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. 1998 Dec 7;6(4):203–215. doi: 10.1002/(SICI)1097-0193(1998)6:4<203::AID-HBM2>3.0.CO;2-7

Functional MRI studies of word‐stem completion: Reliability across laboratories and comparison to blood flow imaging with PET

Jeffrey G Ojemann 1,✉, Randy L Buckner 2,3,4,5, Erbil Akbudak 4,6, Abraham Z Snyder 4, John M Ollinger 4,7, Robert C Mckinstry 4, Bruce R Rosen 5, Steve E Petersen 1,2,3,4,8, Marcus E Raichle 1,2,4,8, Thomas E Conturo 4,6
PMCID: PMC6873367  PMID: 9704261

Abstract

Functional magnetic resonance imaging (fMRI) based on blood oxygen level‐dependent (BOLD) contrast has become an increasingly popular technique for mapping the brain. The relationship between BOLD‐fMRI imaging and imaging of blood flow activation with positron emission tomography (PET) remains unclear. Moreover, BOLD imaging strategies and analysis procedures vary widely across laboratories. To examine the relationship between these different methods, we compared brain activation maps of a word‐stem completion task obtained both using PET and using fMRI across two separate institutions (Washington University and Massachusetts General Hospital) with different acquisitions (gradient‐refocused echo and asymmetric spin echo) and different analysis techniques. Overall, activation maps were highly similar across both fMRI methods and PET. A set of activated brain areas, in consistent locations in Talairach atlas space, were identified across all three studies, including visual striate and extrastriate, left prefrontal, supplementary motor area (SMA), and right cerebellar areas. Decreases in activation were also consistently observed in medial parietal, posterior insular, and medial inferior frontal areas. Some differences were noted that may be related to the silent performance of the task with fMRI. The largely consistent results suggest that comparisons can be made appropriately across imaging modalities and laboratory methods. A further implication of the consistencies, which extended to both increases and decreases in signal, is that the underlying brain physiology leading to BOLD contrast may be more similar to blood flow than originally appreciated. Hum. Brain Mapping 6:203–215, 1998. © 1998 Wiley‐Liss, Inc.

Keywords: BOLD, cerebral blood flow, cerebral oxygen metabolism, cognition, imaging methods

