Skip to main content
SpringerLink
Log in

Alternative language paradigms for functional magnetic resonance imaging as presurgical tools for inducing crossed cerebro-cerebellar language activations in brain tumor patients

  • Neuro
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

Crossed cerebro-cerebellar BOLD activations have recently come to light as additional diagnostic features for patients with brain tumors. The covert verb generation (VG) task is a widely used language paradigm to determine these language-related crossed activations. Here we demonstrate these crossed activations in two additional language paradigms, the semantic and phonological association tasks. We propose the merit of these tasks to language lateralization determination in the clinic as they are easy to monitor and suitable for patients with aphasia.

Methods

Patients with brain tumors localized at different cortical sites (n = 71) performed three language paradigms, namely the VG task as well as the semantic (SA) and phonological (PA) association tasks with button-press responses. Respective language activations in disparate cortical regions and the cerebellum were assigned laterality. Agreements in laterality between the two new tasks and the verb generation task were tested using Cohen’s kappa.

Results

Both tasks significantly agreed in cortical and cerebellar lateralization with the verb generation task in patients. Additionally, a McNemar test confirmed the presence of crossed activations in the cortex and the cerebellum in the entire subject population.

Conclusion

We demonstrated that the semantic and phonological association tasks resulted in crossed cerebro-cerebellar language lateralization activations as those observed due to the covert verb generation task. This may suggest the possibility of these tasks being used conjointly with the traditional verb generation task, especially for subjects that may be unable to perform the latter.

Key Points

• The semantic and phonological association tasks can be useful as additional presurgical fMRI language lateralization paradigms for brain tumor patients along with the standard verb generation task.

• All three tasks also confirm the presence of crossed cerebro-cerebellar language activations in the current subject population.

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

Similar content being viewed by others

Abbreviations

PA:

Phonological association

SA:

Semantic association

VG:

Verb generation

References

  1. Patel AP, Fisher JL, Nichols E et al (2019) Global, regional, and national burden of brain and other CNS cancer, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 18(4):376–393

    Article  Google Scholar 

  2. Ruff IM, Petrovich Brennan NM, Peck KK et al (2008) Assessment of the language laterality index in patients with brain tumor using functional MR imaging: effects of thresholding, task selection, and prior surgery. AJNR Am J Neuroradiol 29(3):528 LP–528535

  3. Maldjian JA, Schulder M, Liu WC et al (1997) Intraoperative functional MRI using a real-time neurosurgical navigation system. J Comput Assist Tomogr 21(6):910–912

    Article  CAS  Google Scholar 

  4. Moritz C, Haughton V (2003) Functional MR imaging: paradigms for clinical preoperative mapping. Magn Reson Imaging Clin N Am 11(4):529–542

    Article  Google Scholar 

  5. Roux FE, Boulanouar K, Lotterie JA, Mejdoubi M, LeSage JP, Berry I (2003) Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery 52(6):1335–1337

    Article  Google Scholar 

  6. Ojemann GA (1993) Functional mapping of cortical language areas in adults. Intraoperative approaches. Adv Neurol 63:155–163

    CAS  PubMed  Google Scholar 

  7. Benson RR, FitzGerald DB, LeSueur LL et al (1999) Language dominance determined by whole brain functional MRI in patients with brain lesions. Neurology 52(4):798–798

    Article  CAS  Google Scholar 

  8. Brannen JH, Badie B, Moritz CH, Quigley M, Meyerand ME, Haughton VM (2001) Reliability of functional MR imaging with word-generation tasks for mapping Broca’s area. AJNR Am J Neuroradiol 22(9):1711 LP–24 1718

  9. Petrovich NM, Holodny AI, Brennan CW, Gutin PH (2004) Isolated translocation of Wernicke’s area to the right hemisphere in a 62-year-man with a temporo-parietal glioma. Am J Neuroradiol 25(1):130 LP–130133

    Google Scholar 

  10. Smits M (2012) Functional magnetic resonance imaging (fMRI) in brain tumour patients. Eur Assoc NeuroOncol Mag 2(3):123–128

    Google Scholar 

  11. Mazoyer B, Zago L, Jobard G et al (2013) Gaussian mixture modeling of hemispheric lateralization for language in a large sample of healthy individuals balanced for handedness. PLoS One 9:e101165–e101165

    Article  Google Scholar 

  12. Knecht S, Dräger B, Deppe M et al (2000) Handedness and hemispheric language dominance in healthy humans. Brain 123:2512–2518

