Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Improving fMRI in signal drop-out regions at 7 T by using tailored radio-frequency pulses: application to the ventral occipito-temporal cortex

Abstract

Objective

Signal drop-off occurs in echo-planar imaging in inferior brain areas due to field gradients from susceptibility differences between air and tissue. Tailored-RF pulses based on a hyperbolic secant (HS) have been shown to partially recover signal at 3 T, but have not been tested at higher fields.

Materials and methods

The aim of this study was to compare the performance of an optimized tailored-RF gradient-echo echo-planar imaging (TRF GRE-EPI) sequence with standard GRE-EPI at 7 T, in a passive viewing of faces or objects fMRI paradigm in healthy subjects.

Results

Increased temporal-SNR (tSNR) was observed in the middle and inferior temporal lobes and orbitofrontal cortex of all subjects scanned, but elsewhere tSNR decreased relative to the standard acquisition. In the TRF GRE-EPI, increased functional signal was observed in the fusiform, lateral occipital cortex, and occipital pole, regions known to be part of the visual pathway involved in face-object perception.

Conclusion

This work highlights the potential of TRF approaches at 7 T. Paired with a reversed-gradient distortion correction to compensate for in-plane susceptibility gradients, it provides an improved acquisition strategy for future neurocognitive studies at ultra-high field imaging in areas suffering from static magnetic field inhomogeneities.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. 1.

    Ogawa S, Lee TM, Kay AR, Tank DW (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 87:9868–9872

  2. 2.

    Mansfield P (1997) Multi-planar image formation using NMR spin echoes. J Phys C: Solid State Phys 10:L55–L58

  3. 3.

    Jezzard P, Clare S (1999) Sources of distortion in functional MRI data. Hum Brain Mapp 8(2–3):80–85

  4. 4.

    Jezzard P (2012) Correction of geometric distortion in fMRI data. NeuroImage 62:648–651

  5. 5.

    Ojemann JG, Akbudak E, Snyder AZ, McKinstry RC, Raichle ME, Conturo TE (1997) Anatomic localization and quantitative analysis of gradient refocused echo-planar fMRI susceptibility artifacts. NeuroImage 6:156–167

  6. 6.

    Jesmanowicz A, Biswal BB, Hyde JS (1999) Reduction in GR-EPI intravoxel dephasing using thin slices and short TE. In: Proceedings of the ISMRM scientific meeting, Philadelphia, p 1619

  7. 7.

    Bellgowan PS, Bandettini PA, van Gelderen P, Martin A, Bodurka J (2006) Improved BOLD detection in the medial temporal region using parallel imaging and voxel volume reduction. NeuroImage 29(4):1244–1251

  8. 8.

    Robinson SD, Pripfl J, Bauer H, Moser E (2008) The impact of EPI voxel size on SNR and BOLD sensitivity in the anterior medio-temporal lobe: a comparative group study of deactivation of the default mode. Magn Reson Mater Phy 21(4):279–290

  9. 9.

    Deichmann R, Gottfried JA, Hutton C, Turner R (2003) Optimized EPI for fMRI studies of the orbitofrontal cortex. NeuroImage 19(2):430–441

  10. 10.

    Frahm J, Klaus-Dietmar M, Wolfgang H (1995) The effects of intravoxel dephasing and incomplete slice refocusing on susceptibility contrast in gradient-echo MRI. J Magn Reson 109(2):234–237

  11. 11.

    Constable RT (1995) Functional MR imaging using gradient-echo echo-planar imaging in the presence of large static field inhomogeneities. J Magn Reson Imaging 5(6):746–752

  12. 12.

    Constable RT, Carpentier A, Pugh K, Westerveld M, Oszunar Y, Spencer DD (2000) Investigation of the human hippocampal formation using a randomized event-related paradigm and z-shimmed functional MRI. NeuroImage 12(1):55–62

  13. 13.

    Constable RT, Spencer DD (1999) Composite image formation in z-shimmed functional MR imaging. Magn Reson Med 42:110–117

  14. 14.

    Cordes D, Turski PA, Sorenson JA (2000) Compensation of susceptibility-induced signal loss in echo-planar imaging for functional applications. Magn Reson Imaging 18(9):1055–1068

  15. 15.

    Weiskopf N, Hutton C, Josephs O, Deichmann R (2006) Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: a whole-brain analysis at 3 T and 1.5 T. NeuroImage 33(2):493–504

  16. 16.

    Cho ZH, Ro YM (1992) Reduction of susceptibility artifact in gradient-echo imaging. Magn Reson Med 23:193–200

  17. 17.

    Chung JY, Yoon HW, Kim YB, Park HW, Cho ZH (2009) Susceptibility compensated fMRI study using a tailored RF echo planar imaging sequence. J Magn Reson Imaging 29(1):221–228

  18. 18.

