Advertisement

Acta Neurochirurgica

, Volume 157, Issue 1, pp 77–84 | Cite as

The evolution of brain surgery on awake patients

  • Werner SurbeckEmail author
  • Gerhard Hildebrandt
  • Hugues Duffau
Review Article - History of Neurosurgery

Abstract

In the early days of modern neurological surgery, the inconveniences and potential dangers of general anesthesia by chloroform and ether using the so-called “open-drop technique” led to the quest for alternative methods of anesthesia. Besides preventing the feared side effects, the introduction of regional anesthesia revealed another decisive advantage over general anesthesia in neurosurgery: While intraoperative direct cortical stimulation under general anesthesia could only delineate the motor area (by evocation of contralateral muscular contraction), now, the awake patients were able to report sensations elicited by this method. These properties advanced regional anesthesia to the regimen of choice for cranial surgeries in the first half of the 20th century. While technical advances and new drugs led to a progressive return to general anesthesia for neurosurgical procedures, the use of regional anesthesia for epilepsy surgery has only decreased in recent decades. Meanwhile, awake craniotomies regained popularity in oncologically motivated surgeries, especially in craniotomies for diffuse low-grade gliomas. Intraoperative mapping of brain functions using electrical stimulation in awake patients enables not only for increased tumor removal while preserving the functional status of the patients but also opens a window to cognitive neuroscience. Observations during such interventions and their correlation with both pre − and postoperative neuropsychological examinations and functional neuroimaging is progressively leading to new insights into the complex functional anatomy of the human brain. Furthermore, it broadens our knowledge on cerebral network reorganization in the presence of disease—with implications for all disciplines of clinical neuroscience.

Keywords

Awake craniotomy History Epilepsy Low-grade glioma Brain networks 

Notes

Acknowledgments

The authors thank Beatrice Scholtes for English editing.

Conflicts of interest

None.

