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Validation of functional motor and language MRI with direct cortical stimulation

  • Experimental research - Brain Tumors
  • Published:
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Abstract

Background

Functional magnetic resonance imaging (fMRI) is a widely available method and is therefore progressively utilized in neurosurgical practice. This study was carried out to determine fMRI sensitivity and specificity and to emphasize the threshold dependence of fMRI data.

Methods

A total of 17 consecutive patients, scheduled for surgery on intracerebral lesions near eloquent brain areas, underwent preoperative motor (N = 12) and language (N = 5) fMRI. Functional data were analyzed with SPM software and displayed on a neuronavigation system for intraoperative guidance. High-risk maps for motor and language deficits obtained from direct electric cortical stimulation (DECS) were used for validation of functional activated areas. In a first analysis step, sensitivity and specificity were calculated in terms of a side-by-side correlation. The next step, the threshold dependence of fMRI data sensitivity and specificity, was estimated according to four statistical thresholds (p1 < 0.05, p2 < 0.0005, p3 < 0.00001, p4 < 0.0000001).

Results

Both functional imaging and DECS revealed definite results for the investigated areas in all patients. Calculation of sensitivity and specificity resulted in 100 % and 68 % for the motor group and a sensitivity of 75 % and specificity of 68 % for the language group at the fixed threshold analysis. Threshold-dependent analysis of the obtained data revealed a sensitivity/specificity relationship from 100 %/0 % at threshold (p1), 100 %/5 % at (p2), 74 %/9 % at (p3), and 37 %/36 % at (p4) for the motor group. Evaluation of threshold-dependent sensitivity and specificity for the language group resulted in 78 %/51 % at threshold (p1), 67 %/75 % at (p2), 50 %/78 % at (p3), and 33 %/89 % at (p4).

Conclusions

The present findings on the threshold dependence of fMRI data demonstrate why individualized thresholds should be obtained in case of fMRI evaluation. Although the results are satisfying in most cases, fMRI is apparently not sufficient for critical intraoperative decision-making.

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References

  1. Bizzi A, Blasi V, Falini A, Ferroli P, Cadioli M, Danesi U, Aquino D, Marras C, Caldiroli D, Broggi G (2008) Presurgical functional MR imaging of language and motor functions: validation with intraoperative electrocortical mapping. Radiology 248:579–589

    Article  PubMed  Google Scholar 

  2. 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. Am J Neuroradiol 22:1711–1718

    PubMed  CAS  Google Scholar 

  3. Fandino J, Kollias SS, Wieser HG, Valavanis A, Yonekawa Y (1999) Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. J Neurosurg 91:238–250

    Article  PubMed  CAS  Google Scholar 

  4. Fernandez G, Specht K, Weis S, Tendolkar I, Reuber M, Fell J, Klaver P, Ruhlmann J, Reul J, Elger CE (2003) Intrasubject reproducibility of presurgical language lateralization and mapping using fMRI. Neurology 60:969–975

    Article  PubMed  CAS  Google Scholar 

  5. Fesl G, Demmel M, Albrecht J, Kopietz R, Schoepf V, Kleemann AM, Pollatos O, Anzinger A, Schreder T, Brueckmann H, Wiesmann M (2010) Bad mood–bad activation?: the influence of emotions on the BOLD signal during finger tapping. Clin Neuroradiol 20:153–159

    Article  PubMed  CAS  Google Scholar 

  6. FitzGerald DB, Cosgrove GR, Ronner S, Jiang H, Buchbinder BR, Belliveau JW, Rosen BR, Benson RR (1997) Location of language in the cortex: a comparison between functional MR imaging and electrocortical stimulation. AJNR Am J Neuroradiol 18:1529–1539

    PubMed  CAS  Google Scholar 

  7. Giussani C, Roux FE, Ojemann J, Sganzerla EP, Pirillo D, Papagno C (2010) Is preoperative functional magnetic resonance imaging reliable for language areas mapping in brain tumor surgery? Review of language functional magnetic resonance imaging and direct cortical stimulation correlation studies. Neurosurgery 66:113–120

    Article  PubMed  Google Scholar 

  8. Haglund MM, Berger MS, Shamseldin M, Lettich E, Ojemann GA (1994) Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 34:567–576

    Article  PubMed  CAS  Google Scholar 

  9. Haglund MM, Ojemann GA, Blasdel GG (1993) Optical imaging of bipolar cortical stimulation. J Neurosurg 78:785–793

    Article  PubMed  CAS  Google Scholar 

  10. Hastreiter P, Rezk-Salama C, Soza G, Bauer M, Greiner G, Fahlbusch R, Ganslandt O, Nimsky C (2004) Strategies for brain shift evaluation. Med Image Anal 8:447–464

