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Localizing hand motor area using resting-state fMRI: validated with direct cortical stimulation

  • Clinical Article - Neurosurgical Techniques
  • Published:
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Abstract

Background

Resting-state functional magnetic resonance imaging (R-fMRI) is a promising tool in clinical application, especially in presurgical mapping for neurosurgery. This study aimed to investigate the sensitivity and specificity of R-fMRI in the localization of hand motor area in patients with brain tumors validated by direct cortical stimulation (DCS). We also compared this technique to task-based blood oxygenation level-dependent (BOLD) fMRI (T-fMRI).

Methods

R-fMRI and T-fMRI were acquired from 17 patients with brain tumors. The cortex sites of the hand motor area were recorded by DCS. Site-by-site comparisons between R-fMRI/T-fMRI and DCS were performed to calculate R-fMRI and T-fMRI sensitivity and specificity using DCS as a “gold standard”. R-fMRI and T-fMRI performances were compared statistically

Results

A total of 609 cortex sites were tested with DCS and compared with R-fMRI findings in 17 patients. For hand motor area localization, R-fMRI sensitivity and specificity were 90.91 and 89.41 %, respectively. Given that two subjects could not comply with T-fMRI, 520 DCS sites were compared with T-fMRI findings in 15 patients. The sensitivity and specificity of T-fMRI were 78.57 and 84.76 %, respectively. In the 15 patients who successfully underwent both R-fMRI and T-fMRI, there was no statistical difference in sensitivity or specificity between the two methods (p = 0.3198 and p = 0.1431, respectively)

Conclusions

R-fMRI sensitivity and specificity are high for localizing hand motor area and even equivalent or slightly higher compared with T-fMRI. Given its convenience for patients, R-fMRI is a promising substitute for T-fMRI for presurgical mapping

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References

  1. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541

    Article  CAS  PubMed  Google Scholar 

  2. 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 

  3. Blume WT, Jones DC, Pathak P (2004) Properties of after-discharges from cortical electrical stimulation in focal epilepsies. Clin Neurophysiol 115:982–989

    Article  PubMed  Google Scholar 

  4. Boroojerdi B, Foltys H, Krings T, Spetzger U, Thron A, Topper R (1999) Localization of the motor hand area using transcranial magnetic stimulation and functional magnetic resonance imaging. Clin Neurophysiol 110:699–704

    Article  CAS  PubMed  Google Scholar 

  5. Chao-Gan Y, Yu-Feng Z (2010) DPARSF: a MATLAB Toolbox for “Pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 4:13

    PubMed Central  PubMed  Google Scholar 

  6. De Luca M, Smith S, De Stefano N, Federico A, Matthews PM (2005) Blood oxygenation level dependent contrast resting state networks are relevant to functional activity in the neocortical sensorimotor system. Exp Brain Res 167:587–594

    Article  PubMed  Google Scholar 

  7. Fair DA, Schlaggar BL, Cohen AL, Miezin FM, Dosenbach NU, Wenger KK, Fox MD, Snyder AZ, Raichle ME, Petersen SE (2007) A method for using blocked and event-related fMRI data to study “resting state” functional connectivity. Neuroimage 35:396–405

    Article  PubMed Central  PubMed  Google Scholar 

  8. Fox MD, Corbetta M, Snyder AZ, Vincent JL, Raichle ME (2006) Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proc Natl Acad Sci USA 103:10046–10051

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711

    Article  CAS  PubMed  Google Scholar 

  10. Jeong B, Choi J, Kim JW (2012) MRI study on the functional and spatial consistency of resting state-related independent components of the brain network. Korean J Radiol 13:265–274

    Article  PubMed Central  PubMed  Google Scholar 

  11. Kim MJ, Holodny AI, Hou BL, Peck KK, Moskowitz CS, Bogomolny DL, Gutin PH (2005) The effect of prior surgery on blood oxygen level-dependent functional MR imaging in the preoperative assessment of brain tumors. AJNR Am J Neuroradiol 26:1980–1985

    PubMed  Google Scholar 

  12. Kim SS, McCutcheon IE, Suki D, Weinberg JS, Sawaya R, Lang FF, Ferson D, Heimberger AB, DeMonte F, Prabhu SS (2009) Awake craniotomy for brain tumors near eloquent cortex: correlation of intraoperative cortical mapping with neurological outcomes in 309 consecutive patients. Neurosurgery 64:836–845, discussion 345–836