References

  1. 1.
    Alstott J, Breakspear M, Hagmann P, Cammoun L, Sporns O (2009) Modeling the impact of lesions in the human brain. PLoS Comput Biol 5(6):e1000408PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Assaf Y, Pasternak O (2008) Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 34(1):51–61PubMedCrossRefGoogle Scholar
  3. 3.
    Bartholow R (1874) Experimental investigations into the functions of the human brain. Am J Med Sci 67:305–313CrossRefGoogle Scholar
  4. 4.
    Beevor C, Horsley V (1890) An experimental investigation into the arrangement of the excitable fibres of the internal capsule of the bonnet monkey (Macacus sinicus). Philos Trans R Soc London 181:49–88CrossRefGoogle Scholar
  5. 5.
    Bennet A, Godlee R (1885) Case of cerebral tumour. Surg Treat Med-Chir Trans 68:243–275Google Scholar
  6. 6.
    Bennett CM, Miller MB (2010) How reliable are the results from functional magnetic resonance imaging? Ann N Y Acad Sci 1191:133–155PubMedCrossRefGoogle Scholar
  7. 7.
    Berger MS, Ojemann GA (1992) Intraoperative brain mapping techniques in neuro-oncology. Stereotact Funct Neurosurg 58:153–161PubMedCrossRefGoogle Scholar
  8. 8.
    Broca P (1861) Remarques sur le siège de la faculté du langage articule suivies d’une observation d’aphemie. Bull Soc Anat Paris 6:330–357Google Scholar
  9. 9.
    Catani M (2007) From hodology to function. Brain 130(Pt 3):602–605PubMedCrossRefGoogle Scholar
  10. 10.
    Catani M, Ffytche DH (2005) The rises and falls of disconnection syndromes. Brain 128(Pt 10):2224–2239PubMedCrossRefGoogle Scholar
  11. 11.
    Chatrian G, Quesney L (1997) Intraoperative electrocorticography. In: Engel JJ, Pedley T (eds) Epilepsy a Compr. Textb. Lippincott-Raven Publishers, Philadelphia, pp 1749–1765Google Scholar
  12. 12.
    Cushing H (1909) A note upon the faradic stimulation of the postcentral gyrus in conscious patients. Brain 32(1):44–53CrossRefGoogle Scholar
  13. 13.
    Danks RA, Aglio LS, Gugino LD, Black PM (2000) Craniotomy under local anesthesia and monitored conscious sedation for the resection of tumors involving eloquent cortex. J Neurooncol 49:131–139PubMedCrossRefGoogle Scholar
  14. 14.
    Deras P, Moulinié G, Maldonado IL, Moritz-Gasser S, Duffau H, Bertram L (2012) Intermittent general anesthesia with controlled ventilation for asleep-awake-asleep brain surgery: a prospective series of 140 gliomas in eloquent areas. Neurosurgery 71(4):764-471.Google Scholar
  15. 15.
    Duffau H (2001) Acute functional reorganisation of the human motor cortex during resection of central lesions : a study using intraoperative brain mapping acute functional reorganisation of the human motor cortex during resection of central lesions . A Study Intrao. doi: 10.1136/jnnp.70.4.506 Google Scholar
  16. 16.
    Duffau H (2013) A new philosophy in surgery for diffuse low-grade glioma (DLGG): oncological and functional outcomes. Neurochirurgie 59:2–8PubMedCrossRefGoogle Scholar
  17. 17.
    Duffau H (2014) The huge plastic potential of adult brain and the role of connectomics: new insights provided by serial mappings in glioma surgery. Cortex 58:325-337.Google Scholar
  18. 18.
    Duffau H, Capelle L, Denvil D et al (2003) Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg 98(4):764–778PubMedCrossRefGoogle Scholar
  19. 19.
    Duffau H, Herbet G, Moritz-Gasser S (2013) Toward a pluri-component, multimodal, and dynamic organization of the ventral semantic stream in humans: lessons from stimulation mapping in awake patients. Front Syst Neurosci 7:44PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Duffau H, Moritz-gasser S, Mandonnet E (2013) Brain & language a re-examination of neural basis of language processing : proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming. Brain Lang. doi: 10.1016/j.bandl.2013.05.011 PubMedGoogle Scholar
  21. 21.
    Duffau H, Moritz-Gasser S, Mandonnet E (2014) A re-examination of neural basis of language processing: proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming. Brain Lang 131:1–10PubMedCrossRefGoogle Scholar
  22. 22.
    Durante F (1887) Contribution to endocranial surgery. Lancet 130(3344):654–655CrossRefGoogle Scholar
  23. 23.
    Elsberg CA (1925) Craniotomy under local anaesthsia. Ann Surg 81(1):213–222PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Feindel W, Leblanc R, de Almeida AN (2009) Epilepsy surgery: historical highlights 1909–2009. Epilepsia 50(Suppl 3):131–151PubMedCrossRefGoogle Scholar
  25. 25.
    Ferrier D (1873) Experimental researches in cerebral physiology and pathology. J Anat Physiol 8(Pt 1):152–155PubMedCentralPubMedGoogle Scholar