    Article  PubMed  Google Scholar 

  11. Havel P, Braun B, Rau S, Tonn J, Fesl G, Brückmann H, Ilmberger J (2006) Reproducibility of activation in four motor paradigms. An fMRI study. J Neurol 253:471–476

    Article  PubMed  Google Scholar 

  12. Hirsch J, Ruge MI, Kim KHS, Correa DD, Victor JD, Relkin NR, Labar DR, Krol G, Bilsky MH, Souweidane MM, DeAngelis LM, Gutin PH (2000) An integrated functional magnetic resonance imaging procedure for preoperative mapping of cortical areas associated with tactile, motor, language, and visual functions. Neurosurg Online 47:711

    CAS  Google Scholar 

  13. Ilmberger J, Ruge M, Kreth FW, Briegel J, Reulen HJ, Tonn JC (2008) Intraoperative mapping of language functions: a longitudinal neurolinguistic analysis. J Neurosurg 109:583–592

    Article  PubMed  Google Scholar 

  14. Kannurpatti SS, Motes MA, Rypma B, Biswal BB (2011) Non-neural BOLD variability in block and event-related paradigms. Magn Reson Imaging 29:140–146

    Article  PubMed  Google Scholar 

  15. Kopietz R, Albrecht J, Linn J, Pollatos O, Anzinger A, Wesemann T, Fesl G, Stephan T, Bruckmann H, Wiesmann M (2009) Echo time dependence of BOLD fMRI studies of the piriform cortex. Klin Neuroradiol 19:275–282

    Article  PubMed  Google Scholar 

  16. Krings T, Buchbinder BR, Butler WE, Chiappa KH, Jiang HJ, Rosen BR, Cosgrove GR (1997) Stereotactic transcranial magnetic stimulation: correlation with direct electrical cortical stimulation. Neurosurgery 41:1319–1325, discussion 1325–1316

    Article  PubMed  CAS  Google Scholar 

  17. Krings T, Schreckenberger M, Rohde V, Spetzger U, Sabri O, Reinges MHT, Hans FJ, Meyer PT, Möller-Hartmann W, Gilsbach JM, Buell U, Throan A (2002) Functional MRI and 18F FDG-positron emission tomography for presurgical planning: comparison with electrical cortical stimulation. Acta Neurochir (Wien) 144:889–899

    Article  CAS  Google Scholar 

  18. Lehericy S, Duffau H, Cornu P, Capelle L, Pidoux B, Carpentier A, Auliac S, Clemenceau S, Sichez JP, Bitar A, Valery CA, Van Effenterre R, Faillot T, Srour A, Fohanno D, Philippon J, Le Bihan D, Marsault C (2000) Correspondence between functional magnetic resonance imaging somatotopy and individual brain anatomy of the central region: comparison with intraoperative stimulation in patients with brain tumors. J Neurosurg 92:589–598

    Article  PubMed  CAS  Google Scholar 

  19. Mattay VS, Frank JA, Santha AK, Pekar JJ, Duyn JH, McLaughlin AC, Weinberger DR (1996) Whole-brain functional mapping with isotropic MR imaging. Radiology 201:399–404

    PubMed  CAS  Google Scholar 

  20. Mueller WM, Yetkin FZ, Hammecke TA, Morris GL, Swanson SJ, Reichert K, Cox R, Haughton VM (1996) Functional magnetic resonance imaging mapping of the motor cortex in patients with cerebral tumors. Neurosurgery 39:515–520

    PubMed  CAS  Google Scholar 

  21. Neggers SF, Langerak TR, Schutter DJ, Mandl RC, Ramsey NF, Lemmens PJ, Postma A (2004) A stereotactic method for image-guided transcranial magnetic stimulation validated with fMRI and motor-evoked potentials. NeuroImage 21:1805–1817

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  23. Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389–443

    Article  Google Scholar 

  24. Pouratian N, Bookheimer SY, Rex DE, Martin NA, Toga AW (2002) Utility of preoperative functional magnetic resonance imaging for identifying language cortices in patients with vascular malformations. J Neurosurg 97:21–32

    Article  PubMed  Google Scholar 

  25. Puce A, Constable R, Luby M, McCarthy G, Nobre A, Spencer D, Gore J, Allison T (1995) Functional magnetic resonance imaging of sensory and motor cortex: comparison with electrophysiological localization. J Neurosurg 83:262–270

    Article  PubMed  CAS  Google Scholar 

  26. Pujol J, Conesa G, Deus J, Lopez-Obarrio L, Isamat F, Capdevila A (1998) Clinical application of functional magnetic resonance imaging in presurgical identification of the central sulcus. J Neurosurg 88:863–869

