Skip to main content

Advertisement

Log in

Post-Surgical Language Reorganization Occurs in Tumors of the Dominant and Non-Dominant Hemisphere

  • Original Article
  • Published:
Clinical Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

Surgical resection of brain tumors may shift the location of cortical language areas. Studies of language reorganization primarily investigated left-hemispheric tumors irrespective of hemispheric language dominance. We used functional magnetic resonance imaging (fMRI) to investigate how tumors influence post-surgical language reorganization in relation to the dominant language areas.

Methods

A total of, 17 patients with brain tumors (16 gliomas, one metastasis) in the frontotemporal and lower parietal lobes planned for awake surgery underwent pre-surgical and post-surgical language fMRI. Language activation post-to-pre surgery was evaluated visually and quantitatively on the statistically thresholded images on patient-by-patient basis. Results were qualitatively compared between three patient groups: temporal, with tumors in the dominant temporal lobe, frontal, with tumors in the dominant frontal lobe and remote, with tumors in the non-dominant hemisphere.

Results

Post-to-pre-surgical distributions of activated voxels changed in all except the one patient with metastasis. Changes were more pronounced in the dominant hemisphere for all three groups, showing increased number of activated voxels and also new activation areas. Tumor resection in the dominant hemisphere (frontal and temporal) shifted the activation from frontal towards temporal, whereas tumor resection in the non-dominant hemisphere shifted the activation from temporal towards frontal dominant areas.

Conclusion

Resection of gliomas in the dominant and in the non-dominant hemisphere induces postsurgical shifts and increase in language activation, indicating that infiltrating gliomas have a widespread influence on the language network. The dominant hemisphere gained most of the language activation irrespective of tumor localization, possibly reflecting recovery of pre-surgical tumor-induced suppression of these activations.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Stippich C, Rapps N, Dreyhaupt J, Durst A, Kress B, Nennig E, Tronnier VM, Sartor K. Localizing and lateralizing language in patients with brain tumors: feasibility of routine preoperative functional MR imaging in 81 consecutive patients. Radiology. 2007;243:828–36.

    Article  PubMed  Google Scholar 

  2. Pillai JJ, Zaca D. Relative utility for hemispheric lateralization of different clinical fMRI activation tasks within a comprehensive language paradigm battery in brain tumor patients as assessed by both threshold-dependent and threshold-independent analysis methods. Neuroimage. 2011;54(Suppl 1):S136–45.

    Article  PubMed  Google Scholar 

  3. Perrone-Bertolotti M, Zoubrinetzky R, Yvert G, Le Bas JF, Baciu M. Functional MRI and neuropsychological evidence for language plasticity before and after surgery in one patient with left temporal lobe epilepsy. Epilepsy Behav. 2012;23:81–6.

    Article  CAS  PubMed  Google Scholar 

  4. Hamberger MJ, Cole J. Language organization and reorganization in epilepsy. Neuropsychol Rev. 2011;21:240–51.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Elkana O, Frost R, Kramer U, Ben-Bashat D, Schweiger A. Cerebral language reorganization in the chronic stage of recovery: a longitudinal fMRI study. Cortex. 2013;49:71–81.

    Article  PubMed  Google Scholar 

  6. Saur D, Lange R, Lange R, Baumgaertner A, Schraknepper V, Willmes K, Rijntjes M, Weiller C. Dynamics of language reorganization after stroke. Brain. 2006;129:1371–84.

    Article  PubMed  Google Scholar 

  7. Pillai JJ. Insights into adult postlesional language cortical plasticity provided by cerebral blood oxygen level-dependent functional MR imaging. AJNR Am J Neuroradiol. 2010;31:990–6.

    Article  CAS  PubMed  Google Scholar 

  8. Rosenberg K, Liebling R, Avidan G, Perry D, Siman-Tov T, Andelman F, Ram Z, Fried I, Hendler T. Language related reorganization in adult brain with slow growing glioma: fMRI prospective case-study. Neurocase. 2008;14:465–73.

