Skip to main content

Advertisement

Log in

The persistent crucial role of the left hemisphere for language in left-handers with a left low grade glioma: a stimulation mapping study

  • Clinical Article - Brain Tumors
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

Left-handers have a more bilateral language representation than right-handers. Therefore, in left-handers with a low-grade glioma (LGG) in the left hemisphere (LH), one could hypothesize that the right hemisphere (RH) might allow language compensation, at least partly, with no or only a minor persistent role of the LH in speech. However, although LGG induces language reorganization in right-handed patients, little is known in left-handers. Here, we report the first series of left-handers who underwent awake surgery for a left LGG using intraoperative mapping, in order to investigate whether there was still an involvement of LH in language.

Method

Ten consecutive left-handed patients were operated for a left LGG (three frontal, four paralimbic, one parietal, one temporal, one parieto-temporal tumor) using an awake procedure with intraoperative electrical language mapping.

Results

Intraoperative language disorders were elicited in all cases but one by electrostimulation in the LH. Cortical language sites were detected in nine cases. Subcortical stimulation also demonstrated the crucial role of left white matter pathways in language, including the inferior occipital-frontal fascicle, arcuate fascicle, lateral segment of the superior longitudinal fascicle and fibers from the ventral premotor cortex. Moreover, stimulation of deep gray nuclei generated language disturbances in four patients. These nine patients experienced transient postoperative language worsening, supporting the persistent critical role of LH in speech. In only one patient, no language deficit was evoked intraoperatively and postoperatively. The ten patients returned to a normal life. Total or subtotal resection was achieved in all cases but one.

Conclusions

Our results suggest that, even though the RH may participate in language compensation, the LH in left-handers still plays a crucial role, despite a left slow-growing LGG. Thus, we propose to routinely consider awake surgery for left LGG removal in left-handers patients, to optimize the extent of resection while preserving language.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Berger MS, Deliganis AV, Dobbins J, Keles GE (1994) The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas. Cancer 74:1784–1791

    Article  CAS  PubMed  Google Scholar 

  2. Broca P (1861) Remarques sur le siège de la faculté du langage articulé, suivies d’une observation d’aphémie (perte de la parole). Bull Soc Anat 36:330–357

    Google Scholar 

  3. Capelle L, Fontaine D, Mandonnet E, Taillandier L, Golmard JL, Bauchet L, Pallud J, Peruzzi P, Baron MH, Kujas M, Guyotat J, Guillevin R, Frenay M, Taillibert S, Colin P, Rigau V, Vandenbos F, Pinelli C, Duffau H (2013) Spontaneous and therapeutic prognostic factors in adult hemispheric World Health Organization Grade II gliomas: a series of 1097 cases. J Neurosurg 118:1157–1168

    Article  PubMed  Google Scholar 

  4. Chang EF, Wang DD, Perry DW, Barbaro NM, Berger MS (2011) Homotopic organization of essential language sites in right and bilateral cerebral hemispheric dominance. J Neurosurg 114:893–902

    Article  PubMed  Google Scholar 

  5. Coello AF, Moritz-Gasser S, Martino J, Martinoni M, Matsuda R, Duffau H (2013) Selection of intraoperative tasks for awake mapping based on relationships between tumor location and functional networks. J Neurosurg. PMID 24053503

  6. De Benedictis A, Moritz-Gasser S, Duffau H (2010) Awake mapping optimizes the extent of resection for low-grade gliomas in eloquent areas. Neurosurgery 66:1074–1084

    Article  PubMed  Google Scholar 

  7. Desmurget M, Bonnetblanc F, Duffau H (2007) Contrasting acute and slow growing lesions: a new door to brain plasticity. Brain 130:898–914

    Article  PubMed  Google Scholar 

  8. De Witt Hamer PC, 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 30:2559–2565

    Article  PubMed  Google Scholar 

  9. Duffau H (2005) Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol 4:476–486

    Article  PubMed  Google Scholar 

  10. Duffau H (2008) The anatomo-functional connectivity of language revisited: new insights provided by electrostimulation and tractography. Neuropsychologia 46:927–934

