Skip to main content
SpringerLink
Log in

The effect of different brain lesions on the reorganization of language functions within the dominant hemisphere assessed with task-based BOLD-fMRI

  • Magnetic Resonance Imaging
  • Published:
La radiologia medica Aims and scope Submit manuscript

Abstract

Background and purpose

Language reorganization has been described in brain lesions with respect to their location and timing, but little is known with respect to their etiology. We used fMRI to investigate the effects of different types of left hemisphere lesions (GL = gliomas, TLE = temporal lobe epilepsy and CA = cavernous angioma) on the topographic intra-hemispheric language plasticity, also considering their location.

Methods

Forty-seven right-handed patients with 3 different left hemisphere lesions (16 GL, 15 TLE and 16 CA) and 17 healthy controls underwent BOLD fMRI with a verb-generation task. Euclidean distance was used to measure activation peak shifts among groups with respect to reference Tailarach coordinates of Inferior Frontal Gyrus, Superior Temporal Sulcus and Temporo-Parietal Junction. Mixed-model ANOVAs were used to test for differences in activation peak shifts.

Results

Significant activation peak shifts were found in GL patients with respect both to HC and other groups (TLA and CA). In addition, in the same group of patients a significant effect of tumor location (anterior or posterior) was detected.

Conclusions

We demonstrated that intra-hemispheric language plasticity is influenced by the type of lesion affecting the left hemisphere and that fMRI is especially valuable in the preoperative assessment of such reorganization in glioma patients.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ANT-GL:

Anterior gliomas

CA:

Cavernous angioma

GL:

Glioma

HC:

Healthy controls

IFG:

Inferior frontal gyrus

POST-GL:

Posterior gliomas

STS:

Superior temporal gyrus

TLE:

Temporal lobe epilepsy

TPJ:

Temporo-parietal junction

References

  1. Ojemann GA (1979) Individual variability in cortical localization of language. J Neurosurg 50(2):164–169

    Article  CAS  PubMed  Google Scholar 

  2. Duffau H (2006) Brain plasticity: from pathophysiological mechanisms to therapeutic applications. J Clin Neurosci 13(9):885–897

    Article  PubMed  Google Scholar 

  3. Devinsky O, Perrine K, Hirsch J, McMullen W, Pacia S, Doyle W (2000) Relation of cortical language distribution and cognitive function in surgical epilepsy patients. Epilepsia 41(4):400–404

    Article  CAS  PubMed  Google Scholar 

  4. Thiel A, Habedank B, Herholz K, Kessler J, Winhuisen L, Haupt WF, Heiss W-D (2006) From the left to the right: how the brain compensates progressive loss of language function. Brain Lang 98(1):57–65

    Article  PubMed  Google Scholar 

  5. Baciu MV, Watson J, McDermott K, Wetzel R, Attarian H, Moran C, Ojemann J (2003) Functional MRI reveals an interhemispheric dissociation of frontal and temporal language regions in a patient with focal epilepsy. Epilepsy Behav 4(6):776–780

    Article  CAS  PubMed  Google Scholar 

  6. Nieberlein L, Rampp S, Gussew A, Prell J, Hartwigsen G (2023) Reorganization and plasticity of the language network in patients with cerebral gliomas. Neuroimage Clin 37:103326. https://doi.org/10.1016/j.nicl.2023.103326

    Article  PubMed  PubMed Central  Google Scholar 

  7. Duffau H (2014) Diffuse low-grade gliomas and neuroplasticity. Diagn Interv Imaging 95(10):945–955

    Article  CAS  PubMed  Google Scholar 

  8. Pasquini L, Peck KK, Tao A, Del Ferraro G, Correa DD, Jenabi M, Kobylarz E, Zhang Z, Brennan C, Tabar V (2023) Longitudinal evaluation of brain plasticity in low-grade gliomas: fMRI and graph-theory provide insights on language reorganization. Cancers 15(3):836