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References

  1. Baker JR, Hoppel BE, Stern CE, Kwong KK, Weisskoff RM, Rosen BR (1993): Dynamic functional imaging of the complete human cortex using gradient‐echo and asymmetric spin‐echo echoplanar magnetic resonance imaging. Proc Soc Magn Reson Abstr, First annual meeting, p 1400.
  2. Bandettini PA, Wong EC, Hinks RS, Tikofsky RS, Hyde JS (1992): Time course EPI of human brain function during task activation. Magn Reson Med 25: 390–397. [DOI] [PubMed] [Google Scholar]
  3. Binder JR, Rao SM, Hammeke TA, Frost JA, Bandettini PA, Jesmanowicz A, Hyde JS (1995): Lateralized human brain language systems demonstrated by task subtraction functional magnetic resonance imaging. Arch Neurol 52: 593–601. [DOI] [PubMed] [Google Scholar]
  4. Birn RM, Bandettini PA, Jesmanowicz A, Shaker R, Cox RW (1997): BZ‐field changes in the brain due to speaking and swallowing. Proc Int Soc Magn Reson Med, 5th annual meeting, p 458. [DOI] [PubMed]
  5. Boxerman JL, Bandettini PA, Kwong DD, Baker JR, Davis TL, Rosen BR, Weisskoff RM (1995): The intravascular contribuion to fMRI signal change: Monte‐Carlo modeling and diffusion‐weighted studies in vivo. Magn Reson Med 34: 4–10. [DOI] [PubMed] [Google Scholar]
  6. Buckner RL, Petersen SE, Ojemann JG, Miezin FM, Squire LR, Raichle ME (1995): Functional anatomical studies of explicit and implicit memory retrieval tasks. J Neurosci 15: 12–29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Buckner RL, Bandettini PA, O'Craven KM, Savoy RL, Petersen SE, Raichle ME, Rosen BR (1996a): Detection of cortical activation during averaged single trials of a cognitive task using functional magnetic resonance imaging. Proc Natl Acad Sci USA 93: 14878–14883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Buckner RL, Raichle ME, Miezin FM, Petersen SE (1996b): Functional anatomic studies of memory retrieval for auditory words and visual pictures. J Neurosci 16: 6219–6235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Buxton RB, Frank LR (1997): A model for the coupling between cerebral blood flow and oxygen metabolism during neural stimulation. J Cereb Blood Flow Metab 17: 64–72. [DOI] [PubMed] [Google Scholar]
  10. Clark VP, Keil K, Maisog JMA, Courtney S, Ungerleider LG, Haxby JV (1996): Functional magnetic resonance imaging of human visual cortex during face matching: A comparison with positron emission tomography. Neuroimage 4: 1–15. [DOI] [PubMed] [Google Scholar]
  11. Coghill RC, Talbot JD, Evans AC, Meyer E, Gjedde A, Bushnell MC, Duncan GH (1994): Distributed processing of pain and vibration by the human brain. J Neurosci 14: 4095–4106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Collins LD, Neelin P, Peters TM, Evans AC (1994): Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr 18: 192–205. [PubMed] [Google Scholar]
  13. Conturo TE, McKinstry RC, Akbudak E, Snyder AZ, Yang TZ, Raichle ME (1996): Sensitivity optimization and experimental design in functional magnetic resonance imaging. Soc Neurosci Abstr 22: 7. [Google Scholar]
  14. Cuenod CA, Bookheimer SY, Hertz‐Pannier L, Zeffiro TA, Theodore WH, Le Bihen D (1995): Functional MRI during word generation, using conventional equipment. Neurology 45: 1821–1827. [DOI] [PubMed] [Google Scholar]
  15. Desmond JE, Sum JM, Wagner AD, Demb JB, Shear PK, Glover GH, Gabrieli JDE, Morrell MJ (1995): Functional MRI measurement of language lateralization in Wada‐tested patients. Brain 118: 1411–1419. [DOI] [PubMed] [Google Scholar]
  16. Fiez JA, Petersen SE, Cheney MK, Raichle ME (1992): Impaired non‐motor learning and error detection associated with cerebellar damage: Asingle case study. Brain 115: 155–178. [DOI] [PubMed] [Google Scholar]
  17. Fiez JA, Raichle ME, Miezin FM, Petersen SE, Tallal P, Katz WF (1995): PET studies of auditory and phonological processing: Effects of stimulus characteristics and task demands. J Cogn Neurosci 7: 357–375. [DOI] [PubMed] [Google Scholar]
  18. Fox PT, Raichle ME (1986): Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc Natl Acad Sci USA 83: 1140–1144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fox PT, Perlmutter JS, Raichle ME (1985): A stereotactic method of anatomical localization for positron emission tomography. J Comput Assist Tomogr 9: 141–153. [DOI] [PubMed] [Google Scholar]