    Article  PubMed  Google Scholar 

  11. Duffau H (2008) Brain plasticity and tumors. Adv Tech Stand Neurosurg 3:3–33

    Article  Google Scholar 

  12. Duffau H (2011) Brain mapping: from neural basis of cognition to surgical applications. Duffau H (ed) Springer, Wien New York

  13. Duffau H (2012) The “frontal syndrome” revisited: lessons from electrostimulation mapping studies. Cortex 48:120–131

    Article  PubMed  Google Scholar 

  14. Duffau H (2012) A new concept of diffuse (low-grade) glioma surgery. Adv Tech Stand Neurosurg 38:3–272

    CAS  PubMed  Google Scholar 

  15. Duffau H (2013) Diffuse Low-Grade Gliomas in Adults: Natural History, Interaction with the Brain, and New Individualized Therapeutic Strategies. Duffau H (Ed.). Springer London

  16. Duffau H (2013) The huge plastic potential of adult brain and the role of connectomics: new insights provided by serial mappings in glioma surgery. Cortex PMID 24050218

  17. Duffau H, Capelle L, Denvil D, Gatignol P, Sichez N, Lopes M, Sichez JP, van Effenterre R (2003) The role of dominant premotor cortex in language: a study using intraoperative functional mapping in awake patients. NeuroImage 20:1903–1914

    Article  PubMed  Google Scholar 

  18. Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP, Fohanno D (2002) Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 125:199–214

    Article  PubMed  Google Scholar 

  19. Duffau H, Gatignol P, Denvil D, Lopes M, Capelle L (2003) The articulatory loop: study of the subcortical connectivity by electrostimulation. Neuroreport 14:2005–2008

    Article  PubMed  Google Scholar 

  20. Duffau H, Gatignol P, Mandonnet E, Capelle L, Taillandier L (2008) Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. J Neurosurg 109:461–471

    Article  PubMed  Google Scholar 

  21. Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N, Capelle L (2005) New insights into the anatomo-functional connectivity of the semantic system: a study using corticosubcortical electrostimulations. Brain 128:797–810

    Article  PubMed  Google Scholar 

  22. Duffau H, Gatignol P, Moritz-Gasser S, Mandonnet E (2009) Is the left uncinate fasciculus essential for language? A cerebral stimulation study. J Neurol 256:382–389

    Article  PubMed  Google Scholar 

  23. 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 7:44

    Article  PubMed Central  PubMed  Google Scholar 

  24. Duffau H, Leroy M, Gatignol P (2008) Cortico-subcortical organization of language networks in the right hemisphere : An electrostimulation study in left-handers. Neuropsychologia 46:3197–3209

    Article  PubMed  Google Scholar 

  25. Duffau H, Lopes M, Arthuis F, Bitar A, Sichez JP, van Effenterre R, Capelle L (2005) Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: a comparative study between two series without (1985–96) and with (1996–2003) functional mapping in the same institution. J Neurol Neurosurg Psychiatry 76:845–851

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Duffau H, Moritz-Gasser S, Mandonnet E (2013) 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 PMID 23866901

  27. Faurie C, Schiefenhovel W, Le Bomin S, Billiard S, Raymond M (2005) Variation in the frequency of lefthandedness in traditional societies. Curr Anthropol 46:142–147

    Article  Google Scholar 

  28. Geschwind N (1970) The organization of language and the brain. Science 170:940–944

    Article  CAS  PubMed  Google Scholar 

  29. Gil Robles S, Duffau H (2010) Surgical management of World Health Organization Grade II gliomas in eloquent areas: the necessity of preserving a margin around functional structures? Neurosurg Focus 28(2):E8

