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High-resolution mapping of iso-orientation columns by fMRI

Nature Neuroscience volume 3, pages 164–169 (2000)Cite this article

Abstract

Blood-oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) is an important tool for localizing brain functions in vivo . However, the ability of BOLD fMRI to map cortical columnar structures is highly controversial, as the ultimate functional specificity of BOLD remains unknown. Here we report a biphasic BOLD response to visual stimulation in the primary visual cortex of cats. In functional imaging, the initial BOLD signal decrease accurately labeled individual iso-orientation columns. In contrast, the delayed positive BOLD changes indicated the pattern of overall activation in the visual cortex, but were less suited to discriminate active from inactive columns.

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Figure 1: Improvement of spatial specificity of BOLD using the initial negative signal changes.
Figure 2: Representation of orthogonal orientations in complementary cortical domains.
Figure 3: Representation of orthogonal orientations of positive BOLD maps.
Figure 4: fMRI-based composite angle maps.

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References

  1. Brodmann, K. Vergleichende Lokalisationslehre der Grosshirnrinde (Johann Ambrosius Barth, Leipzig, 1909).

  2. Hubel, D. H. & Wiesel, T. N. Receptve field, binocular interactions and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 ( 1962).

    Article  CAS  Google Scholar 

  3. LeVay, S., Stryker, M. P. & Shatz, C. J. Ocular dominance columns and their development in layer IV of cat's visual cortex. J. Comp. Neurol. 179 , 223–244 (1978).

    Article  CAS  Google Scholar 

  4. LeVay, S. & Nelson, S. B. Vision and Visual Dysfunction 266–315 (Macmillan, Houndsmill, 1991).

  5. Sokoloff, L. et al. The 14C-deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J. Neurochem. 28, 897–916 (1977).

    Article  CAS  Google Scholar 

  6. Grinvald, A., Lieke, E., Frostig, R. D., Gilbert, C. D. & Wiesel, T. N. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324, 361–364 (1986).

    Article  CAS  Google Scholar 

  7. Ts'o, D. Y., Frostig, R. D., Lieke, E. E. & Grinvald, A. Functional organization of primate visual cortex revealed by high resolution optical imaging. Science 249, 417– 420 (1990).

    Article  CAS  Google Scholar 

  8. Frostig, R. D., Lieke, E. E., Ts'o, D. Y. & Grinvald, A. 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 (1990).

    Article  CAS  Google Scholar 

  9. Bonhoeffer, T. & Grinvald, A. The layout of iso-orientation domains in area 18 of cat visual cortex: optical imaging reveals a pinwheel-like organization . J. Neurosci. 13, 4157– 4180 (1993).

    Article  CAS  Google Scholar 

  10. Stetter, M. & Obemayer K. Simulation of scanning laser technique for optical imaging of blood-related intrinsic signals. J. Opt. Soc. Am. A 16, 58–70 ( 1999).

    Article  CAS  Google Scholar 

  11. Ogawa, S. et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc. Natl. Acad. Sci. USA 89, 5951–5955 ( 1992).

    Article  CAS  Google Scholar 

  12. Kwong, K. K. et al. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc. Natl. Acad. Sci. USA 89, 5675–5679 ( 1992).

    Article  CAS  Google Scholar 

  13. Loewel, S. & Singer, W. Tangential intracortical pathways and the development of iso-orientation bands in cat striate cortex. Dev. Brain Res. 56, 99–115 (1990).

    Article  Google Scholar 

  14. Fox, P. T. & Raichle, M. E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl. Acad. Sci. USA 83, 1140–1144 (1986).

    Article  CAS  Google Scholar 

  15. Posner, M. I. & Raichle, M. E. Images of Mind (Freeman, New York, 1994).

  16. Wagner, A. D. et al. Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 281, 1188–1191 (1998).

    Article  CAS  Google Scholar 

  17. Kim, S.-G. et al. Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. Science 261, 615 –617 (1993).

    Article  CAS  Google Scholar 

  18. DeYoe, E. A. et al. Mapping striate and extrastriate visual areas in human cerebral cortex. Proc. Natl. Acad. Sci. USA 93, 2382 –2386 (1996).