    Article  PubMed  PubMed Central  Google Scholar 

  9. Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Lopes M, Mitchell M, Sichez J, Van Effenterre R (2003) Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry 74(7):901–907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Cargnelutti E, Ius T, Skrap M, Tomasino B (2020) What do we know about pre-and postoperative plasticity in patients with glioma? A review of neuroimaging and intraoperative mapping studies. Neuroimage: Clin 28:102435

    Article  PubMed  Google Scholar 

  11. Jeon JS, Kim JE, Chung YS, Oh S, Ahn JH, Cho W-S, Son Y-J, Bang JS, Kang H-S, Sohn C-H (2014) A risk factor analysis of prospective symptomatic haemorrhage in adult patients with cerebral cavernous malformation. J Neurol Neurosurg Psychiatry 85(12):1366–1370

    Article  PubMed  Google Scholar 

  12. Maestú F, Saldaña C, Amo C, González-Hidalgo M, Fernandez A, Fernandez S, Mata P, Papanicolaou A, Ortiz T (2004) Can small lesions induce language reorganization as large lesions do? Brain Lang 89(3):433–438

    Article  PubMed  Google Scholar 

  13. Li G-Z, Yang J, Ye C-Z, Geng D-Y (2006) Degree prediction of malignancy in brain glioma using support vector machines. Comput Biol Med 36(3):313–325

    Article  CAS  PubMed  Google Scholar 

  14. Talairach J (1988) 3-dimensional proportional system; an approach to cerebral imaging. co-planar stereotaxic atlas of the human brain. Thieme:1–122

  15. Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RS (1994) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2(4):189–210

    Article  Google Scholar 

  16. Boynton GM, Engel SA, Glover GH, Heeger DJ (1996) Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci 16(13):4207–4221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Seghier ML, Lazeyras F, Pegna AJ, Annoni JM, Zimine I, Mayer E, Michel CM, Khateb A (2004) Variability of fMRI activation during a phonological and semantic language task in healthy subjects. Hum Brain Mapp 23(3):140–155

    Article  PubMed  PubMed Central  Google Scholar 

  18. Desmurget M, Bonnetblanc F, Duffau H (2007) Contrasting acute and slow-growing lesions: a new door to brain plasticity. Brain 130(4):898–914

    Article  PubMed  Google Scholar 

  19. Liégeois F, Connelly A, Cross JH, Boyd SG, Gadian D, Vargha-Khadem F, Baldeweg T (2004) Language reorganization in children with early-onset lesions of the left hemisphere: an fMRI study. Brain 127(6):1229–1236

    Article  PubMed  Google Scholar 

  20. Cirillo S, Caulo M, Pieri V, Falini A, Castellano A (2019) Role of functional imaging techniques to assess motor and language cortical plasticity in glioma patients: a systematic review. Neural Plast. https://doi.org/10.1155/2019/4056436

    Article  PubMed  PubMed Central  Google Scholar 

  21. Briganti C, Sestieri C, Mattei P, Esposito R, Galzio R, Tartaro A, Romani G, Caulo M (2012) Reorganization of functional connectivity of the language network in patients with brain gliomas. Am J Neuroradiol 33(10):1983–1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Meyer PT, Sturz L, Schreckenberger M, Spetzger U, Meyer GF, Setani KS, Sabri O, Buell U (2003) Preoperative mapping of cortical language areas in adult brain tumour patients using PET and individual non-normalised SPM analyses. Eur J Nucl Med Mol Imag 30(7):951–960

    Article  Google Scholar 

  23. Duffau H, Sichez JP, Lehericy S (2000) Intraoperative unmasking of brain redundant motor sites during resection of a precentral angioma: evidence using direct cortical stimulation. Ann Neurol 47(1):132–135

    Article  CAS  PubMed  Google Scholar 

  24. Ille S, Engel L, Albers L, Schroeder A, Kelm A, Meyer B, Krieg SM (2019) Functional reorganization of cortical language function in glioma patients–a preliminary study. Front Oncol 9:446. https://doi.org/10.3389/fonc.2019.00446