    Article  PubMed  Google Scholar 

  30. Gil Robles S, Gatignol P, Capelle L, Mitchell MC, Duffau H (2005) The role of dominant striatum in language: a study using intraoperative electrical stimulations. J Neurol Neurosurg Psychiatry 76:940–946

    Article  CAS  PubMed  Google Scholar 

  31. Haecan H, De Agostini M, Monzon-Montes A (1981) Cerebral organization in left-handers. Brain Lang 12:261–284

    Article  Google Scholar 

  32. Haecan H, Sauguet J (1971) Cerebral dominance in left handers. Cortex 7:19–48

    Article  Google Scholar 

  33. Jakola AS, Myrmel KS, Kloster R, Torp SH, Lindal S, Unsgard G, Solheim O (2012) Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas. JAMA 308:1881–1888

    Article  CAS  PubMed  Google Scholar 

  34. Karnofsky DA, Burchenal JH (1949) The clinical evaluation of chemotherapeutic agents in cancer. In: MacLeod CM (ed) Evaluation of Chemotherapeutic Agents. Columbia University Press, New York, pp 191–205

    Google Scholar 

  35. Loddenkemper T, Dinner D, Kubu C, Prayson R, Bingaman W, Dagirmanjian A, Wyllie E (2004) Aphasia after hemispherectomy in an adult with early onset epilepsy and hemiplegia. J Neurol Neurosurg Psychiatry 75:149–151

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Maldonado IL, Moritz-Gasser S, Champfleur NM, Bertram L, Moulinie G, Duffau H (2011) Surgery for gliomas involving the left inferior parietal lobule: new insights into the functional anatomy provided by stimulation mapping in awake patients. J Neurosurg 115:770–779

    Article  PubMed  Google Scholar 

  37. Maldonado IL, Moritz-Gasser S (2011) Duffau H (2011) Does the left superior longitudinal fascicle subserve language semantics? A brain electrostimulation study. Brain Struct Funct 216:263–264

    Article  PubMed  Google Scholar 

  38. Mandonnet E, Nouet A, Gatignol P, Capelle L (2007) Duffau H (2007) Does the left inferior longitudinal fasciculus play a role in language? A brain stimulation study. Brain 130:623–629

    Article  PubMed  Google Scholar 

  39. Metz-Lutz M, Kremin H (1991) Deloche G (1991) Standardisation d’un test de dénomination orale. Contrôle des effets de l’âge, du sexe et du niveau de scolarité chez les sujets adultes normaux. Rev Neuropsychol 1:73–95

    Google Scholar 

  40. Moritz-Gasser S, Herbet G, Duffau H (2013) Mapping the connectivity underlying multimodal (verbal and non-verbal) semantic processing: A brain electrostimulation study. Neuropsychologia 51:1814–1822

    Article  PubMed  Google Scholar 

  41. Ojemann G, Ojemann J, Lettich E (1989) Berger MS (1989) Cortical language localization in left, dominant hemisphere. J Neurosurg 71:316–326

    Article  CAS  PubMed  Google Scholar 

  42. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  43. Pujol J, Deus J, Losilla J, Capdevila A (1999) Cerebral lateralization of language in normal left-handed people studied by functional MRI. Neurology 52:1038–1043

    Article  CAS  PubMed  Google Scholar 

  44. Rasmussen T, Milner B (1977) The role of early left-brain injury in determining lateralization of cerebral speech functions. Ann N Y Acad Sci 299:355–369

    Article  CAS  PubMed  Google Scholar 

  45. Sabbah P, Chassoux F, Leveque C, Landre E, Baudoin-chial S, Devaux B, Mann M, Godon-Hardy S, Nioche C, Aït-Ameur A, Sarrazin JL, Chodkiewicz JP, Cordoliani YS (2003) Functional MR imaging in assessment of language dominance in epileptic patients. NeuroImage 18:460–467

    Article  CAS  PubMed  Google Scholar 

  46. Sanai N, Mirzadeh Z, Berger MS (2008) Functional outcome after language mapping for glioma Resection. N Engl J Med 358:18–27

