an appropriate cerebellar stimulus. In theory, the preservation of this either inhibitory or facilitatory modulation may predict the preservation of this pathway, while a loss of the effect may indicate an injury to the pathway, and predict a CM. Analogously, in the extra-operative setting, the comparison of pre-operative and post-operative transcranial magnetic stimulation of the cerebellum may predict the onset of CM whenever a pre-existing modulatory effect is lost as a result of surgery.

Conclusion

Virtually, no data exist on the intraoperative neurophysiology of the cerebellum. This limited knowledge, nevertheless, offers a unique opportunity to pediatric neurosurgeons to develop and test working hypotheses on the pathophysiology of CM, through the use of IONM.

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References

  1. 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 

  2. Allen GI, Tsukahara N (1974) Cerebrocerebellar communication systems. Physiol Rev 54(4):957–1006

    Article  CAS  PubMed  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(5):535–544. https://doi.org/10.21037/qims.2016.10.11

    Article  PubMed  PubMed Central  Google Scholar 

  4. Brodal P (1978) Principles of organization of the monkey corticopontine projection. Brain Res 148(1):214–218

    Article  CAS  PubMed  Google Scholar 

  5. Deletis V, Sala F, Morota N (2000) Intraoperative neurophysiological monitoring and mapping during brain stem surgery: a modern approach. Oper Tech Neurosurg 3(2):109–113. https://doi.org/10.1053/oy.2000.6562

    Article  Google Scholar 

  6. Dum RP, Strick PL (2003) An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol 89(1):634–639. https://doi.org/10.1152/jn.00626.2002

    Article  PubMed  Google Scholar 

  7. Gordon N (2007) The cerebellum and cognition. Eur J Paediatr Neurol 11(4):232–234

    Article  PubMed  Google Scholar 

  8. Grimaldi G, Manto M (2012) Topography of cerebellar deficits in humans. Cerebellum:336–351

  9. Grodd W, Hülsmann E, Lotze M, Wildgruber D, Erb M (2001) Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Hum Brain Mapp 13(2):55–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Gudrunardottir T, Sehested A, Juhler M, Grill J, Schmiegelow K (2011) Cerebellar mutism: definitions, classification and grading of symptoms. Childs Nerv Syst 27(9):1361–1363

    Article  PubMed  Google Scholar 

  11. Gudrunardottir T, Sehested A, Juhler M, Schmiegelow K (2011) Cerebellar mutism: review of the literature. Childs Nerv Syst 27(3):355–363

    Article  PubMed  Google Scholar 

  12. Gudrunardottir T, Sehested A, Juhler M, Schmiegelow K (2011) Cerebellar mutism: incidence, risk factors and prognosis. Childs Nerv Syst 27(4):513–514

    Article  PubMed  Google Scholar 

  13. Gudrunardottir T, De Smet HJ, Bartha-Doering L, Van Dun K, Verhoeven J, Paquier P, Mariën P (2015) Posterior fossa syndrome (PFS) and cerebellar mutism. Linguist Cerebellum:257–313

  14. Hoover JE, Strick PL (1999) The organization of cerebellar and basal ganglia outputs to primary motor cortex as revealed by retrograde transneuronal transport of herpes simplex virus type 1. J Neurosci 19(4):1446–1463. https://doi.org/10.1523/JNEUROSCI.19-04-01446.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Iwata NK, Ugawa Y (2005) The effects of cerebellar stimulation on the motor cortical excitability in neurological disorders: a review. Cerebellum. 4(4):2018–2023. https://doi.org/10.1080/14734220500277007

    Article  Google Scholar 

  16. Kamali A, Karbasian N, Rabiei P, Cano A, Riascos RF, Tandon N, Arevalo O, Ocasio L, Younes K, Khayat-Khoei M, Mirbagheri S, Hasan KM (2018) Revealing the cerebello-ponto-hypothalamic pathway in the human brain. Neurosci Lett 677:1–5

    Article  CAS  PubMed  Google Scholar 

  17. Kelly RM, Strick PL (2003) Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci 23(23):8432–8444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 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(10):1294–1303

    Article  PubMed  PubMed Central  Google Scholar 

  19. Matano S (2001) Brief communication: proportions of the ventral half of the cerebellar dentate nucleus in humans and great apes. Am J Phys Anthropol 114(2):163–165. https://doi.org/10.1002/1096-8644(200102)114:2<163::AID-AJPA1016>3.0.CO;2-F

    Article  CAS  PubMed  Google Scholar 

  20. Matano S, Baron G, Stephan H, Frahm HD (1985) Volume comparisons in the cerebellar complex of primates. II. Cerebellar nuclei. Folia Primatol (Basel) 44(3–4):182–203. https://doi.org/10.1016/j.msea.2014.07.007

