Skip to content
Frontiers
Search

Neuroenergetics

Frontiers in Neuroenergetics ·

Volume 2 - 2010 | https://doi.org/10.3389/fnene.2010.00130

Recent Advances in High-Resolution MR Application and Its Implications for Neurovascular Coupling Research

  • Noam Harel1*corresponding author
  • Patrick J. Bolan1
  • Robert Turner2
  • Kamil Ugurbil1
  • Essa Yacoub1
  1. 11 Center for Magnetic Resonance Research, Department of Radiology, School of Medicine, University of Minnesota Minneapolis, MN, USA
  2. 22 Max Planck Institute for Human Cognitive and Brain Sciences Leipzig, Germany
Article metrics0 viewsView details
PDFCiteMetrics

Abstract

The current understanding of fMRI, regarding its vascular origins, is based on numerous assumptions and theoretical modeling, but little experimental validation exists to support or challenge these models. The known functional properties of cerebral vasculature are limited mainly to the large pial surface and the small capillary level vessels. However, a significant lack of knowledge exists regarding the cluster of intermediate-sized vessels, mainly the intracortical, connecting these two groups of vessels and where, arguably, key blood flow regulation takes place. In recent years, advances in MR technology and methodology have enabled the probing of the brain, both structurally and functionally, at resolutions and coverage not previously attainable. Functional MRI has been utilized to map functional units down to the levels of cortical columns and lamina. These capabilities open new possibilities for investigating neurovascular coupling and testing hypotheses regarding fundamental cerebral organization. Here, we summarize recent cutting-edge MR applications for studying neurovascular and functional imaging, both in humans as well as in animal models. In light of the described imaging capabilities, we put forward a theory in which a cortical column, an ensemble of neurons involved in a particular neuronal computation is spatially correlated with a specific vascular unit, i.e., a cluster of an emerging principle vein surrounded by a set of diving arteries. If indeed such a correlation between functional (neuronal) and structural (vascular) units exist as a fundamental intrinsic cortical feature, one could conceivably delineate functional domains in cortical areas that are not known or have not been identified.