    Article  Google Scholar 

  13. Szaflarski JP, Binder JR, Possing ET, McKiernan KA, Ward BD, Hammeke TA (2002) Language lateralization in left-handed and ambidextrous people fMRI data. Neurology 59:238–244

    Article  CAS  Google Scholar 

  14. Tzourio-Mazoyer NN, Josse G, Crivello F, Mazoyer B (2004) Interindividual variability in the hemispheric organization for speech. Neuroimage 21:422–435

  15. Hubrich-Ungureanu P, Kaemmerer N, Henn FA, Braus DF (2003) Lateralized organization of the cerebellum in a silent verbal fluency task: a functional magnetic resonance imaging study in healthy volunteers. Neurosci Lett 319:91–94

    Article  Google Scholar 

  16. Mendez Orellana CM, Visch-Brink EG, Vernooij M et al (2015) Crossed cerebrocerebellar language lateralization: an additional diagnostic feature for assessing atypical language representation in presurgical functional MR imaging. AJNR Am J Neuroradiol 36:518–524

    Article  CAS  Google Scholar 

  17. Jansen A, Flo ̈el A, Van Randenborgh J et al (2005) Crossed cerebro-cerebellar language dominance. Hum Brain Mapp 24:165–172

    Article  Google Scholar 

  18. Fabbro F, Moretti R, Bava A (2000) Language impairments in patients with cerebellar lesions. J Neurolinguistics 13(2–3):173–188

    Article  Google Scholar 

  19. Cook M, Murdoch B, Cahill L, Whelan BM (2004) Higher-level language deficits resulting from left primary cerebellar lesions. Aphasiology 18(9):771–784

    Article  Google Scholar 

  20. Murdoch BE, Whelan BM (2007) Language disorders subsequent to left cerebellar lesions: a case for bilateral cerebellar involvement in language? Folia Phoniatr Logop 59(4):184–189

    Article  Google Scholar 

  21. Frank B, Maschke M, Groetschel H et al (2010) Aphasia and neglect are uncommon in cerebellar disease: negative findings in a prospective study in acute cerebellar stroke. Cerebellum 9(4):556–566

    Article  Google Scholar 

  22. FitzGerald DB, Cosgrove GR, Ronner S et al (1997) Location of language in the cortex: a comparison between functional MR imaging and electrocortical stimulation. AJNR Am J Neuroradiol 18:1529–1539

  23. Mendez Orellana CM, Visch-Brink EG, de Jong-Hagelstein M, Koudstaal PJ, van der Lugt A, Smits M (2012) Decreased relative contribution to language processing of the right hemisphere after language therapy assessed with fMRI in chronic aphasia patients. Procedia Soc Behav Sci 61:20–21

    Article  Google Scholar 

  24. Dym RJ, Burns J, Freeman K, Lipton ML (2011) Is functional MR imaging assessment of hemispheric language dominance as good as the Wada test? A meta-analysis. Radiology 261:446–455

    Article  Google Scholar 

  25. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113

    Article  CAS  Google Scholar 

  26. Méndez-Orellana CM, Holme C, Sandoval-León K, Cortés-Rivera B, Méndez-Orellana P, Martínez-Ferreiro S (2019) Spontaneous speech analysis in Spanish-speaking adults: normative data in healthy adults, elderly adults and patients with brain lesions. Stem-, Spraak- en Taalpathologie 24:224–226

    Google Scholar 

  27. Renzi ED, Faglioni P (1978) Normative data and screening power of a shortened version of the Token Test. Cortex. 14:41–49

    Article  Google Scholar 

  28. Witte ED, Satoer D, Robert E et al (2015) The Dutch Linguistic Intraoperative Protocol: a valid linguistic approach to awake brain surgery. Brain Lang 140:35–48

    Article  Google Scholar 

  29. Smits M, Visch-Brink EG, Schraa-Tam CK, Koudstaal PJ, van der Lugt A (2006) Functional MR imaging of language processing: an overview of easy-to-implement paradigms for patient care and clinical research. Radiographics 26:S145–S158

    Article  Google Scholar 

  30. Jakola AS, Unsgård G, Myrmel KS et al (2012) Low grade gliomas in eloquent locations – implications for surgical strategy, survival and long term quality of life. PLoS One 7(12):e51450