    Article  PubMed  CAS  Google Scholar 

  27. Rau S, Fesl G, Bruhns P, Havel P, Braun B, Tonn JC, Ilmberger J (2007) Reproducibility of activations in Broca area with two language tasks: a functional MR imaging study. AJNR Am J Neuroradiol 28:1346–1353

    Article  PubMed  CAS  Google Scholar 

  28. Reinges MH, Nguyen HH, Krings T, Hutter BO, Rohde V, Gilsbach JM (2004) Course of brain shift during microsurgical resection of supratentorial cerebral lesions: limits of conventional neuronavigation. Acta Neurochir 146:369–377

    Article  PubMed  CAS  Google Scholar 

  29. Roessler K, Donat M, Lanzenberger R, Novak K, Geissler A, Gartus A, Tahamtan AR, Milakara D, Czech T, Barth M, Knosp E, Beisteiner R (2005) Evaluation of preoperative high magnetic field motor functional MRI (3 T) in glioma patients by navigated electrocortical stimulation and postoperative outcome. J Neurol Neurosurg Psychiatry 76:1152–1157

    Article  PubMed  CAS  Google Scholar 

  30. 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 52:1335–13345

    Article  PubMed  Google Scholar 

  31. Roux FE, Boulanouar K, Ranjeva J, Tremoulet M, Henry P, Manelfe C, Sabatier J, Berry I (1999) Usefulness of motor functional MRI correlated to cortical mapping in rolandic low-grade astrocytomas. Acta Neurochir 141:71–79

    Article  PubMed  CAS  Google Scholar 

  32. Roux FE, Ibarrola D, Tremoulet M, Lazorthes Y, Henry P, Sol JC, Berry I (2001) Methodological and technical issues for integrating functional magnetic resonance imaging data in a neuronavigational system. Neurosurgery 49:1145–1156

    PubMed  CAS  Google Scholar 

  33. Ruff IM, Petrovich Brennan NM, Peck KK, Hou BL, Tabar V, Brennan CW, Holodny AI (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 29:528–535

    Article  PubMed  CAS  Google Scholar 

  34. Ruge MI, Victor J, Hosain S, Correa DD, Relkin NR, Tabar V, Brennan C, Gutin PH, Hirscha J (1999) Concordance between functional magnetic resonance imaging and intraoperative language mapping. Stereotact Funct Neurosurg 72:95–102

    Article  PubMed  CAS  Google Scholar 

  35. Rutten GJM, Ramsey NF, van Rijen PC, Noordmans HJ, van Veelen CWM (2002) Development of a functional magnetic resonance imaging protocol for intraoperative localization of critical temporoparietal language areas. Ann Neurol 51:350–360

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  37. Schreckenberger M, Spetzger U, Sabri O, Meyer PT, Zeggel T, Zimny M, Gilsbach J, Buell U (2001) Localisation of motor areas in brain tumour patients: a comparison of preoperative [18F]FDG-PET and intraoperative cortical electrostimulation. Eur J Nucl Med 28:1394–1403

    Article  PubMed  CAS  Google Scholar 

  38. Schulder M, Azmi H, Biswal B (2003) Functional magnetic resonance imaging in a low-field intraoperative scanner. Stereotact Funct Neurosurg 80:125–131

    Article  PubMed  Google Scholar 

  39. Shinoura N, Yamada R, Kodama T, Suzuki Y, Takahashi M, Yagi K (2005) Intraoperative cortical mapping has low sensitivity for the detection of motor function in proximity to a tumor in the primary motor area. Stereotact Funct Neurosurg 83:135–141

    Article  PubMed  CAS  Google Scholar 

  40. Tharin S, Golby A (2007) Functional brain mapping and its applications to neurosurgery. Neurosurgery 60:185–201

    Article  PubMed  Google Scholar 

  41. Vinas FC, Zamorano L, Mueller RA, Jiang Z, Chugani H, Fuerst D, Muzik O, Mangner TJ, Diaz FG (1997) [15O]-Water PET and intraoperative brain mapping: a comparison in the localization of eloquent cortex. Neurol Res 19:601–608

    PubMed  CAS  Google Scholar 

  42. Yetkin FZ, McAuliffe TL, Cox R (1996) Test-Retest precision of functional MR in sensory and motor task activation. AJNR Am J Neuroradiol 17:95–98

    PubMed  CAS  Google Scholar 

  43. Yousry TA, Schmid UD, Alkadhi HSD, Peraud A, Buettner A, Winkler P (1997) Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 120:141–157

    Article  PubMed  Google Scholar 

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Meier, M.P., Ilmberger, J., Fesl, G. et al. Validation of functional motor and language MRI with direct cortical stimulation. Acta Neurochir 155, 675–683 (2013). https://doi.org/10.1007/s00701-013-1624-1

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  • DOI: https://doi.org/10.1007/s00701-013-1624-1

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