Keywords

References

  1. Bartfeld E., Grinvald A. (1992). Relationships between orientation-preference pinwheels, cytochrome oxidase blobs, and ocular-dominance columns in primate striate cortex. Proc. Natl. Acad. Sci. U.S.A. 89, 11905 – 11909. doi:10.1073/pnas.89.24.11905
  2. Blasdel G. G. (1992). Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex. J. Neurosci. 12, 3115 – 3138.
  3. Blasdel G. G., Salama G. (1986). Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321, 579 – 585. doi:10.1038/321579a0
  4. Boas D. A., Jones S. R., Devor A., Huppert T. J., Dale A. M. (2008). A vascular anatomical network model of the spatio-temporal response to brain activation. Neuroimage 40, 1116 – 1129. doi:10.1016/j.neuroimage.2007.12.061
  5. Bolan P. J., Yacoub E., Garwood M., Ugurbil K., Harel N. (2006). In vivo micro-MRI of intracortical neurovasculature. Neuroimage 32, 62 – 69. doi:10.1016/j.neuroimage.2006.03.027
  6. Bonhoeffer T., Grinvald A. (1991). Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature 353, 429 – 431. doi:10.1038/353429a0
  7. Bonhoeffer T., Grinvald A. (1993). 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.
  8. Cheng K., Waggoner R. A., Tanaka K. (2001). Human ocular dominance columns as revealed by high-field functional magnetic resonance imaging. Neuron 32, 359 – 374. doi:10.1016/S0896-6273(01)00477-9
  9. Dechent P., Frahm J. (2000). Direct mapping of ocular dominance columns in human primary visual cortex. Neuroreport 11, 3247 – 3249. doi:10.1097/00001756-200009280-00039
  10. Duong T. Q., Kim D. S., Ugurbil K., Kim S. G. (2001). Localized cerebral blood flow response at submillimeter columnar resolution. Proc. Natl. Acad. Sci. U.S.A. 98, 10904 – 10909. doi:10.1073/pnas.191101098
  11. Duong T. Q., Yacoub E., Adriany G., Hu X., Ugurbil K., Kim S. G. (2003). Microvascular BOLD contribution at 4 and 7 T in the human brain: gradient-echo and spin-echo fMRI with suppression of blood effects. Magn. Reson. Med. 49, 1019 – 1027. doi:10.1002/mrm.10472
  12. Duvernoy H. M. (1991). The Human Brain: Surface, Three-Dimensional Sectional Anatomy and MRI. Wien, Austria: Springer-Verlag.
  13. Duvernoy H. M. (1999). Vascularization of the cerebral cortex. Rev. Neurol. (Paris) 155, 684 – 687.
  14. Duvernoy H. M., Delon S., Vannson J. L. (1981). Cortical blood vessels of the human brain. Brain Res. Bull. 7, 519 – 579. doi:10.1016/0361-9230(81)90007-1
  15. Feinberg D., Harel N., Ramanna S., Ugurbil K., Yacoub E. (2008). “Sub-millimeter single-shot 3D GRASE with inner volume selection for T2 weighted fMRI applications at 7 Tesla,” in Proceedings of the 16th Annual Meeting of the International Society for Magnetic Resonance in Medicine, Toronto, Abstract 2373.
  16. Fukuda M., Moon C. H., Wang P., Kim S. G. (2006). Mapping iso-orientation columns by contrast agent-enhanced functional magnetic resonance imaging: reproducibility, specificity, and evaluation by optical imaging of intrinsic signal. J. Neurosci. 26, 11821 – 11832. doi:10.1523/JNEUROSCI.3098-06.2006
  17. Goense J. B., Logothetis N. K. (2006). Laminar specificity in monkey V1 using high-resolution SE-fMRI. Magn. Reson. Imaging 24, 381 – 392. doi:10.1016/j.mri.2005.12.032
  18. Harel N., Lin J., Moeller S., Ugurbil K., Yacoub E. (2006). Combined imaging-histological study of cortical laminar specificity of fMRI signals. Neuroimage 29, 879 – 887. doi:10.1016/j.neuroimage.2005.08.016
  19. Harel N., Zhao Z., Wang P., Kim S. G. (2002). “Layer specificity of BOLD & CBV fMRI signals at ultra-high resolution,” in 8th International Conference on Functional Mapping of the Human Brain, Sendai Vol. 16, 1221 – 1223.
  20. Harrison R. V., Harel N., Panesar J., Mount R. J. (2002). Blood capillary distribution correlates with hemodynamic-based functional imaging in cerebral cortex. Cereb. Cortex 12, 225 – 233. doi:10.1093/cercor/12.3.225
  21. Horton J., Hedley-Whyte E. T. (1984). Mapping of cytochrome oxidase patches and ocular dominance columns in human visual cortex. Philos. Trans. R. Soc. Lond. Biol. B. 304, 255 – 272. doi:10.1098/rstb.1984.0022
  22. Horton J. C., Dagi L. R., McCrane E. P. (1990). Arrangement of ocular dominance columns in human visual cortex. Arch. Opthalmol. 108, 1025 – 1031.
  23. Hubel D., Wiesel T. N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106 – 154.
  24. Hubel D., Wiesel T. N. (1965). Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J. Neurophysiol. 28, 229 – 289.
  25. Hubel D. H., Wiesel T. N. (1963). Shape and arrangement of columns in cat's striate cortex. J. Physiol. (Lond.) 165, 559 – 568.
  26. Hubel D. H., Wiesel T. N. (1977). Functional architecture of macaque monkey visual cortex. Proc. R. Soc. Lond. [Biol.] 198, 1 – 59. doi:10.1098/rspb.1977.0085
  27. Hubener M., Shoham D., Grinvald A., Bonhoeffer T. (1997). Spatial relationships among three columnar systems in cat area 17. J. Neurosci. 17, 9270 – 9284.
  28. Issa N. P., Trepel C., Stryker M. P. (2000). Spatial frequency maps in cat visual cortex. J. Neurosci. 20, 8504 – 8514.
  29. Kim D. S., Duong T. Q., Kim S. G. (2000). High-resolution mapping of iso-orientation columns by fMRI. Nat. Neurosci. 3, 164 – 169. doi:10.1038/72109
  30. Kim D. S., Ronen I., Olman C., Kim S. G., Ugurbil K., Toth L. J. (2004). Spatial relationship between neuronal activity and BOLD functional MRI. Neuroimage 21, 876 – 885. doi:10.1016/j.neuroimage.2003.10.018
  31. Kleinfeld D., Mitra P. P., Helmchen F., Denk W. (1998). Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc. Natl. Acad. Sci. U.S.A. 95, 15741 – 15746. doi:10.1073/pnas.95.26.15741
  32. LaManna J. C., Chavez J. C., Pichiule P. (2004). Structural and functional adaptation to hypoxia in the rat brain. J. Exp. Biol. 207, 3163 – 3169. doi:10.1242/jeb.00976
  33. LaManna J. C., Vendel L. M., Farrell R. M. (1992). Brain adaptation to chronic hypobaric hypoxia in rats. J. Appl. Physiol. 72, 2238 – 2243.
  34. Lauwers F., Cassot F., Lauwers-Cances V., Puwanarajah P., Duvernoy H. (2008). Morphometry of the human cerebral cortex microcirculation: general characteristics and space-related profiles. Neuroimage 39, 936 – 948. doi:10.1016/j.neuroimage.2007.09.024
  35. Logothetis N. K., Pauls J., Augath M., Trinath T., Oeltermann A. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature 412, 150 – 157. doi:10.1038/35084005