    Article  CAS  Google Scholar 

  21. Matsumoto R, Nair DR, LaPresto E, Najm I, Bingaman W, Shibasaki H, Lüders HO (2004) Functional connectivity in the human language system: a cortico-cortical evoked potential study. Brain 127(Pt10):2316–2330. https://doi.org/10.1093/brain/awh246

    Article  PubMed  Google Scholar 

  22. Matsumoto R, Nair DR, LaPresto E, Bingaman W, Shibasaki H, Lüders HO (2007) Functional connectivity in human cortical motor system: a cortico-cortical evoked potential study. Brain 130(PT 1):181–197. https://doi.org/10.1093/brain/awl257

    Article  PubMed  Google Scholar 

  23. Méndez Orellana C, Visch-Brink E, Vernooij M, Kalloe S, Satoer D, Vincent A, Van Der Lugt A, Smits M (2015) Crossed cerebrocerebellar language lateralization: an additional diagnostic feature for assessing atypical language representation in presurgical functional MR imaging. Am J Neuroradiol 36(3):518–524

    Article  PubMed  PubMed Central  Google Scholar 

  24. Middleton FA, Strick PL (1997) Dentate output channels: motor and cognitive components. Prog Brain Res 114:553–566. https://doi.org/10.1016/S0079-6123(08)63386-5

    Article  CAS  PubMed  Google Scholar 

  25. Morota N, Deletis V, Epstein FJ, Kofler M, Abbott R, Lee M, Ruskin K (1995) Brain stem mapping: neurophysiological localization of motor nuclei on the floor of the fourth ventricle. Neurosurgery 37(5):922–929. https://doi.org/10.1227/00006123-199511000-00011

    Article  CAS  PubMed  Google Scholar 

  26. Mottolese C, Richard N, Harquel S, Szathmari A, Sirigu A, Desmurget M (2013) Mapping motor representations in the human cerebellum. Brain 136(1):330–342

    Article  PubMed  Google Scholar 

  27. Mottolese C, Szathmari A, Beuriat PA, Sirigu A, Desmurget M (2015) Sensorimotor mapping of the human cerebellum during pineal region surgery. Neurochirurgie 61(2–3):101–105

    Article  CAS  PubMed  Google Scholar 

  28. Rekate HL, Grubb RL, Aram DM, Hahn JF, Ratcheson RA (1985) Muteness of cerebellar origin. Arch Neurol 42(7):697–698

    Article  CAS  PubMed  Google Scholar 

  29. Riddle CN, Baker SN (2010) Convergence of pyramidal and medial brain stem descending pathways onto macaque cervical spinal interneurons. J Neurophysiol 103(5):2821–2832. https://doi.org/10.1152/jn.00491.2009

    Article  PubMed  PubMed Central  Google Scholar 

  30. Riddle CN, Edgley SA, Baker SN (2009) Direct and indirect connections with upper limb motoneurons from the primate reticulospinal tract. J Neurosci 29(15):4993–4999. https://doi.org/10.1523/JNEUROSCI.3720-08.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Rijntjes M, Buechel C, Kiebel S, Weiller C (1999) Multiple somatotopic representations in the human cerebellum. Neuroreport 10(17):3653–3658. https://doi.org/10.1097/00001756-199911260-00035

    Article  CAS  PubMed  Google Scholar 

  32. Sala F, Kržan MJ, Deletis V (2002) Intraoperative neurophysiological monitoring in pediatric neurosurgery: why, when, how? Child’s Nerv Syst 18(6–7):264–287. https://doi.org/10.1007/s00381-002-0582-3

    Article  Google Scholar 

  33. Sala F, Lanteri P, Bricolo A (2004) Motor evoked potential monitoring for spinal cord and brain stem surgery. Adv Tech Stand Neurosurg 29:133–169

    Article  CAS  PubMed  Google Scholar 

  34. Sala F, Coppola A, Tramontano V (2015) Intraoperative neurophysiology in posterior fossa tumor surgery in children. Childs Nerv Syst 31:1791–1806. https://doi.org/10.1007/s00381-015-2893-1

    Article  PubMed  Google Scholar 

  35. Schmahmann JD (2004) Cognition and the cerebellum. Neurology 63(11):1991

    Article  Google Scholar 

  36. Schmahmann JD (2010) The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychol Rev 20(3):236–260

    Article  PubMed  Google Scholar 

  37. Schmahmann JD, Caplan D (2006) Cognition, emotion and the cerebellum. Brain 129(Pt 2):290–292

    Article  PubMed  Google Scholar 

  38. Schmahmann JD, Sherman JC (1998) The cerebellar cognitive affective syndrome. Brain 121(4):561–579

    Article  PubMed  Google Scholar 

  39. Schultz W, Montgomery EB, Marini R (1979) Proximal limb movements in response to microstimulation of primate dentate and interpositus nuclei mediated by brain-stem structures. Brain 102(1):127–146. https://doi.org/10.1093/brain/102.1.127