    Article  CAS  PubMed  Google Scholar 

  47. Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, Tihan T, Vandenberg S, McDermott MW, Berger MS (2008) Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26:1338–1345

    Article  PubMed  Google Scholar 

  48. Soffietti R, Baumert BG, Bello L, von Deimling A, Duffau H, Frenay M, Grisold W, Grant R, Graus F, Hoang-Xuan K, Klein M, Melin B, Rees J, Siegal T, Smits A, Stupp R, Wick W (2010) Guidelines on management of low-grade gliomas: report of an EFNS-EANO Task Force. Eur J Neurol 17:1124–1133

    Article  CAS  PubMed  Google Scholar 

  49. Szaflarski J, Binder J, Possing E, McKiernan K, Ward B, Hammeke T (2002) Language lateralization in left-handed and ambidextrous people: fMRI data. Neurology 59:238–244

    Article  CAS  PubMed  Google Scholar 

  50. Thiel A, Habedank B, Winhuisen L, Herholz K, Kessler J, Haupt WF (2005) Essential Language Function of the Right Hemisphere in Brain Tumor Patients. Ann Neurol 57:128–131

    Article  PubMed  Google Scholar 

  51. Ulmer JL, Krouwer HG, Mueller WM, Ugurel MS, Kocak M, Mark LP (2003) Pseudo-reorganization of language cortical function at fMR imaging : A consequence of tumor-induced neurovascular uncoupling. Am J Neuroradiol 24:213–217

    PubMed  Google Scholar 

  52. Wernicke C (1874) Der aphasische Symptomenkomplex: eine psychologische Studie auf anatomischer Basis. Max Cohn and Weigert, Breslau

    Google Scholar 

  53. Winhuisen L, Thiel A, Schumacher B, Kessler J, Rudolf J, Walter F, Heiss WD (2007) The right inferior frontal gyrus and poststroke aphasia: A follow-up investigation. Stroke 38:1286–1292

    Article  PubMed  Google Scholar 

  54. van Geemen K, Herbet G, Moritz-Gasser S, Duffau H (2013) Limited plastic potential of the left ventral premotor cortex in speech articulation: Evidence From intraoperative awake mapping in glioma patients. Hum Brain Mapp. doi:10.1002/hbm.22275

    PubMed  Google Scholar 

Download references

Conflict of Interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hugues Duffau.

Additional information

Comment

This is a well written retrospective report stressing the need of language mapping in patients with left hemisphere tumours even if they are left handed. The idea behind the report is very attractive, with a shift from a localizationistic view to a connectionistic approach: language function is not located at the right or left hemisphere, rather both hemispheres work together and the left hemisphere has still an important function even in left handers or after functional plastic rearrangement.

However, nothing is known about the language distribution between both hemispheres, or about the laterality index in these patients, because fMRI or Wada's tests were not used. The clinical uselessness of these tests is justified by the authors because intraoperative electrical stimulation is a far superior tool to detect language function. However, as the authors note, most left handers (70-78%) have a left dominant hemisphere. So it is likely that these nine patients out of ten with language function detected with intraoperative stimulation at the left hemisphere have had activation in the fMRI at the left side or a positive Wada test for language at the left hemisphere.

The series of the authors is impressive and ten left handers with left LGG may be difficult to collect. Still, it is not possible to generalize about the structure of language function with only those cases and no other functional imaging studies.

Juan A. Barcia

Madrid, Spain

Rights and permissions

Reprints and permissions

About this article

Cite this article

Matsuda, R., Moritz-Gasser, S., Duvaux, S. et al. The persistent crucial role of the left hemisphere for language in left-handers with a left low grade glioma: a stimulation mapping study. Acta Neurochir 156, 661–670 (2014). https://doi.org/10.1007/s00701-014-2003-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-014-2003-2

Keywords

Navigation