    Article  PubMed  Google Scholar 

  9. Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Lopes M, Mitchell MC, Sichez JP, Van Effenterre R. Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry. 2003;74:901–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  11. Duffau H, Sichez JP, Lehéricy S. Intraoperative unmasking of brain redundant motor sites during resection of a precentral angioma: evidence using direct cortical stimulation. Ann Neurol. 2000;47:132–5.

    Article  CAS  PubMed  Google Scholar 

  12. Robles SG, Gatignol P, Lehéricy S, Duffau H. Long-term brain plasticity allowing a multistage surgical approach to World Health Organization Grade II gliomas in eloquent areas. J Neurosurg. 2008;109:615–24.

    Article  PubMed  Google Scholar 

  13. Spreer J, Arnold S, Quiske A, Wohlfarth R, Ziyeh S, Altenmüller D, Herpers M, Kassubek J, Klisch J, Steinhoff BJ, Honegger J, Schulze-Bonhage A, Schumacher M. Determination of hemisphere dominance for language: comparison of frontal and temporal fMRI activation with intracarotid amytal testing. Neuroradiology. 2002;44:467–74.

    Article  CAS  PubMed  Google Scholar 

  14. Spreer J, Ziyeh S, Wohlfahrt R, Hammen A, Schreiber A, Hubbe U, Schmider K, Schumacher M. Vergleich verschiedener Paradigmen für die fMRT zur Bestimmung der Hemisphärendominanz für sprachliche Funktionen. Klin Neuroradiol. 1998;8:173–81.

    Article  Google Scholar 

  15. Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM. FSL. Neuroimage. 2012;62:782–90.

    Article  PubMed  Google Scholar 

  16. Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17:825–41.

    Article  PubMed  Google Scholar 

  17. Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17:143–55.

    Article  PubMed  Google Scholar 

  18. Woolrich MW, Ripley BD, Brady M, Smith SM. Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage. 2001;14:1370–86.

    Article  CAS  PubMed  Google Scholar 

  19. Abbott DF, Waites AB, Lillywhite LM, Jackson GD. fMRI assessment of language lateralization: an objective approach. Neuroimage. 2010;50:1446–55.

    Article  PubMed  Google Scholar 

  20. Jansen A, Menke R, Sommer J, Förster AF, Bruchmann S, Hempleman J, Weber B, Knecht S. The assessment of hemispheric lateralization in functional MRI–robustness and reproducibility. Neuroimage. 2006;33:204–17.

    Article  CAS  PubMed  Google Scholar 

  21. Knecht S, Jansen A, Frank A, van Randenborgh J, Sommer J, Kanowski M, Heinze HJ. How atypical is atypical language dominance? Neuroimage. 2003;18:917–27.

    Article  CAS  PubMed  Google Scholar 

  22. Specht K, Willmes K, Shah NJ, Jäncke L. Assessment of reliability in functional imaging studies. J Magn Reson Imaging. 2003;17:463–71.

    Article  PubMed  Google Scholar 

  23. Baciu MV, Watson JM, Maccotta L, McDermott KB, Buckner RL, Gilliam FG, Ojemann JG. Evaluating functional MRI procedures for assessing hemispheric language dominance in neurosurgical patients. Neuroradiology. 2005;47:835–44.

    Article  CAS  PubMed  Google Scholar 

  24. Ojemann GA. Individual variability in cortical localization of language. J Neurosurg. 1979;50:164–9.

    Article  CAS  PubMed  Google Scholar 

  25. Corina DP, Loudermilk BC, Detwiler L, Martin RF, Brinkley JF, Ojemann G. Analysis of naming errors during cortical stimulation mapping: implications for models of language representation. Brain Lang. 2010;115:101–12.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Szelényi A, Bello L, Duffau H, Fava E, Feigl GC, Galanda M, Neuloh G, Signorelli F, Sala F. Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus. 2010;28:E7.