  26. 26.
    Flourens P (1842) Recherches expérimentales sur les propriétés et les fonctions du système nerveux dans les animaux vertébrés. 516Google Scholar
  27. 27.
    Foerster O (1936) The motor cortex in man in the light of Hughlings Jackson’s doctrines. Brain 59(2):135–159CrossRefGoogle Scholar
  28. 28.
    Fritsch GT, Hitzig E (1870) Electric excitability of the cerebrum (Über die elektrische Erregbarkeit des Grosshirns). Arch fuer Anat Physiol und wissenschaftliche Med 37:300–332Google Scholar
  29. 29.
    Van Geemen K, Herbet G, Moritz-Gasser S, Duffau H (2014) Limited plastic potential of the left ventral premotor cortex in speech articulation: evidence from intraoperative awake mapping in glioma patients. Hum Brain Mapp 35(4):1587–1596PubMedCrossRefGoogle Scholar
  30. 30.
    Gibbs F, Lennox W, Gibbs E (1936) The electro-encephalogram in diagnosis and in localisation of epileptic seizures. Arch Neurol Psychiatry 36(6):1225–1235CrossRefGoogle Scholar
  31. 31.
    Gignac E, Manninen PH, Gelb AW, After M, Committee E, Ontario W, Road W (1993) Comparison of fentanyl, sufentanil and alfentanil during awake craniotomy for epilepsy. Can J Anaesth 40(February):421–424PubMedCrossRefGoogle Scholar
  32. 32.
    Gras-Combe G, Moritz-Gasser S, Herbet G, Duffau H (2012) Intraoperative subcortical electrical mapping of optic radiations in awake surgery for glioma involving visual pathways. J Neurosurg 117(3):466–473PubMedCrossRefGoogle Scholar
  33. 33.
    Hamer PCDW, Robles SG, Zwinderman AH, Duffau H, Berger MS (2012) Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol 30(20):2559–2565CrossRefGoogle Scholar
  34. 34.
    Hans P, Bonhomme V (2006) Why we still use intravenous drugs as the basic regimen for neurosurgical anaesthesia. Curr Opin Anaesthesiol 19:498–503PubMedCrossRefGoogle Scholar
  35. 35.
    Harlow JM (1869) Recovery from the passage of an iron bar through the head. Publ. Massachusetts Med. Soc. Clapp, Boston, pp 327–346Google Scholar
  36. 36.
    Herbet G, Lafargue G, Bonnetblanc F, Moritz-Gasser S, Menjot de Champfleur N, Duffau H (2014) Inferring a dual-stream model of mentalizing from associative white matter fibres disconnection. Brain 944–959Google Scholar
  37. 37.
    Herbet G, Lafargue G, Moritz-Gasser S, Bonnetblanc F, Duffau H (2014) Interfering with the neural activity of mirror-related frontal areas impairs mentalistic inferences. Brain Struct, FunctGoogle Scholar
  38. 38.
    Honey CJ, Kötter R, Breakspear M, Sporns O (2007) Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc Natl Acad Sci U S A 104(24):10240–10245PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Ius T, Angelini E, Thiebaut de Schotten M, Mandonnet E, Duffau H, Thiebaut M, Schotten D (2011) Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: towards a “minimal common brain”. Neuroimage 56(3):992–1000PubMedCrossRefGoogle Scholar
  40. 40.
    Loring DW (2010) History of neuropsychology through epilepsy eyes. Arch Clin Neuropsychol 25(4):259–273PubMedCentralPubMedCrossRefGoogle Scholar
  41. 41.
    Macewen W (1881) Intracranial lesions. Lancet 118(3031):581–583CrossRefGoogle Scholar
  42. 42.
    Maldonado IL, Moritz-Gasser S, Duffau H (2011) Does the left superior longitudinal fascicle subserve language semantics? A brain electrostimulation study. Brain Struct Funct 216(3):263–274PubMedCrossRefGoogle Scholar
  43. 43.
    Mandonnet E (2011) Intraoperative electrical mapping: advances, limitations and perspectives. In: Duffau H (ed) Brain Mapp. - From Neural Basis Cogn. to Surg. Appl. Springer, Vienna, pp 101–108Google Scholar
  44. 44.
    Manninen P, Contreras J (1986) Anesthetic considerations for craniotomy in awake patients. Int Anesthesiol Clin 24(3):157–174PubMedCrossRefGoogle Scholar
  45. 45.
    Marik PE (2004) Propofol: therapeutic indications and side-effects. Curr Pharm Des 10(29):3639–3649PubMedCrossRefGoogle Scholar
  46. 46.
    Matsuda R, Coello AF, De Benedictis A, Martinoni M, Duffau H (2012) Awake mapping for resection of cavernous angioma and surrounding gliosis in the left dominant hemisphere: surgical technique and functional results: clinical article. J Neurosurg 117(6):1076–1081PubMedCrossRefGoogle Scholar
  47. 47.
    Mikuni N, Ohara S, Ikeda A, Hayashi N, Nishida N, Taki J, Enatsu R, Matsumoto R, Shibasaki H, Hashimoto N (2006) Evidence for a wide distribution of negative motor areas in the perirolandic cortex. Clin Neurophysiol. 117(1):33-40.Google Scholar
  48. 48.
    Mitchell TJ, Hacker CD, Breshears JD et al (2013) A novel data-driven approach to preoperative mapping of functional cortex using resting-state functional magnetic resonance imaging. Neurosurgery 73(6):969–982, discussion 982–3PubMedCentralPubMedCrossRefGoogle Scholar
