The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow (original) (raw)

References

  1. Magistretti, P.J. & Pellerin, L. Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354, 1155–1163 (1999).
    Article CAS PubMed PubMed Central Google Scholar
  2. Attwell, D. & Laughlin, S.B. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 21, 1133–1145 (2001).
    Article CAS PubMed Google Scholar
  3. Mchedlishvili, G. Arterial Behavior and Blood Circulation in the Brain (Consultants Bureau, New York, 1963).
  4. Schaffer, C.B. et al. Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol. 4, 22 (2006).
    Article CAS Google Scholar
  5. Blinder, P., Shih, A.Y., Rafie, C.A. & Kleinfeld, D. Topological basis for the robust distribution of blood to rodent neocortex. Proc. Natl. Acad. Sci. USA 107, 12670–12675 (2010).
    Article PubMed PubMed Central Google Scholar
  6. Devor, A. et al. Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level–dependent signaling. J. Neurosci. 27, 4452–4459 (2007).
    Article CAS PubMed PubMed Central Google Scholar
  7. Derdikman, D., Hildesheim, R., Ahissar, E., Arieli, A. & Grinvald, A. Imaging spatiotemporal dynamics of surround inhibition in the barrels somatosensory cortex. J. Neurosci. 23, 3100–3105 (2003).
    Article CAS PubMed PubMed Central Google Scholar
  8. Gorelick, P.B. et al. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 42, 2672–2713 (2011).
    Article PubMed PubMed Central Google Scholar
  9. Iadecola, C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 5, 347–360 (2004).
    Article CAS PubMed Google Scholar
  10. Cauli, B. et al. Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J. Neurosci. 24, 8940–8949 (2004).
    Article CAS PubMed PubMed Central Google Scholar
  11. Attwell, D. & Iadecola, C. The neural basis of functional brain imaging signals. Trends Neurosci. 25, 621–625 (2002).
    Article CAS PubMed Google Scholar
  12. Weber, B., Keller, A.L., Reichold, J. & Logothetis, N.K. The microvascular system of the striate and extrastriate visual cortex of the macaque. Cereb. Cortex 18, 2318–2330 (2008).
    Article PubMed Google Scholar
  13. Grinvald, A., Lieke, E.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 PubMed Google Scholar
  14. Woolsey, T.A. & Van Der Loos, H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. Brain Res. 17, 205–242 (1970).
    Article CAS PubMed Google Scholar
  15. Woolsey, T.A. et al. Neuronal units linked to microvascular modules in cerebral cortex: response elements for imaging the brain. Cereb. Cortex 6, 647–660 (1996).
    Article CAS PubMed Google Scholar
  16. Nishimura, N., Schaffer, C.B., Friedman, B., Lyden, P.D. & Kleinfeld, D. Penetrating arterioles are a bottleneck in the perfusion of neocortex. Proc. Natl. Acad. Sci. USA 104, 365–370 (2007).
    Article CAS PubMed Google Scholar
  17. Nishimura, N., Rosidi, N.L., Iadecola, C. & Schaffer, C.B. Limitations of collateral flow after occlusion of a single cortical penetrating arteriole. J. Cereb. Blood Flow Metab. 30, 1914–1927 (2010).
    Article PubMed PubMed Central Google Scholar
  18. Drew, P.J. et al. Chronic optical access through a polished and reinforced thinned skull. Nat. Methods 7, 981–984 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  19. Tsai, P.S. et al. Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of cell nuclei and microvessels. J. Neurosci. 29, 14553–14570 (2009).
    Article CAS PubMed PubMed Central Google Scholar
  20. Tsai, P.S. et al. All-optical histology using ultrashort laser pulses. Neuron 39, 27–41 (2003).
    Article CAS PubMed Google Scholar
  21. Shih, A.Y. et al. The smallest stroke: occlusion of one penetrating vessel leads to infarction and a cognitive deficit. Nat. Neurosci. 16, 55–63 (2013).
    Article CAS PubMed Google Scholar
  22. Nguyen, J., Nishimura, N., Fetcho, R.N., Iadecola, C. & Schaffer, C.B. Occlusion of cortical ascending venules causes blood flow decreases, reversals in flow direction, and vessel dilation in upstream capillaries. J. Cereb. Blood Flow Metab. 31, 2243–2254 (2011).