    Article  PubMed  Google Scholar 

  27. Huber W, Weniger D, Poeck K, Willmes K. The Aachen Aphasia Test Rationale and construct validity (author’s transl). Nervenarzt. 1980;51:475–82.

    CAS  PubMed  Google Scholar 

  28. Wang L, Chen D, Yang X, Olson JJ, Gopinath K, Fan T, Mao H. Group independent component analysis and functional MRI examination of changes in language areas associated with brain tumors at different locations. PLoS One. 2013;8:e59657.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Kundu B, Penwarden A, Wood JM, Gallagher TA, Andreoli MJ, Voss J, Meier T, Nair VA, Kuo JS, Field AS, Moritz C, Meyerand ME, Prabhakaran V. Association of functional magnetic resonance imaging indices with postoperative language outcomes in patients with primary brain tumors. Neurosurg Focus. 2013;34:E6.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Partovi S, Jacobi B, Rapps N, Zipp L, Karimi S, Rengier F, Lyo JK, Stippich C. Clinical standardized fMRI reveals altered language lateralization in patients with brain tumor. AJNR Am J Neuroradiol. 2012;33:2151–7.

    Article  CAS  PubMed  Google Scholar 

  31. Thiel A, Herholz K, Koyuncu A, Ghaemi M, Kracht LW, Habedank B, Heiss WD. Plasticity of language networks in patients with brain tumors: a positron emission tomography activation study. Ann Neurol. 2001;50:620–9.

    Article  CAS  PubMed  Google Scholar 

  32. Giese A, Kluwe L, Laube B, Meissner H, Berens ME, Westphal M. Migration of human glioma cells on myelin. Neurosurgery. 1996;38:755–64.

    Article  CAS  PubMed  Google Scholar 

  33. Kallenberg K, Goldmann T, Menke J, Strik H, Bock HC, Stockhammer F, Buhk JH, Frahm J, Dechent P, Knauth M. Glioma infiltration of the corpus callosum: early signs detected by DTI. J Neurooncol. 2013;112:217–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ulmer JL, Hacein-Bey L, Mathews VP, Mueller WM, DeYoe EA, Prost RW, Meyer GA, Krouwer HG, Schmainda KM. Lesion-induced pseudo-dominance at functional magnetic resonance imaging: implications for preoperative assessments. Neurosurgery. 2004;55:569–79. (discussion 580–1).

    Article  PubMed  Google Scholar 

  35. Kell CA, Morillon B, Kouneiher F, Giraud A. Lateralization of speech production starts in sensory cortices–a possible sensory origin of cerebral left dominance for speech. Cereb Cortex. 2011;21:932–7.

    Article  PubMed  Google Scholar 

  36. Gould RL, Arroyo B, Brown RG, Owen AM, Bullmore ET, Howard RJ. Brain mechanisms of successful compensation during learning in Alzheimer disease. Neurology. 2006;67:1011–7.

    Article  CAS  PubMed  Google Scholar 

  37. Nelissen N, Dupont P, Vandenbulcke M, Tousseyn T, Peeters R, Vandenberghe R. Right hemisphere recruitment during language processing in frontotemporal lobar degeneration and Alzheimer’s disease. J Mol Neurosci. 2011;45:637–47.

    Article  CAS  PubMed  Google Scholar 

  38. Mahdavi A, Houshmand S, Oghabian MA, Zarei M, Mahdavi A, Shoar MH, Ghanaati H. Developing optimized fMRI protocol for clinical use: comparison of different language paradigms. J Magn Reson Imaging. 2011;34:413–9.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank our patients and their families for their cooperation.

Funding

None.

Previous Full/Part Presentation of Data

None.

Conflict of Interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Jurcoane.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Avramescu-Murphy, M., Hattingen, E., Forster, MT. et al. Post-Surgical Language Reorganization Occurs in Tumors of the Dominant and Non-Dominant Hemisphere. Clin Neuroradiol 27, 299–309 (2017). https://doi.org/10.1007/s00062-015-0496-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00062-015-0496-6

Keywords

Navigation