    Article  PubMed  Google Scholar 

  13. Kokkonen SM, Nikkinen J, Remes J, Kantola J, Starck T, Haapea M, Tuominen J, Tervonen O, Kiviniemi V (2009) Preoperative localization of the sensorimotor area using independent component analysis of resting-state fMRI. Magn Reson Imaging 27:733–740

    Article  PubMed  Google Scholar 

  14. Liu H, Buckner RL, Talukdar T, Tanaka N, Madsen JR, Stufflebeam SM (2009) Task-free presurgical mapping using functional magnetic resonance imaging intrinsic activity. J Neurosurg 111:746–754

    Article  PubMed Central  PubMed  Google Scholar 

  15. Mathews S, Oommen KJ, Francel P (2001) Functional reorganization of motor cortex due to brain tumor: a case report. J Okla State Med Assoc 94:7–11

    CAS  PubMed  Google Scholar 

  16. Matz PG, Cobbs C, Berger MS (1999) Intraoperative cortical mapping as a guide to the surgical resection of gliomas. J Neurooncol 42:233–245

    Article  CAS  PubMed  Google Scholar 

  17. Morgan VL, Sonmezturk HH, Gore JC, Abou-Khalil B (2012) Lateralization of temporal lobe epilepsy using resting functional magnetic resonance imaging connectivity of hippocampal networks. Epilepsia 53:1628–1635

    Article  PubMed Central  PubMed  Google Scholar 

  18. Pekar JJ (2006) A brief introduction to functional MRI. IEEE Eng Med Biol Mag 25:24–26

    Article  PubMed  Google Scholar 

  19. 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  CAS  PubMed  Google Scholar 

  20. Qiu TM, Wu JS, Zhuang DX, Yao C, Lu J, Zhang J, Gong X, Mao Y, Zhou L (2012) Preliminary application of resting-state functional magnetic resonance imaging in localizing language cortex for glioma patients. Chin J Neurosurg 28:1196–1200

  21. 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 Tesla) in glioma patients by navigated electrocortical stimulation and postoperative outcome. J Neurol Neurosurg Psychiatry 76:1152–1157

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. 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 52:1335–1345, discussion 1345–1337

    Article  PubMed  Google Scholar 

  23. Rutten GJ, Ramsey NF (2010) The role of functional magnetic resonance imaging in brain surgery. Neurosurg Focus 28:E4

    Article  PubMed  Google Scholar 

  24. Shimony JS, Zhang D, Johnston JM, Fox MD, Roy A, Leuthardt EC (2009) Resting-state spontaneous fluctuations in brain activity: a new paradigm for presurgical planning using fMRI. Acad Radiol 16:578–583

    Article  PubMed Central  PubMed  Google Scholar 

  25. Shinoura N, Suzuki Y, Yamada R, Kodama T, Takahashi M, Yagi K (2006) Restored activation of primary motor area from motor reorganization and improved motor function after brain tumor resection. AJNR Am J Neuroradiol 27:1275–1282

    CAS  PubMed  Google Scholar 

  26. Song XW, Dong ZY, Long XY, Li SF, Zuo XN, Zhu CZ, He Y, Yan CG, Zang YF (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6:e25031

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Spagnolli F, Cerini R, Cardobi N, Barillari M, Manganotti P, Storti S, Mucelli RP (2013) Brain modifications after acute alcohol consumption analyzed by resting state fMRI. Magn Reson Imaging 31:1325-1330

  28. Talacchi A, Turazzi S, Locatelli F, Sala F, Beltramello A, Alessandrini F, Manganotti P, Lanteri P, Gambin R, Ganau M, Tramontano V, Santini B, Gerosa M (2010) Surgical treatment of high-grade gliomas in motor areas. The impact of different supportive technologies: a 171-patient series. J Neurooncol 100:417–426

    Article  PubMed  Google Scholar 

  29. Thomas JB, Brier MR, Snyder AZ, Vaida FF, Ances BM (2013) Pathways to neurodegeneration: effects of HIV and aging on resting-state functional connectivity. Neurology 80:1186–1193