  36. Lorente de No R. (1938). “Architectonics and structure of the cerberal cortex,” in Physiology of the Nervous System, ed. Fulton J. F. (New York: Oxford University Press), 291 – 330.
  37. Lowel S., Singer W. (1987). The pattern of ocular dominance columns in flat-mounts of the cat visual cortex. Exp. Brain Res. 68, 661 – 666. doi:10.1007/BF00249809
  38. Malonek D., Dirnagl U., Lindauer U., Yamada K., Kanno I., Grinvald A. (1997). Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. Proc. Natl. Acad. Sci. U.S.A. 94, 14826 – 14831. doi:10.1073/pnas.94.26.14826
  39. Malonek D., Grinvald A. (1996). Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implication for functional brain mapping. Science 272, 551 – 554. doi:10.1126/science.272.5261.551
  40. McHedlishvili G., Kuridze N. (1984). The modular organization of the pial arterial system in phylogeny. J. Cereb. Blood Flow Metab. 4, 391 – 396.
  41. Menon R. S., Ogawa S., Strupp J. P., Ugurbil K. (1997). Ocular dominance in human V1 demonstrated by functional magnetic resonance imaging. J. Neurophysiol. 77, 2780 – 2787.
  42. Moeller S., Yacoub E., Olman C., Auerbach E. J., Stupp J., Harel N., Ugurbil K. (2010). Multiband multislice GE-EPI at 7 tesla, with 16-fold acceleration using partial parallel imaging with application to high spatial and temporal whole-brain fMRI. Magn. Reson. Med. 63, 1144 – 1153. doi:10.1002/mrm.22361
  43. Mountcastle V. B. (1957). Modality and topographic properties of single neurons of cat's somatic sensory cortex. J. Neurophysiol. 20, 408 – 434.
  44. Mountcastle V. B. (1997). The columnar organization of the neocortex. Brain 120 (Pt 4), 701 – 722. doi:10.1093/brain/120.4.701
  45. Mountcastle V. B. (2003). Introduction. Computation in cortical columns. Cereb. Cortex 13, 2 – 4. doi:10.1093/cercor/13.1.2
  46. Park S. H., Masamoto K., Hendrich K., Kanno I., Kim S. G. (2008). Imaging brain vasculature with BOLD microscopy: MR detection limits determined by in vivo two-photon microscopy. Magn. Reson. Med. 59, 855 – 865. doi:10.1002/mrm.21573
  47. Reina-De La Torre F., Rodriguez-Baeza A., Sahuquillo-Barris J. (1998). Morphological characteristics and distribution pattern of the arterial vessels in human cerebral cortex: a scanning electron microscope study. Anat. Rec. 251, 87 – 96. doi:10.1002/(SICI)1097-0185(199805)251:1<87::AID-AR14>3.0.CO;2-7
  48. Roggendorf W., Cervos-Navarro J., Lazaro-Lacalle M. D. (1978). Ultrastructure of venules in the cat brain. Cell Tissue Res. 192, 461 – 474. doi:10.1007/BF00212326
  49. Roy C., Sherrington C. (1890). On the regulation of the blood supply of the brain. J. Physiol. 11, 85 – 108.
  50. Schaffer C. B., Friedman B., Nishimura N., Schroeder L. F., Tsai P. S., Ebner F. F., Lyden P. D., Kleinfeld D. (2006). Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol. 4: e22. doi:10.1371/journal.pbio.0040022
  51. Shen T., Weissleder R., Papisov M., Bogdanov A. Jr., Brady T. J. (1993). Monocrystalline iron oxide nanocompounds (MION): physicochemical properties. Magn. Reson. Med. 29, 599 – 604. doi:10.1002/mrm.1910290504
  52. Shoham D., Hubener M., Schulze S., Grinvald A., Bonhoeffer T. (1997). Spatio-temporal frequency domains and their relation to cytochrome oxidase staining in cat visual cortex. Nature 385, 529 – 533. doi:10.1038/385529a0
  53. Silva A. C., Koretsky A. P. (2002). Laminar specificity of functional MRI onset times during somatosensory stimulation in rat. Proc. Natl. Acad. Sci. U.S.A. 99, 15182 – 15187. doi:10.1073/pnas.222561899
  54. Sun P., Ueno K., Waggoner R. A., Gardner J. L., Tanaka K., Cheng K. (2007). A temporal frequency-dependent functional architecture in human V1 revealed by high-resolution fMRI. Nat. Neurosci. 10, 1404 – 1406. doi:10.1038/nn1983
  55. Tanaka K. (1996). Inferotemporal cortex and object vision. Annu. Rev. Neurosci. 19, 109 – 139. doi:10.1146/annurev.ne.19.030196.000545
  56. Thompson J. K., Peterson M. R., Freeman R. D. (2003). Single-neuron activity and tissue oxygenation in the cerebral cortex. Science 299, 1070 – 1072. doi:10.1126/science.1079220
  57. Tieman S. B., Mollers S., Tieman D. G., White J. (2004). The blood supply of the cat's visual cortex and its postnatal development. Brain Res. 998, 100 – 112. doi:10.1016/j.brainres.2003.11.023
  58. Turner R. (2002). How much cortex can a vein drain? Downstream dilution of activation-related cerebral blood oxygenation changes. Neuroimage 16, 1062 – 1067. doi:10.1006/nimg.2002.1082
  59. Weliky M., Bosking W. H., Fitzpatrick D. (1996). A systematic map of direction preference in primary visual cortex. Nature 379, 725 – 728. doi:10.1038/379725a0
  60. Wolff J. R. (1976). Proceedings: an ontogenetically defined angi oarchitecture of the neocortex. Arzneimittelforschung 26, 1239.
  61. Woolsey T. A., Rovainen C. M., Cox S. B., Henegar M. H., Liang G. E., Liu D., Moskalenko Y. E., Sui J., Wei L. (1996). Neuronal units linked to microvascular modules in cerebral cortex: response elements for imaging the brain. Cereb. Cortex 6, 647 – 660. doi:10.1093/cercor/6.5.647
  62. Yacoub E., Harel N., Ugurbil K. (2008). High-field fMRI unveils orientation columns in humans. Proc. Natl. Acad. Sci. U.S.A. 105, 10607 – 10612. doi:10.1073/pnas.0804110105
  63. Yacoub E., Shmuel A., Logothetis N., Ugurbil K. (2007). Robust detection of ocular dominance columns in humans using Hahn Spin Echo BOLD functional MRI at 7 Tesla. Neuroimage 37, 1161 – 1177. doi:10.1016/j.neuroimage.2007.05.020
  64. Zhao F., Wang P., Hendrich K., Kim S. G. (2005). Spatial specificity of cerebral blood volume-weighted fMRI responses at columnar resolution. Neuroimage 27, 416 – 424. doi:10.1016/j.neuroimage.2005.04.011
  65. Zhao F., Wang P., Hendrich K., Ugurbil K., Kim S. G. (2006). Cortical layer-dependent BOLD and CBV responses measured by spin-echo and gradient-echo fMRI: insights into hemodynamic regulation. Neuroimage 30, 1149 – 1160. doi:10.1016/j.neuroimage.2005.11.013
  66. Zhao F., Wang P., Kim S. G. (2004). Cortical depth-dependent gradient-echo and spin-echo BOLD fMRI at 9.4T. Magn. Reson. Med. 51, 518 – 524. doi:10.1002/mrm.10720
  67. Zheng D., LaMantia A-.S., Purves D. (1991). Specialized vascularization of the primate visual cortex. J. Neurosci. 11, 2622 – 2629.