  20. Fox PT, Miezin FM, Allman JM, Van Essen DC, Raichle ME (1987): Retinotopic organization of human visual cortex mapped with positron‐emission tomography. J Neurosci 7: 913–922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fox PT, Raichle ME, Mintun MA, Dence C (1988): Nonoxidative glucose consumption during focal physiologic neural activity. Science 241: 462–464. [DOI] [PubMed] [Google Scholar]
  22. Frahm J, Merboldt K‐D, Hänicke W (1988): Direct FLASH MR imaging of magnetic field inhomogeneities by gradient compensation. Magn Reson Med 6: 474–480. [DOI] [PubMed] [Google Scholar]
  23. Frahm J, Merboldt K‐D, Hänicke W, Kleinschmidt A, Boecker H (1994): Brain or vein—Oxygenation or flow? On signal physiology in functional MRI of human brain activation. NMR Biomed 7: 45–53. [DOI] [PubMed] [Google Scholar]
  24. Fried I, Nenov VI, Ojemann SG, Woods RW (1995): Functional MR and PET imaging of Rolandic and visual cortices for neurosurgical planning. J Neurosurg 83: 854–861. [DOI] [PubMed] [Google Scholar]
  25. Friston KJ, Jezzard P, Turner R (1994): Analysis of functional MRI time‐series. Hum Brain Mapp 1: 153–171. [Google Scholar]
  26. Frostig RD, Lieke EE, Ts'o DY, Grinvald A (1990): Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high‐resolution optical imaging of intrinsic signals. Proc Natl Acad Sci USA 87: 6082–6086. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hajnal JV, Saeed N, Soar EJ, Oatridge A, Young IR, Bydder GM (1995): A registration and interpolation procedure for subvoxel matching of serially acquired MR images. J Comput Assist Tomogr 19: 289–296. [DOI] [PubMed] [Google Scholar]
  28. Hunton DL, Miezin FM, Buckner RL, van Mier HI, Raichle ME, Petersen SE (1996): An assessment of functional‐anatomical variability in neuroimaging studies. Hum Brain Mapp 4: 122–139. [DOI] [PubMed] [Google Scholar]
  29. Kraut MA, Marenco S, Soher BJ, Wong DF, Bryan RN (1995): Comparions of functional MR and H2‐15O positron emission tomography in stimulation of the primary visual cortex. AJNR 16: 2101–2107. [PMC free article] [PubMed] [Google Scholar]
  30. Kucera H, Francis WN (1967): Computational Analysis of Present‐Day American English, Providence, RI: Brown University Press. [Google Scholar]
  31. Kwong KK, Belliveau JW, Chesler DA, Goldberg IE, Weisskoff RM, Poncelet BP, Kennedy DN, Hoppel BE, Cohen MS, Turner R, Cheng H‐M, Brady TJ, Rosen BR (1992): Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci USA 89: 5675–5679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lancaster JL, Glass TG, Lankipalli BR, Downs H, Mayberg H, Fox PT (1995): A modality‐independent approach to spatial normalization of tomographic images of the human brain. Hum Brain Mapp 3: 209–223. [Google Scholar]
  33. Maldjian J, Atlas SW, Howard RS, Greenstein E, Alsop D, Detre JA, Listerud J, D'Esposito M, Flamm ES (1996): Functional magnetic resonance imaging of regional brain activity in patients with intracerebral arteriovenous malformations before surgical or endovascular therapy. J Neurosurg 84: 477–483. [DOI] [PubMed] [Google Scholar]
  34. Malonek D, Grinvald A (1996): Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science 272: 551–554. [DOI] [PubMed] [Google Scholar]
  35. McCarthy G, Blamire AM, Rothman DL, Gruetter R, Shulman RG (1993): Echo‐planar magnetic resonance imaging studies of frontal cortex activation during word generation in humans. Proc Natl Acad Sci USA 90: 4952–4956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mugler JP III, Brookeman JR (1990): Three‐dimensional magnetization‐prepared rapid gradient‐echo imaging (3D MP‐RAGE). Magn Reson Med 15: 152–157. [DOI] [PubMed] [Google Scholar]
  37. Ogawa S, Lee TM, Naycik AS, Glynn P (1990): Oxygenation‐sensitive contrast in magnetic resonance imaging of rodent brain at high magnetic fields. Magn Reson Med 14: 68–78. [DOI] [PubMed] [Google Scholar]
  38. Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, Ugurbil K (1992): Intrinsic signal changes accompanying sensory stimulation. Proc Natl Acad Sci USA 89: 5951–5955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ojemann GA (1975): Language and the thalamus: Object naming and recall during and after thalamic stimuation. Brain Lang 2: 101–120. [DOI] [PubMed] [Google Scholar]