    Article  CAS  Google Scholar 

  19. Sereno, M. I. et al. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268, 889–893 (1995).

    Article  CAS  Google Scholar 

  20. Tootell, R. B. et al. Functional analysis of V3A and related areas in monkey visual cortex. J. Neurosci. 17, 7070– 7078 (1997).

    Article  Google Scholar 

  21. Engel, A. S., Glover, G. H. & Wandell, B. A. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb. Cortex 7, 181–192 (1997).

    Article  CAS  Google Scholar 

  22. Malonek, D. & Grinvald, A. Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: Implication for functional brain mapping. Science 272, 551–554 (1996).

    Article  CAS  Google Scholar 

  23. Malonek, D. et al. Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. Proc. Natl. Acad. Sci. USA 94, 14826–14831 (1997).

    Article  CAS  Google Scholar 

  24. Ernst, T. & Henning, J. Observation of a fast response in functional MR. Magn. Reson. Med. 32, 146 –149 (1994).

    Article  CAS  Google Scholar 

  25. Menon, R. S. et al. BOLD based functional MRI at 4 Tesla includes a capillary bed contribution: Echo planar imaging correlates with previous optical imaging using intrinsic signals. Magn. Reson. Med. 33, 453–459 (1995).

    Article  CAS  Google Scholar 

  26. Hu, X., Le, T. H. & Ugurbil, K. Evaluation of the early response in fMRI in individual subjects using short stimulus duration. Magn. Reson. Med. 37, 877–884 (1997).

    Article  CAS  Google Scholar 

  27. Marota, J. J. A. et al. Investigation of the early response to rat forepaw stimulation . Magn. Reson. Med. 41, 247– 252 (1999).

    Article  CAS  Google Scholar 

  28. Silva, A. C., Lee, S.-P., Iadecola, C. & Kim, S.-G. Early characteristics of CBF and deoxyhemoglobin changes during somatosensory stimulation. J. Cereb. Blood Flow Metab. 20, 201– 206 (2000).

    Article  CAS  Google Scholar 

  29. Movshon, J. A., Thompson, I. D. & Tolhurst, D. J. Spatial and temporal contrast sensitivity of neurons in areas 17 and 18 of the cat's visual cortex. J. Physiol. (Lond.) 283, 101–120 ( 1978).

    Article  CAS  Google Scholar 

  30. Loewel, S., Freeman, B. & Singer, W. Topographic organization of the orientation column system in large, flat-mounts of the cat visual cortex: A 2-deoxyglucose study. J. Comp. Neurol. 255, 401–415 (1987).

    Article  Google Scholar 

  31. Jezzard, P., Rauschecker, J. P. & Malonek, D. An in vivo model for functional MRI in cat visual cortex. Magn. Reson. Med. 38, 699– 705 (1997).

    Article  CAS  Google Scholar 

  32. Bonhoeffer, T. & Grinvald, A. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like pattern. Nature 353, 429–432 ( 1991).

    Article  CAS  Google Scholar 

  33. Kim, D.-S. & Bonhoeffer, T. Reverse occlusion leads to a precise restoration of orientation preference maps in visual cortex. Nature 370, 370–372 ( 1994).

    Article  CAS  Google Scholar 

  34. Swindale, N. W Matsubara, J. A. & Cynader, M. S. Surface organization of orientation and direction selectivity in cat area 18. J. Neurosci. 7, 1414–1427 (1987).

    Article  CAS  Google Scholar 

  35. Diao, Y. C., Jia, W. G., Swindale, N. V. & Cynader, M. S. Functional organization of the cortical 17 per 18 border region in the cat . Exp. Brain Res. 79, 271– 282 (1990).