    Article PubMed PubMed Central Google Scholar
  23. Kim, T. & Kim, S.G. Temporal dynamics and spatial specificity of aterial and venous blood volume changes during visual stimulation: implication for BOLD quantification. J. Cereb. Blood Flow Metab. 31, 1211–1222 (2011).
    Article PubMed Google Scholar
  24. 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 PubMed PubMed Central Google Scholar
  25. Kaufhold, J.P., Tsai, P.S., Blinder, P. & Kleinfeld, D. Vectorization of optically sectioned brain microvasculature: learning aids completion of vascular graphs by connecting gaps and deleting open-ended segments. Med. Image Anal. 16, 1241–1258 (2012).
    Article PubMed PubMed Central Google Scholar
  26. Lauwers, F., Cassot, F., Lauwers-Cances, V., Puwanarajah, P. & Duvernoy, H. Morphometry of the human cerebral cortex microcirculation: general characteristics and space-related profiles. Neuroimage 39, 936–948 (2008).
    Article PubMed Google Scholar
  27. Hirsch, S., Reichold, J., Schneider, M., Székely, G. & Weber, B. Topology and hemodynamics of the cortical cerebrovascular system. J. Cereb. Blood Flow Metab. 32, 952–967 (2012).
    Article PubMed PubMed Central Google Scholar
  28. Duvernoy, H.M., Delon, S. & Vannson, J.L. Cortical blood vessels of the human brain. Brain Res. Bull. 7, 519–579 (1981).
    Article CAS PubMed Google Scholar
  29. Nishimura, N. et al. Targeted insult to individual subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke. Nat. Methods 3, 99–108 (2006).
    Article CAS PubMed Google Scholar
  30. Shih, A.Y. et al. Active dilation of penetrating arterioles restores red blood cell flux to penumbral neocortex after focal stroke. J. Cereb. Blood Flow Metab. 29, 738–751 (2009).
    Article PubMed Google Scholar
  31. Cserti, J. Application of the lattice Green's function for calculating the resistance of infinite networks of resistors. Am. J. Phys. 68, 896–913 (2000).
    Article Google Scholar
  32. Pries, A.R., Secomb, T.W., Gaehtgens, P. & Gross, J.F. Blood flow in microvascular networks. Experiments and simulation. Circ. Res. 67, 826–834 (1990).
    Article CAS PubMed Google Scholar
  33. Wu, F.Y. Theory of resistor networks: the two-point resistance. J. Phys. A Math. Gen. 37, 6653 (2004).
    Article Google Scholar
  34. Newman, M.E.J. Modularity and community structure in networks. Proc. Natl. Acad. Sci. USA 103, 8577–8582 (2006).
    Article CAS PubMed PubMed Central Google Scholar
  35. Mayhan, W.G. & Heistad, D.D. Role of veins and cerebral venous pressure in disruption of the blood-brain barrier. Circ. Res. 59, 216–220 (1986).
    Article CAS PubMed Google Scholar
  36. Grinvald, A., Frostig, R.D., Siegel, R.M. & Bartfeld, E. High-resolution optical imaging of functional brain architecture in the awake monkey. Proc. Natl. Acad. Sci. USA 88, 11559–11563 (1991).
    Article CAS PubMed PubMed Central Google Scholar
  37. 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 PubMed PubMed Central Google Scholar
  38. Vazquez, A.L., Fukuda, M. & Kim, S.G. Evolution of the dynamic changes in functional cerebral oxidative metabolism from tissue mitochondria to blood oxygen. J. Cereb. Blood Flow Metab. 32, 745–758 (2012).
    Article CAS PubMed PubMed Central Google Scholar
  39. Chen-Bee, C.H., Agoncillo, T., Xiong, Y. & Frostig, R.D. The triphasic intrinsic signal: implications for functional imaging. J. Neurosci. 27, 4572–4586 (2007).
    Article CAS PubMed PubMed Central Google Scholar
  40. Sirotin, Y.B., Hillman, E.M., Bordier, C. & Das, A. Spatiotemporal precision and hemodynamic mechanism of optical point spreads in alert primates. Proc. Natl. Acad. Sci. USA 106, 18390–18395 (2009).
    Article PubMed PubMed Central Google Scholar
  41. Eppihimer, M.J. & Lipowsky, H.H. Effects of leukocyte-capillary plugging on the resistance to flow in the microvasculature of cremaster muscle for normal and activated leukocytes. Microvasc. Res. 51, 187–201 (1996).