    Article  CAS  PubMed  Google Scholar 

  40. Sloan T (2010) Anesthesia and intraoperative neurophysiological monitoring in children. Child’s Nerv Syst (2):227–235. https://doi.org/10.1007/s00381-009-1023-3

    Article  PubMed  Google Scholar 

  41. Snider RS, Eldred E (1949) Maintenance of spontaneous activity within the cerebellum. Proc Soc Exp Biol Med 72:124–127

    Article  CAS  PubMed  Google Scholar 

  42. Soelva V, Hernáiz Driever P, Abbushi A, Rueckriegel S, Bruhn H, Eisner W, Thomale UW (2013) Fronto-cerebellar fiber tractography in pediatric patients following posterior fossa tumor surgery. Childs Nerv Syst 29(4):597–607

    Article  PubMed  Google Scholar 

  43. Stoodley CJ, Schmahmann JD (2008) Functional topography in the human cerebellum : a meta - analysis of neuroimaging studies. Neuroimage 44:489–501

    Article  PubMed  Google Scholar 

  44. Stoodley CJ, Schmahmann JD (2018) Functional topography of the human cerebellum. Handb Clin Neurol:59–70

  45. Stoodley CJ, Valera EM, Schmahmann JD (2012) Functional topography of the cerebellum for motor and cognitive tasks: an fMRI study. Neuroimage 59(2):1560–1570

    Article  PubMed  Google Scholar 

  46. Strauss C, Romstöck J, Fahlbusch R (1999) Pericollicular approaches to the rhomboid fossa. Part II. Neurophysiological basis. J Neurosurg 91(5):768–765. https://doi.org/10.3171/jns.1999.91.5.0768

    Article  CAS  PubMed  Google Scholar 

  47. Strick PL, Dum RP, Fiez JA (2009) Cerebellum and nonmotor function. Annu Rev Neurosci 32:413–434. https://doi.org/10.1146/annurev.neuro.31.060407.125606

    Article  CAS  PubMed  Google Scholar 

  48. Tamburrini G, Frassanito P, Chieffo D, Massimi L, Caldarelli M, Di Rocco C (2015) Cerebellar mutism. Childs Nerv Syst 31(10):1841–1851. https://doi.org/10.1007/s00381-015-2803-6

    Article  CAS  PubMed  Google Scholar 

  49. Vaidya MV, Lazar M, Deniz CM, Haemer GG, Chen G, Bruno M, Sodickson DK, Lattanzi R, Collins CM (2018) Improved detection of fMRI activation in the cerebellum at 7T with dielectric pads extending the imaging region of a commercial head coil. J Magn Reson Imaging 48(2):431–440

    Article  PubMed  PubMed Central  Google Scholar 

  50. Van Baarsen KM, Grotenhuis JA (2014) The anatomical substrate of cerebellar mutism. Med Hypotheses 82(6):774–780

    Article  PubMed  Google Scholar 

  51. Wells EM, Walsh KS, Khademian ZP, Keating RF, Packer RJ (2008) The cerebellar mutism syndrome and its relation to cerebellar cognitive function and the cerebellar cognitive affective disorder. Dev Disabil Res Rev 14(3):221–228. https://doi.org/10.1002/ddrr.25

    Article  PubMed  Google Scholar 

  52. Wibroe M, Cappelen J, Castor C et al (2017) Cerebellar mutism syndrome in children with brain tumours of the posterior fossa. BMC Cancer 17(1):439. https://doi.org/10.1186/s12885-017-3416-0

    Article  PubMed  PubMed Central  Google Scholar 

  53. Wibroe M, Rochat P, Juhler M (2018) Cerebellar mutism syndrome and other complications after surgery in the posterior fossa in adults: a prospective study. World Neurosurg 110:e738–e746

    Article  PubMed  Google Scholar 

  54. Yecies D, Shpanskaya K, Grant G, Cheshier S, Hong D, Edwards M, Yeom K (2018) ASL perfusion imaging of the frontal lobes predicts the occurrence and resolution of posterior fossa syndrome. Medscape- May 09,2018

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Correspondence to Francesco Sala.

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D’Amico, A., Sala, F. Intraoperative neurophysiology of the cerebellum: a tabula rasa. Childs Nerv Syst 36, 1181–1186 (2020). https://doi.org/10.1007/s00381-020-04565-y

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