    Article  PubMed Central  PubMed  Google Scholar 

  30. Trebuchon A, Guye M, Tcherniack V, Tramoni E, Bruder N, Metellus P (2012) Interest of EEG recording during direct electrical stimulation for brain mapping function in surgery. Ann Fr Anesth Reanim 31:e87–e90

    Article  CAS  PubMed  Google Scholar 

  31. Wang L, Li K, Zhang QE, Zeng YW, Jin Z, Dai WJ, Su YA, Wang G, Tan YL, Yu X, Si TM (2013) Interhemispheric functional connectivity and its relationships with clinical characteristics in major depressive disorder: a resting state fMRI study. PLoS One 8:e60191

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Wengenroth M, Blatow M, Guenther J, Akbar M, Tronnier VM, Stippich C (2011) Diagnostic benefits of presurgical fMRI in patients with brain tumours in the primary sensorimotor cortex. Eur Radiol 21:1517–1525

    Article  PubMed Central  PubMed  Google Scholar 

  33. Xiong J, Parsons LM, Gao JH, Fox PT (1999) Interregional connectivity to primary motor cortex revealed using MRI resting state images. Hum Brain Mapp 8:151–156

    Article  CAS  PubMed  Google Scholar 

  34. Yang H, Chopp M, Weiland B, Zhang X, Tepley N, Jiang F, Schallert T (2007) Sensorimotor deficits associated with brain tumor progression and tumor-induced brain plasticity mechanisms. Exp Neurol 207:357–367

    Article  CAS  PubMed  Google Scholar 

  35. Yousry TA, Schmid UD, Alkadhi H, Schmidt D, 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(Pt 1):141–157

    Article  Google Scholar 

  36. Yu Y, Shen H, Zhang H, Zeng LL, Xue Z, Hu D (2013) Functional connectivity-based signatures of schizophrenia revealed by multiclass pattern analysis of resting-state fMRI from schizophrenic patients and their healthy siblings. Biomed Eng Online 12:10

    Article  PubMed Central  PubMed  Google Scholar 

  37. Zeng H, Pizarro R, Nair VA, La C, Prabhakaran V (2013) Alterations in regional homogeneity of resting-state brain activity in mesial temporal lobe epilepsy. Epilepsia 54:658–666

    Article  PubMed Central  PubMed  Google Scholar 

  38. Zhang D, Johnston JM, Fox MD, Leuthardt EC, Grubb RL, Chicoine MR, Smyth MD, Snyder AZ, Raichle ME, Shimony JS (2009) Preoperative sensorimotor mapping in brain tumor patients using spontaneous fluctuations in neuronal activity imaged with functional magnetic resonance imaging: initial experience. Neurosurgery 65:226–236

    Article  PubMed Central  PubMed  Google Scholar 

  39. Zhang LJ, Qi R, Zhong J, Ni L, Zheng G, Xu J, Lu GM (2013) Disrupted functional connectivity of the anterior cingulate cortex in cirrhotic patients without overt hepatic encephalopathy: a resting state fMRI study. PLoS One 8:e53206

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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The authors would like to thank Jian-bing Shi and Zhong Yang for assembling the image database, Gen Xu for direct cortical stimulation, and Yan-yan Song for statistical analysis.

Author contributions

Study concept and design: Zhou and Wu. Processing of data: Qiu, Zhuang, Yao, Lu, Zhu, and Tang. Analysis and interpretation of data: Qiu and Yan. Drafting of the manuscript: Qiu and Yan. Critical revision of the manuscript for important intellectual content: Wu, Mao and Zhou.

Financial Disclosure

None reported.

Funding

This work was funded by the National Natural Science Foundation of China (Project No. 81271517, 81171295), The National Key Technology R&D Program of China (No. 2014BAI04B05), and Shanghai Municipal Health Bureau (XBR2011022).

Conflict of interest

None.

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Corresponding author

Correspondence to Liang-fu Zhou.

Additional information

Tian-ming Qiu and Chao-gan Yan contributed equally to this paper.

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Qiu, Tm., Yan, Cg., Tang, Wj. et al. Localizing hand motor area using resting-state fMRI: validated with direct cortical stimulation. Acta Neurochir 156, 2295–2302 (2014). https://doi.org/10.1007/s00701-014-2236-0

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  • DOI: https://doi.org/10.1007/s00701-014-2236-0

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