Citation

Harel, N., et al. (2010). Recent Advances in High-Resolution MR Application and Its Implications for Neurovascular Coupling Research. Frontiers in Neuroenergetics, Volume 2. https://doi.org/
Received
Accepted
Published
Volume
2 - 2010

Copyright

Copyright © 2010 Harel, Bolan, Turner, Ugurbil and Yacoub.

License: http://www.frontiersin.org/licenseagreement

*Correspondence: Noam Harel

Article metrics

Views
0
Downloads
0
Citations
0
Shares
0

Related articles

NeuroscienceInduction of ischemic stroke in awake freely moving mice reveals that isoflurane anesthesia can mask the benefits of a neuroprotection therapyAngela Seto, Stephanie Taylor, Dustin Trudeau, Ian Swan, Jay Leung, Patrick Reeson, Kerry R. Delaney, Craig E. BrownNeuroscienceImpaired cortical mitochondrial function following TBI precedes behavioral changesWilliam D. Watson, John E. Buonora, Angela M. Yarnell, Jessica J. Lucky, Michaela I. D’Acchille, David C. McMullen, Andrew G. Boston, Andrew V. Kuczmarski, William S. Kean, Ajay Verma, Neil E. Grunberg, Jeffrey T. ColeNeuroscienceFDG-PET imaging in mild traumatic brain injury: a critical reviewKimberly R. Byrnes, Colin M. Wilson, Fiona Brabazon, Ramona von Leden, Jennifer S. Jurgens, Terrence R. Oakes, Reed G. Selwyn