    Article  PubMed  PubMed Central  Google Scholar 

  25. Atlas SW, Howard RS 2nd, Maldjian J, Alsop D, Detre JA, Listerud J, D’Esposito M, Judy KD, Zager E, Stecker M (1996) Functional magnetic resonance imaging of regional brain activity in patients with intracerebral gliomas: findings and implications for clinical management. Neurosurgery 38(2):329–338. https://doi.org/10.1097/00006123-199602000-00019

    Article  CAS  PubMed  Google Scholar 

  26. Baciu M, Perrone-Bertolotti M (2015) What do patients with epilepsy tell us about language dynamics? A review of fMRI studies. Rev Neurosci 26(3):323–341

    Article  PubMed  Google Scholar 

  27. Pravatà E, Sestieri C, Mantini D, Briganti C, Colicchio G, Marra C, Colosimo C, Tartaro A, Romani G, Caulo M (2011) Functional connectivity MR imaging of the language network in patients with drug-resistant epilepsy. Am J Neuroradiol 32(3):532–540

    Article  PubMed  PubMed Central  Google Scholar 

  28. 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. https://doi.org/10.1111/j.1749-6632.1977.tb41921.x

    Article  CAS  PubMed  Google Scholar 

  29. Mbwana J, Berl M, Ritzl E, Rosenberger L, Mayo J, Weinstein S, Conry J, Pearl P, Shamim S, Moore E (2009) Limitations to plasticity of language network reorganization in localization related epilepsy. Brain 132(2):347–356

    Article  CAS  PubMed  Google Scholar 

  30. Berl MM, Zimmaro LA, Khan OI, Dustin I, Ritzl E, Duke ES, Sepeta LN, Sato S, Theodore WH, Gaillard WD (2014) Characterization of atypical language activation patterns in focal epilepsy. Ann Neurol 75(1):33–42

    Article  PubMed  PubMed Central  Google Scholar 

  31. Perrone-Bertolotti M, Zoubrinetzky R, Yvert G, Le Bas JF, Baciu M (2012) Functional MRI and neuropsychological evidence for language plasticity before and after surgery in one patient with left temporal lobe epilepsy. Epilepsy Behav 23(1):81–86

    Article  CAS  PubMed  Google Scholar 

  32. Stasenko A, Schadler A, Kaestner E, Reyes A, Diaz-Santos M, Polczynska M, McDonald CR (2022) Can bilingualism increase neuroplasticity of language networks in epilepsy? Epilepsy Res 182:106893. https://doi.org/10.1016/j.eplepsyres.2022.106893

    Article  PubMed  PubMed Central  Google Scholar 

  33. Tzourio-Mazoyer N, Perrone-Bertolotti M, Jobard G, Mazoyer B, Baciu M (2017) Multi-factorial modulation of hemispheric specialization and plasticity for language in healthy and pathological conditions: a review. Cortex 86:314–339. https://doi.org/10.1016/j.cortex.2016.05.013

    Article  PubMed  Google Scholar 

  34. Hamberger MJ, Cole J (2011) Language organization and reorganization in epilepsy. Neuropsychol Rev 21(3):240–251

    Article  PubMed  PubMed Central  Google Scholar 

  35. Baciu M, Le Bas JF, Segebarth C, Benabid AL (2003) Presurgical fMRI evaluation of cerebral reorganization and motor deficit in patients with tumors and vascular malformations. Eur J Radiol 46(2):139–146. https://doi.org/10.1016/s0720-048x(02)00083-9

    Article  CAS  PubMed  Google Scholar 

  36. Deng X, Xu L, Zhang Y, Wang B, Wang S, Zhao Y, Cao Y, Zhang D, Wang R, Ye X, Wu J, Zhao J (2016) Difference of language cortex reorganization between cerebral arteriovenous malformations, cavernous malformations, and gliomas: a functional MRI study. Neurosurg Rev 39(2):241–249. https://doi.org/10.1007/s10143-015-0682-7

    Article  PubMed  Google Scholar 

  37. Chang EF, Gabriel RA, Potts MB, Garcia PA, Barbaro NM, Lawton MT (2009) Seizure characteristics and control after microsurgical resection of supratentorial cerebral cavernous malformations. Neurosurgery 65(1):31–37. https://doi.org/10.1227/01.NEU.0000346648.03272.07