    Wastling S, Barker GJ (2014) Designing hyperbolic secant excitation pulses to reduce signal dropout in gradient-echo echo-planar imaging. Mag Reson Med 74(3):661–672

  19. 19.

    Triantafyllou C, Hoge RD, Krueger G, Wiggins CJ, Potthast A, Wiggins GC, Wald LL (2005) Comparison of physiological noise at 1.5, 3 and 7 T and optimization of fMRI acquisition parameters. NeuroImage 26(1):243–250

  20. 20.

    van der Zwaag W, Francis S, Head K, Peters A, Gowland P, Morris P, Bowtell R (2009) fMRI at 1.5, 3 and 7 T: characterising BOLD signal changes. NeuroImage 47(4):1425–1434

  21. 21.

    Beisteiner R, Robinson S, Wurnig M, Hilbert M, Merksa K, Rath J et al (2011) Clinical fMRI: evidence for a 7 T benefit over 3T. NeuroImage 57(3):1015–1021

  22. 22.

    Rua C, Costagli M, Symms MR, Biagi L, Donatelli G, Cosottini M, Del Guerra A, Tosetti M (2017) Characterization of high-resolution gradient echo and spin echo EPI for fMRI in the human visual cortex at 7T. Magn Reson Imaging 40:98–108

  23. 23.

    Robitaille PM, Berliner L (2007) Ultra high field magnetic resonance imaging, vol 26. Springer US, New York

  24. 24.

    Farzaneh F, Riederer SJ, Pelc NJ (1990) Analysis of T2 limitations and off-resonance effects on spatial resolution and artifacts in echo-planar imaging. Magn Reson Med 14(1):123–139

  25. 25.

    Moser E, Stahlberg F, Ladd ME, Trattnig S (2012) 7-T MR—from research to clinical applications? NMR Biomed 25(5):695–716

  26. 26.

    Rua C, Wastling SJ, Costagli M, Biagi L, Symms MR, Del Guerra A, Cosottini M, Tosetti M, Barker GJ (2015) Demonstration of recovery of signal loss at 7T in gradient echo EPI using tailored-RF pulses. In: Proceedings of the ISMRM scientific meeting, Toronto, p 3917

  27. 27.

    De Renzi E, Perani D, Carlesimo GA, Silveri MC, Fazio F (1994) Prosopagnosia can be associated with damage confined to the right hemisphere—an MRI and PET study and a review of the literature. Neuropsychol 32:893–902

  28. 28.

    Puce A, Allison T, Asgari M, Gore JC, McCarthy G (1996) Differential sensitivity of human visual cortex to faces, letterings, and textures: a functional magnetic resonance imaging study. J Neurosci 16:5205–5215

  29. 29.

    Kanwisher N, McDermott J, Chun MM (1997) The Fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17(11):4302–4311

  30. 30.

    Haxby JV, Hoffman EA, Gobbini MI (2000) The distributed human neural system for face perception. Trends Neurosci 4(6):223–233

  31. 31.

    Rossion B, Caldara R, Seghier M, Schuller A-M, Lazeyras F, Mayer E (2003) A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 126:2381–2395

  32. 32.

    Pitcher D, Walsh V, Duchaine B (2011) The role of the occipital face area in the cortical face perception network. Exp Brain Res 209:481–493

  33. 33.

    Grill-Spector K, Kushnir T, Edelman S, Avidan G, Itzchak Y, Malach R (1999) Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron 24(1):187–203

  34. 34.

    Grill-Spector K, Kanwisher N (2005) Visual Recognition: as soon as you know it is there, you know what it is. Psychol Sci 16(2):152–160

  35. 35.

    Kourtzi Z, Kanwisher N (2001) Representation of perceived object shape by the human lateral occipital complex. Science 293(5534):1506–1509

  36. 36.

    Wright P, Mougin O, Totman J, Peters A, Brookes M, Coxon R, Morris P, Clemence M, Francis S, Bowtell R, Gowland P (2008) Water proton T1 measurements in brain tissue at 7, 3, and 1.5 T using IR-EPI, IR-TSE, and MPRAGE: results and optimization. Magn Reson Mater Phy 21:121–130

  37. 37.

    Yacoub E, Duong TQ, De Moortele V, Lindquist M, Adriany G, Kim SG, Uğurbil K, Hu X (2003) Spin-echo fMRI in humans using high spatial resolutions and high magnetic fields. Magn Reson Med 49(4):655–664

  38. 38.

    Jenkinson M, Bannister P, Brady JM, Smith SM (2002) Improved optimisation for the Robust and accurate linear registration and motion correction of brain images. NeuroImage 17(2):825–841

  39. 39.

    Sergent J, Ohta S, Macdonald B (1992) Functional neuroanatomy of face and object processing—a positron emission tomography study. Brain 115:15–36

  40. 40.