  40. Ojemann JG, Akbudak E, Snyder AZ, McKinstry RC, Raichle ME, Conturo TE (1997): Anatomic localiztion and quantitative analysis of gradient refocused echo‐planar fMRI susceptibility artifacts. Neuroimage 6: 156–167. [DOI] [PubMed] [Google Scholar]
  41. Ollinger JM (1997): Correcting for multiple comparisons in fMRI activation studies with region‐size dependent thresholds. Proc Inte Soc Magn Reson Med Abstr, 5th annual meeting, p 672.
  42. Paulesu E, Connelly A, Frith CD, Friston KJ, Heather J, Myers R, Gadian DG, Frackowiak RSJ (1995): Functional MR imaging correlations with positron emission tomography. Neuroimaging Clin North Am 5: 207–225. [PubMed] [Google Scholar]
  43. Petersen SE, Fox PT, Posner MI, Mintun M, Raichle ME (1988): Positron emission tomorgraphic studies of the cortical anatomy of single‐word processing. Nature 331: 585–589. [DOI] [PubMed] [Google Scholar]
  44. Petersen SE, Fox PT, Posner MI, Mintun M, Raichle ME (1989): Positron emission tomographic studies of the processing of single words. J Cogn Neurosci 1: 153–170. [DOI] [PubMed] [Google Scholar]
  45. Picard N, Strick P (1996): Motor areas of the medial wall: Areview of their location and functional activation. Cereb Cortex 6: 342–353. [DOI] [PubMed] [Google Scholar]
  46. Press WH, Flanner BP, Teukolsky SA, Veterling WT (1988): Numerical Recipes in C: The Art of Scientific Computing, New York: Cambridge University Press. [Google Scholar]
  47. Raichle ME (1987): Circulatory and metabolic correlates of brain function in normal humans In: Plum F, Mountcastle V. (eds): Handbook of Physiology–The Nervous System V, Higher Brain Functions. Bethesda, MD: American Physiological Society, pp 643–674. [Google Scholar]
  48. Raichle ME, Grubb RL Jr, Gado MH, Eichling JO, Ter‐Pogossian MM (1976): Correlation between regional cerebral blood flow and oxidative metabolism. Arch Neurol 33: 523–526. [DOI] [PubMed] [Google Scholar]
  49. Raichle ME, Fiez JA, Videen TO, MacLeod AK, Pardo JV, Fox PT, Petersen SE (1994): Practice‐related changes in human brain functional anatomy during nonmotor learning. Cereb Cortex 4: 8–26. [DOI] [PubMed] [Google Scholar]
  50. Ramsey NF, Kirkby BS, Van Gelderen P, Berman KF, Duyn JH, Frank JA, Mattay VS, Van Horn JD, Esposito G, Moonen CTW, Weinberger DR (1996): Functional mapping of human sensorimotor cortex with 3D BOLD fMRI correlates highly with H2 15O PET rCBF. J Cereb Blood Flow Metab 16: 755–764. [DOI] [PubMed] [Google Scholar]
  51. Reese TG, Davis TL, Weisskoff RM (1995): Automated shimming at 1.5 T using echo‐planar image frequency maps. J Magn Reson Imaging 5: 739–745. [DOI] [PubMed] [Google Scholar]
  52. Rosen HJ, Ojemann JG, Fiez JA, Raichle ME, Petersen SE (1997): Comparison of overt and silent verb generation. Soc Neurosci Abstr 23: 1054. [Google Scholar]
  53. Shulman GL, Fiez JA, Corbetta M, Buckner RL, Miezin FM, Raichle ME, Petersen SE (1997): Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. J Cogn Neurosci 9: 648–663. [DOI] [PubMed] [Google Scholar]
  54. Snyder AZ (1996): Difference image vs. ratio image error function forms in PET‐PET realignment In: Bailey D, Jones T. (eds): Quantification of Brain Function Using PET. San Diego: Academic Press, pp 131–137. [Google Scholar]
  55. Squire LR, Ojemann JG, Miezin FM, Petersen SE, Videen TO, Raichle ME (1992): Activation of the hippocampus in normal humans: A functional anatomical study of memory. Proc Natl Acad Sci USA 89: 1837–1841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Talairach J, Tournoux P (1988): Co‐Planar Stereotaxic Atlas of the Human Brain, New York: Thieme. [Google Scholar]
  57. Talairach J, Szikla G, Tournoux P (1967): Atlas d'Anatomie Stereotaxique du Telencephale, Paris: Masson. [Google Scholar]
  58. Wise R, Chollet F, Hadar U, Friston K, Hoffner E, Frackowiak R (1991): Distribution of cortical neural networks involved in word comprehension and word retrieval. Brain 114: 1803–1817. [DOI] [PubMed] [Google Scholar]
  59. Woods RP, Mazziotta JC, Cherry SR (1993): MRI‐PET registration with automated algorithm. J Comput Assist Tomogr 17: 536–546. [DOI] [PubMed] [Google Scholar]
  60. Yetkin FZ, Gammeke TA, Swanson SJ, Morris GL, Mueller WM, McAuliffe TL, Haughton VM (1995): A comparison of funcitonal MR activation patterns during silent and audible language tasks. AJNR 16: 1087–1092. [PMC free article] [PubMed] [Google Scholar]

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