    Article  PubMed  Google Scholar 

  38. Baumann CR, Schuknecht B, Lo Russo G, Cossu M, Citterio A, Andermann F, Siegel AM (2006) Seizure outcome after resection of cavernous malformations is better when surrounding hemosiderin-stained brain also is removed. Epilepsia 47(3):563–566. https://doi.org/10.1111/j.1528-1167.2006.00468.x

    Article  PubMed  Google Scholar 

  39. Thickbroom GW, Byrnes ML, Morris IT, Fallon MJ, Knuckey NW, Mastaglia FL (2004) Functional MRI near vascular anomalies: comparison of cavernoma and arteriovenous malformation. J Clin Neurosci 11(8):845–848

    Article  PubMed  Google Scholar 

  40. Chang CY, Peck KK, Brennan NM, Hou BL, Gutin PH, Holodny AI (2010) Functional MRI in the presurgical evaluation of patients with brain tumors: characterization of the statistical threshold. Stereotact Funct Neurosurg 88(1):35–41. https://doi.org/10.1159/000268740

    Article  PubMed  Google Scholar 

  41. Pak RW, Hadjiabadi DH, Senarathna J, Agarwal S, Thakor NV, Pillai JJ, Pathak AP (2017) Implications of neurovascular uncoupling in functional magnetic resonance imaging (fMRI) of brain tumors. J Cereb Blood Flow Metab 37(11):3475–3487. https://doi.org/10.1177/0271678X17707398

    Article  PubMed  PubMed Central  Google Scholar 

  42. Pillai JJ, Zaca D (2011) Clinical utility of cerebrovascular reactivity mapping in patients with low grade gliomas. World J Clin Oncol 2(12):397–403. https://doi.org/10.5306/wjco.v2.i12.397

    Article  PubMed  PubMed Central  Google Scholar 

  43. Qi C, Wang R, Meng L, Li S, Li Y (2022) Functional reorganization of contralesional networks varies according to isocitrate dehydrogenase 1 mutation status in patients with left frontal lobe glioma. Neuroradiology 64(9):1819–1828. https://doi.org/10.1007/s00234-022-02932-x

    Article  PubMed  Google Scholar 

Download references

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Author information

Authors and Affiliations

  1. Department of Neuroscience, Imaging and Clinical Sciences (DNISC), Università Degli Studi Gabriele d’Annunzio Di Chieti Pescara, 66100, Chieti, Italy

    Eleonora Piccirilli, Carlo Sestieri & Massimo Caulo

  2. Institute for Advanced Biomedical Technologies (ITAB), Università Degli Studi Gabriele d’Annunzio Di Chieti Pescara, Chieti, Italy

    Eleonora Piccirilli, Carlo Sestieri, Loris Di Clemente, Valentina Panara & Massimo Caulo

  3. Department of Imaging, Ospedale Pediatrico Bambino Gesù, IRCSS, Rome, Italy

    Eleonora Piccirilli

  4. Department of Innovative Technologies in Medicine and Dentistry, Università Degli Studi Gabriele d’Annunzio Di Chieti Pescara, Chieti, Italy

    Andrea Delli Pizzi

  5. Department of Radiology, SS. Annunziata University Hospital, Chieti, Italy

    Andrea Delli Pizzi, Marco Colasurdo, Valentina Panara & Massimo Caulo

Authors
  1. Eleonora Piccirilli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carlo Sestieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Loris Di Clemente
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrea Delli Pizzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marco Colasurdo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Valentina Panara
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Massimo Caulo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Massimo Caulo.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Piccirilli, E., Sestieri, C., Di Clemente, L. et al. The effect of different brain lesions on the reorganization of language functions within the dominant hemisphere assessed with task-based BOLD-fMRI. Radiol med 128, 775–783 (2023). https://doi.org/10.1007/s11547-023-01642-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11547-023-01642-5

Keywords

Search

Navigation