  49. 49.
    Molnár C, Nemes C, Szabó S, Fülesdi B, Care I (2008) Harvey Cushing, a pioneer of neuroanesthesia. J Anesth 22(4):483–486PubMedCrossRefGoogle Scholar
  50. 50.
    Moritz-Gasser S, Herbet G, Duffau H (2013) Mapping the connectivity underlying multimodal (verbal and non-verbal) semantic processing: a brain electrostimulation study. Neuropsychologia 51(10):1814–1822PubMedCrossRefGoogle Scholar
  51. 51.
    Niemeyer P (1958) The transventricular amygdala-hippocampectomy in temporal lobe epilepsy. In: Baldwin M, Bailey P (eds) Temporal Lobe Epilepsy. Charles Thomas, Springfield, MA, USA, pp 461–482Google Scholar
  52. 52.
    Olivier A, Boling WW, Tanriverdi T (2012) Anesthesia and awake procedure. In: Olivier A, et al (eds) Techniques in Epilepsy Surgery: The MNI Approach. Cambridge University Press New York, pp 75–78Google Scholar
  53. 53.
    Olsen KS (2008) The asleep-awake technique using propofol-remifentanil anaesthesia for awake craniotomy for cerebral tumours. Eur J Anaesthesiol 25:662–669PubMedCrossRefGoogle Scholar
  54. 54.
    Paper O, 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(2):74–82CrossRefGoogle Scholar
  55. 55.
    Penfield W (1954) Combined regional and general anesthesia for craniotomy and cortical exploration. I. Neurosurgical considerations. Curr Res Anesth Analg 33(3):145–155PubMedGoogle Scholar
  56. 56.
    Penfield W, Baldwin M (1952) Temporal lobe seizures and the technic of subtotal temporal lobectomy. Ann Surg 136(4):625–634PubMedCentralPubMedGoogle Scholar
  57. 57.
    Penfield W, Rasmussen T (1950) The cerebral cortex of man. A clinical study of localization of function. New YorkGoogle Scholar
  58. 58.
    Piccioni F, Fanzio M (2008) Management of anesthesia in awake craniotomy. Minerva Anestesiol 74(7–8):393–408PubMedGoogle Scholar
  59. 59.
    Dos Reis A Sigmund Freud (1856-1939) and Karl Köller (1857-1944) and the discovery of local anesthesia. Rev Bras Anestesiol 59(2):244–57Google Scholar
  60. 60.
    Rolando L (1823) Expériences sur les fonctions du système nerveux. J Physiol expér path 3:95–113Google Scholar
  61. 61.
    Rowbotham ES, Magill I (1921) Anaesthetics in the plastic surgery of the face and jaws. Proc R Soc Med 14(Sect Anaesth):17–27PubMedCentralGoogle Scholar
  62. 62.
    Samuels SI (1996) History of neuroanesthesia: a contemporary review. Int Anesthesiol Clin 34(4):1–20PubMedCrossRefGoogle Scholar
  63. 63.
    Sanai N, Berger MS (2008) Glioma extent of resection and its impact on patient outcome. Neurosurgery 62(4):753–766PubMedCrossRefGoogle Scholar
  64. 64.
    Schmahmann JD, Pandya DN (2007) Cerebral white matter--historical evolution of facts and notions concerning the organization of the fiber pathways of the brain. J Hist Neurosci. 16(3):237-267.Google Scholar
  65. 65.
    Schucht P, Moritz-gasser S, Herbet G, Raabe A, Duffau H (2013) Subcortical Electrostimulation to Identify Network Subserving Motor Control. 3030:3023–3030Google Scholar
  66. 66.
    Sills AK (2005) Current treatment approaches to surgery for brain metastases. Neurosurgery 57(5 Supp):S24–S32, discussion S1–4PubMedGoogle Scholar
  67. 67.
    Sporns O (2011) The human connectome: a complex network. Ann N Y Acad Sci 1224:109–125PubMedCrossRefGoogle Scholar
  68. 68.
    Sykes W (1960) Essays on the First Hundred Years of Anaesthesia. Surv Anesthesiol 4(6):595–597CrossRefGoogle Scholar
  69. 69.
    Thiebaut de Schotten M, Urbanski M, Duffau H, Volle E, Lévy R, Dubois B, Bartolomeo P (2005) Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 30;309(5744):2226-2228.Google Scholar
  70. 70.
    Wawersik J (1997) History of chloroform anesthesia. Anaesthesiol Reanim 22(6):144–152PubMedGoogle Scholar
  71. 71.
    Wicker P (1994) Local anaesthesia in the operating theatre. Nurs Times 90(46):34–35PubMedGoogle Scholar
  72. 72.
    Wilkinson E (1987) History of neuroanesthesia. BNI Q 3(2):27–36PubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  • Werner Surbeck
    • 1
    • 4
    Email author
  • Gerhard Hildebrandt
    • 1
  • Hugues Duffau
    • 2
    • 3
  1. 1.Department of Neurosurgery Cantonal Hospital of St. GallGallSwitzerland
  2. 2.Department of Neurosurgery, Gui-de-Chauliac HospitalMontpellierFrance
  3. 3.Institute of Neuroscience of Montpellier, INSERM U1051, Team “Plasticity of Central Nervous SystemHuman Stem Cells and Glial Tumors,” Saint Eloi HospitalMontpellierFrance
  4. 4.Department of Neurosurgery, Cantonal Hospital of St. GallSt. GallSwitzerland

Personalised recommendations