    Article  CAS  Google Scholar 

  36. Maldonado, P. E., Goedecke, I., Gray, C. M. & Bonhoeffer, T. Orientation selectivity in pinwheel centers in cat visual cortex. Science 276, 1551–1555 ( 1997).

    Article  CAS  Google Scholar 

  37. Shmuel, A. & Grinvald, A. Functional organization for direction of motion and its relationship to orientation maps in cat area 18. J. Neurosci. 16, 6945–6964 (1996).

    Article  CAS  Google Scholar 

  38. Crair, M. C., Gillespie, D. C. & Stryker, M. P. The role of visual experience in the development of columns in cat visual cortex. Science 279, 566–570 (1998).

    Article  CAS  Google Scholar 

  39. Rojer, A. S. & Schwartz, E. L. Cat and monkey cortical columnar patterns modeled by bandpass-filtered 2D white noise. Biol. Cybern. 62, 381–391 ( 1990).

    Article  CAS  Google Scholar 

  40. Blasdel, G. G. Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex. J. Neurosci. 12, 3115– 3138 (1992).

    Article  CAS  Google Scholar 

  41. Menon, R. S., Ogawa, S. Strupp, J. P. & Ugurbil, K. Ocular dominance in human V1 demonstrated by functional magnetic resonance imaging. J. Neurophysiol. 77, 2780–2787 (1997).

    Article  CAS  Google Scholar 

  42. Ogawa, S., Menon, R. S., Kim, S.-G. & Ugurbil, K. On the characterizatics of functional magnetic resonance imaging of the brain. Annu. Rev. Biophys. Biomol. Struct. 27, 447–474 (1998).

    Article  CAS  Google Scholar 

  43. Janz, C., Speck, O. & Henning, J. Time-resolved measurements of brain activation after a short visual stimulus: new results on the physiological mechanisms of the cortical response. NMR Biomed. 10, 222– 229 (1997).

    Article  CAS  Google Scholar 

  44. Vanzetta, I. & Grinvald, A. Increased cortical oxidative metabolism due to sensory stimulation: implications for functional brain imaging. Science 286, 1555–1558 ( 1999).

    Article  CAS  Google Scholar 

  45. Yacoub, E. & Hu, X. Detection of the early negative response in fMRI at 1.5 Tesla. Magn. Reson. Med. 41, 1088–1092 (1999).

    Article  CAS  Google Scholar 

  46. Logothetis, N. K., Guggenberger, H., Peled, S. & Pauls, J. Functional imaging of the monkey brain. Nat. Neurosci. 2, 555–562 (1999).

    Article  CAS  Google Scholar 

  47. Forman, S. D. et al. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn. Reson. Med. 33, 636–647 (1995).

    Article  CAS  Google Scholar 

  48. Press, W. H., Teukolsky, S. A., Vetterling, W. T. & Flannery, B.P. Numerical Recipes in C (Cambridge, UK, 1992).

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Acknowledgements

We thank K. Ugurbil for continuing support of our project and S. Ogawa, A. Grinvald, R.B. Tootell, J. Ashe and A. P. Georgopoulos for suggestions and comments. H. Merkle and J. Strupp provided support in hardware and software. This work was supported by the NIH (NS38295, MH57180, NS10930, RR08079), the Minnesota Medical Foundation and the Keck Foundation.

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  1. Center for Magnetic Resonance Research, University of Minnesota Medical School, 2021 6th Street S.E., Minneapolis, 55455, Minnesota, USA

    Dae-Shik Kim, Timothy Q. Duong & Seong-Gi Kim

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Correspondence to Seong-Gi Kim.

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Kim, DS., Duong, T. & Kim, SG. High-resolution mapping of iso-orientation columns by fMRI. Nat Neurosci 3, 164–169 (2000). https://doi.org/10.1038/72109

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