    Article  CAS  Google Scholar 

  31. Asher A, Fu JB, Bailey C, Hughes JK (2016) Fatigue among patients with brain tumors. CNS Oncol 5(2):91–100

    Article  CAS  Google Scholar 

  32. Banerjee P, Leu K, Harris RJ et al (2015) Association between lesion location and language function in adult glioma using voxel-based lesion-symptom mapping. Neuroimage Clin 9:617–624

    Article  Google Scholar 

  33. Cabeza R (2002) Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol Aging 17(1):85

    Article  Google Scholar 

  34. Wierenga CE, Benjamin M, Gopinath K et al (2008) Age-related changes in word retrieval: the role of bilateral frontal and subcortical networks. Neurobiol Aging 29(3):436–451

    Article  Google Scholar 

  35. Abrahams S, Goldstein LH, Simmons A et al (2003) Functional magnetic resonance imaging of verbal fluency and confrontation naming using compressed image acquisition to permit overt responses. Hum Brain Mapp 20:29–40

    Article  Google Scholar 

  36. Zaca D, Jarso S, Pillai JJ (2013) Role of semantic paradigms for optimization of language mapping in clinical FMRI studies. AJNR Am J Neuroradiol 34:1966–1971

    Article  CAS  Google Scholar 

  37. Fiez JA, Petersen SE (1998) Neuroimaging studies of word reading. Proc Natl Acad Sci U S A 95:914–921

    Article  CAS  Google Scholar 

  38. Meinzer M, Wilser L, Flaisch T et al (2009) Neural signatures of semantic and phonemic fluency in young and old adults. J Cogn Neurosci 21:2007–2018

    Article  Google Scholar 

  39. Friederici AD (2011) The brain basis of language processing: from structure to function. Physiol Rev 91:1357–1392

    Article  Google Scholar 

  40. Friederici AD, Chomsky N, Berwick RC, Moro A, Bolhuis JJ (2017) Language, mind and brain. Nat Hum Behav 1:713–722

    Article  Google Scholar 

Download references

Acknowledgements

The researchers acknowledge the help of the following clinical radiographers: Patricio-Díaz-López, Felipe Navarrete-Fernandez, Joel Guerrero Galdames, Eric Sánchez Sanhueza, and Rodrigo Bastidas-Martínez.

Funding

This study was funded by the Agencia Nacional de Investigación y Desarrollo (ANID Chile) grant FONDECYT Initiation into Research Study N° 111150429 and the 2020 ANID doctoral scholarship grant N° 21201983.

Author information

Authors and Affiliations

  1. Interdisciplinary Center for Neuroscience, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile

    Ishani Thakkar

  2. Department of Radiology, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile

    Leonardo Arraño-Carrasco & Romina Zunino-Pesce

  3. School of Speech and Language Pathology, Faculty of Health, Universidad Santo Tomás, Santiago, Chile

    Barbara Cortes-Rivera

  4. Department of Neurosurgery, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile

    Francisco Mery-Muñoz

  5. Institute for Biological and Medical Engineering, Pontificia Universidad Católica de Chile, Santiago, Chile

    María Rodriguez-Fernández

  6. Department of Radiology & Nuclear Medicine, Erasmus MC–University Medical Center Rotterdam, Rotterdam, The Netherlands

    Marion Smits

  7. School of Speech and Language Pathology, Health Sciences Department, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile

    Carolina Mendez-Orellana

Authors
  1. Ishani Thakkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leonardo Arraño-Carrasco
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Barbara Cortes-Rivera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Romina Zunino-Pesce
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Francisco Mery-Muñoz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. María Rodriguez-Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marion Smits
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Carolina Mendez-Orellana
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carolina Mendez-Orellana.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Carolina P. Mendez-Orellana.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.

Study subjects or cohorts overlap

In a pilot study that aimed to evaluate the effect of demographic variables in the performance of the verbal generation, semantic and phonological association language tasks, we reported data from 10 brain tumor patients included in this study.

Methodology

• cross-sectional study

• multicenter study

Additional information

Publisher’s note

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

Supplementary Information

ESM 1

(DOCX 393 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thakkar, I., Arraño-Carrasco, L., Cortes-Rivera, B. et al. Alternative language paradigms for functional magnetic resonance imaging as presurgical tools for inducing crossed cerebro-cerebellar language activations in brain tumor patients. Eur Radiol 32, 300–307 (2022). https://doi.org/10.1007/s00330-021-08137-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-021-08137-9

Keywords

Search

Navigation