    Gauthier I, Tarr MJ, Moylan J, Skudlarski P, Gore JC, Anderson AW (2000) The fusiform “face area” is part of a network that processes faces at the individual level. J Cogn Neurosci 12(3):495–504

  41. 41.

    Çukur T, Huth AG, Nishimoto S, Gallant JL (2013) Functional subdomains within FFA. J Neurosci 33:16748–16766

  42. 42.

    Rajimehr R, Young JC, Tootell RB (2009) An anterior temporal face patch in human cortex predicted my macaque maps. Proc Nat Acad Sci USA 106:1995–2000

  43. 43.

    Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Gannister PR, De Luca M et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23(S1):208–219

  44. 44.

    Worsley KJ (2001) Statistical analysis of activation images. In: Matthews PM, Smith SM, Jezzard P (eds) Functional MRI: an introduction to methods. Oxford University Press, Oxford, pp 251–270

  45. 45.

    Andersson JLR, Skare S, Ashburner J (2003) How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. NeuroImage 20:870–888

  46. 46.

    Greve DN, Fischl B (2009) Accurate and robust brain image alignment using boundary-based registration. NeuroImage 48(1):63–72

  47. 47.

    Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Human BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31:968–980

  48. 48.

    Kriegeskorte N, Formisano E, Sorger B, Goebel R (2007) Individual faces elicit distinct response patterns in human anterior temporal cortex. Proc Natl Acad Sci USA 104(51):20600–20605

  49. 49.

    Yang H, Susilo T, Duchaine B (2014) The anterior temporal face area contains invariant representations of face identity that can persist despite the loss of right FFA and OFA. Cereb Cortex 26(3):1096–1107

  50. 50.

    Nasr S, Tootell RBH (2012) Role of fusiform and anterior temporal cortical areas in facial recognition. NeuroImage 63(3):1743–1753

  51. 51.

    Uddin LQ, Kaplan JT, Molnar-Szakacs I, Zaidel E, Iacoboni M (2005) Self-face recognition activates a frontoparietal “mirror” network in the right hemisphere: an event-related fMRI study. NeuroImage 25:926–935

  52. 52.

    Robert Powell HW, Koepp MJ, Richardson MP, Symms MR, Thompson PJ, Duncan JS (2004) The application of functional MRI of memory in temporal lobe epilepsy: a clinical review. Epilepsia 45(7):855–863

  53. 53.

    Benke T, Köylü B, Visani P, Karner E, Brenneis C, Bartha L et al (2006) Language lateralization in temporal lobe epilepsy: a comparison between fMRI and the Wada Test. Epilepsia 47(8):1308–1319

  54. 54.

    Devlin JT, Russell RP, Davis MH, Price CJ, Wilson J, Moss HE, Matthews PM, Tyler LK (2000) Susceptibility induced loss of signal: comparing PET and fMRI on a semantic task. NeuroImage 11:589–600

  55. 55.

    Carr VA, Rissman J, Wagner AD (2010) Imaging the human medial temporal lobe with high-resolution fMRI. Neuron 65(3):298–308

  56. 56.

    Bonelli SB, Powell RH, Yogarajah M, Samson RS, Symms MR, Thompson PJ, Koepp MJ, Duncan JS (2010) Imaging memory in temporal lobe epilepsy: predicting the effects of temporal lobe resection. Brain 133(4):1186–1199

Download references

Acknowledgements

This work was supported by the Initial Training Network, HiMR, funded by the FP7 Marie Curie Actions of the European Commission (FP7-PEOPLE-2012-ITN-316716).

Author information

CR Project development, data collection and data analysis. SJW Project development and data collection. MC Project development, data collection and data analysis. MRS Project development, data collection and data analysis. LB Project development and data collection. MC Project development and data management. ADG Project development. MT Project development and data management. GJB Project development and data management.

Correspondence to Mauro Costagli.

Ethics declarations

Funding

CR was supported by the Initial Training Network, HiMR, funded by the FP7 Marie Curie Actions of the European Commission (FP7-PEOPLE-2012-ITN-316716).

Conflict of interest

MRS is employed by General Electric Healthcare. GJB receives honoraria for teaching from General Electric Healthcare, who also part fund a PhD studentship. GJB acts as a consultant for IXICO.

Human rights

All procedures involving human participants were in accordance with the ethical standards of the competent ethics committee and with the 1964 Helsinki declaration and its later amendments.

Informed consent

Written informed consent was obtained from all individual participants included in the study.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 289 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rua, C., Wastling, S.J., Costagli, M. et al. Improving fMRI in signal drop-out regions at 7 T by using tailored radio-frequency pulses: application to the ventral occipito-temporal cortex. Magn Reson Mater Phy 31, 257–267 (2018). https://doi.org/10.1007/s10334-017-0652-x

Download citation

Keywords

  • Functional MRI
  • Ultra high field
  • Tailored radio-frequency pulse
  • Signal drop-out recovery