    Article CAS PubMed Google Scholar
  42. Nakai, K. et al. Microangioarchitecture of rat parietal cortex with special reference to vascular “sphincters”: scanning electron microscopic and dark field microscopic study. Stroke 12, 653–659 (1981).
    Article CAS PubMed Google Scholar
  43. Boas, D.A., Jones, S.R., Devor, A., Huppert, T.J. & Dale, A.M. A vascular anatomical network model of the spatio-temporal response to brain activation. Neuroimage 40, 1116–1129 (2008).
    Article PubMed Google Scholar
  44. Guibert, R., Fonta, C. & Plouraboué, F. Cerebral blood flow modeling in primate cortex. J. Cereb. Blood Flow Metab. 30, 1860–1873 (2010).
    Article PubMed PubMed Central Google Scholar
  45. Risser, L., Plouraboue, F., Cloetens, P. & Fonta, C. A 3D-investigation shows that angiogenesis in primate cerebral cortex mainly occurs at capillary level. Int. J. Dev. Neurosci. 27, 185–196 (2009).
    Article PubMed Google Scholar
  46. Kleinfeld, D. et al. A guide to delineate the logic of neurovascular signaling in the brain. Front. Neuroenergetics 1, 1–9 (2011).
    Google Scholar
  47. Attwell, D. et al. Glial and neuronal control of brain blood flow. Nature 468, 232–243 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  48. Zhang, S. & Murphy, T.H. Imaging the impact of cortical microcirculation on synaptic structure and sensory-evoked hemodynamic responses in vivo. PLoS Biol. 5, e119 (2007).
    Article CAS PubMed PubMed Central Google Scholar
  49. Smith, E.E., Schneider, J.A., Wardlaw, J.M. & Greenberg, S.M. Cerebral microinfarcts: the invisible lesions. Lancet Neurol. 11, 272–282 (2012).
    Article PubMed PubMed Central Google Scholar
  50. Brundel, M., de Bresser, J., van Dillen, J.J., Kappelle, L.J. & Biessels, G.J. Cerebral microinfarcts: a systematic review of neuropathological studies. J. Cereb. Blood Flow Metab. 32, 425–436 (2012).
    Article PubMed PubMed Central Google Scholar
  51. Kohn, A., Metz, C., Quibrera, M., Tommerdahl, M.A. & Whitsel, B.L. Functional neocortical microcircuitry demonstrated with intrinsic signal optical imaging in vitro. Neuroscience 95, 51–62 (2000).
    Article CAS PubMed Google Scholar
  52. Denk, W., Strickler, J.H. & Webb, W.W. Two-photon laser scanning fluorescence microscopy. Science 248, 73–76 (1990).
    Article CAS PubMed Google Scholar
  53. Oraevsky, A. et al. Plasma mediated ablation of biological tissues with nanosecond-to-femtosecond laser pulses: relative role of linear and nonlinear absorption. IEEE J. Sel. Top. Quantum Electron. 2, 801–809 (1996).
    Article CAS Google Scholar
  54. Nguyen, Q.-T., Tsai, P.S. & Kleinfeld, D. MPScope: a versatile software suite for multiphoton microscopy. J. Neurosci. Methods 156, 351–359 (2006).
    Article PubMed Google Scholar
  55. Emmenlauer, M. et al. XuvTools: free, fast and reliable stitching of large 3D datasets. J. Microsc. 233, 42–60 (2009).
    Article CAS PubMed Google Scholar
  56. Blondel, V.D., Guillaume, J.-L., Lambiotte, R. & Lefebvre, E. Fast unfolding of communities in large networks. J. Stat. Mech. published online, doi:10.1088/1742-5468/2008/10/P10008 (9 October 2008).
  57. Fortunat, S. Community detection in graphs. Phys. Rep. 486, 74–175 (2010).
    Google Scholar
  58. Strehl, A. & Ghosh, J. Cluster ensembles: a knowledge reuse framework for combining multiple partitions. J. Mach. Learn. Res. 3, 583–617 (2001).
    Google Scholar
  59. Watts, D.J. & Strogatz, S.H. Collective dynamics of 'small-world' networks. Nature 393, 440–442 (1998).
    Article CAS PubMed Google Scholar
  60. Newman, M. Networks: An Introduction (Oxford University Press, New York, 2010).

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