Vascular supply of the cerebral cortex is specialized for cell layers but not columns

Cerebral Cortex

Volumn 25, Issue 10, 2015, Pages 3673-3681

  Adams, Daniel L ^a,b   Piserchia, Valentina ^b   Economides, John R ^a   Horton, Jonathan C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TRENTO   (Italy)

Author keywords

Cytochrome oxidase blob; fMRI; Macaque visual cortex; Microvascular lobule; Microvascular sphincter

Indexed keywords

CYTOCHROME C OXIDASE; PEROXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIAL CIRCULATION; ARTERIOLE; ARTICLE; BLOOD OXYGENATION; BRAIN BLOOD FLOW; BRAIN CIRCULATION; BRAIN CORTEX; BRAIN MICROCIRCULATION; CELL MEMBRANE; CELL POPULATION; CONTROLLED STUDY; ERYTHROCYTE; FEMALE; GREAT BLOOD VESSEL; LAMINAR FLOW; MACACA; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; STRIATE CORTEX; VENULE; ANIMAL; BLOOD CELL; METABOLISM; RHESUS MONKEY; VASCULARIZATION; VISUAL CORTEX;

ANIMALS; BLOOD CELLS; CEREBRAL CORTEX; FEMALE; MACACA MULATTA; PEROXIDASE; VISUAL CORTEX;

EID: 84948657480     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu221     Document Type: Article

References (70)

1. Atkins GB, Jain MK, Hamik A. 2011. Endothelial differentiation: molecular mechanisms of specification and heterogeneity. Arterioscler Thromb Vasc Biol. 31:1476-1484.
2. Baramidze D, McHedlishvili G, Gordeladze Z, Levkovitch Y. 1992. Cerebral microcirculation: heterogeneity of pial arterial network controlling microcirculation of cerebral cortex. Int J Microcirc Clin Exp. 11:143-155.
3. Baramidze DG, Reidler RM, Gadamski R, McHedlishvili GI. 1982. Pattern and innervation of pial microvascular effectors which control blood supply to cerebral cortex. Blood Vessels. 19:284-291.
4. Bell MA, Ball MJ. 1985. Laminar variation in the microvascular architecture of normal human visual cortex (area 17). Brain Res. 335:139-143.
5. Blinder P, Tsai PS, Kaufhold JP, Knutsen PM, Suhl H, Kleinfeld D. 2013. The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow. Nat Neurosci. 16:889-897.
6. Bonhoeffer T, Grinvald A. 1991. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature. 353:429-431.
7. Boynton GM. 2005. Imaging orientation selectivity: decoding conscious perception in V1. Nat Neurosci. 8:541-542.
8. Cheng K, Waggoner RA, Tanaka K. 2001. Human ocular dominance columns as revealed by high-field functional magnetic resonance imaging. Neuron. 32:359-374.
9. Cox SB, Woolsey TA, Rovainen CM. 1993. Localized dynamic changes in cortical blood flow with whisker stimulation corresponds to matched vascular and neuronal architecture of rat barrels. J Cereb Blood Flow Metab. 13:899-913.
10. Craigie EH. 1945. The architecture of the cerebral capillary bed. Biol Rev. 20:133-146.
11. dela Paz NG, D'Amore PA. 2009. Arterial versus venous endothelial cells. Cell Tissue Res. 335:5-16.
12. DeYoe EA, Trusk TC, Wong-Riley MT. 1995. Activity correlates of cyto-chrome oxidase-defined compartments in granular and supragra-nular layers of primary visual cortex of the macaque monkey. Vis Neurosci. 12:629-639.
13. Dunning HS, Wolff HG. 1937. The relative vascularity of various parts of the central and peripheral nervous system of the cat and its relation to function. J Comp Neurol. 67:433-450.
14. Duret M. 1874. Recherches anatomiques sur la circulation de l'encéphale. Arch Physiol Norm Patholol. I:60-91, 316-353, 664-693, 919-957.
15. Duvernoy HM, Delon S, Vannson JL. 1981. Cortical blood vessels of the human brain. Brain Res Bull. 7:519-579.
16. Economides JR, Sincich LC, Adams DL, Horton JC. 2011. Orientation tuning of cytochrome oxidase patches in macaque primary visual cortex. Nat Neurosci. 14:1574-1580.
17. Farias MF, Gattass R, Piñón MC, Ungerleider LG. 1997. Tangential distribution of cytochrome oxidase-rich blobs in the primary visual cortex of macaque monkeys. J Comp Neurol. 386:217-228.
18. Fernandez-Klett F, Offenhauser N, Dirnagl U, Priller J, Lindauer U. 2010. Pericytes in capillaries are contractile in vivo, but arterioles mediate functional hyperemia in the mouse brain. Proc Natl Acad Sci USA. 107:22290-22295.
19. Florey H. 1925. Microscopical observations on the circulation of the blood in the cerebral cortex. Brain. 48:43-64.
20. Fonta C, Imbert M. 2002. Vascularization in the primate visual cortex during development. Cereb Cortex. 12:199-211.
21. Gardner JL. 2010. Is cortical vasculature functionally organized? Neuro-image. 49:1953-1956.
22. Gillilan LA. 1974. Potential collateral circulation to the human cerebral cortex. Neurology. 24:941-948.
23. Goense JB, Logothetis NK. 2006. Laminar specificity in monkey V1 using high-resolution SE-fMRI. Magn Reson Imaging. 24:381-392.
24. Goense J, Merkle H, Logothetis NK. 2012. High-resolution fMRI reveals laminar differences in neurovascular coupling between positive and negative BOLD responses. Neuron. 76:629-639.
25. Gordon GR, Mulligan SJ, MacVicar BA. 2007. Astrocyte control of the cerebrovasculature. Glia. 55:1214-1221.
26. Hakim S, Fisher C. 1957. A new technique for the microscopic examination of cerebral vessels in vivo. J Neurosurg. 14:405-412.
27. Harb R, Whiteus C, Freitas C, Grutzendler J. 2013. In vivo imaging of cerebral microvascular plasticity from birth to death. J Cereb Blood Flow Metab. 33:146-156.
28. Harel N, Bolan PJ, Turner R, Ugurbil K, Yacoub E. 2010. Recent advances in high-resolution MR application and its implications for neurovascular coupling research. Front Neuroenerg. 2:130.
29. Harrison RV, Harel N, Panesar J, Mount RJ. 2002. Blood capillary distribution correlates with hemodynamic-based functional imaging in cerebral cortex. Cereb Cortex. 12:225-233.
30. Hirsch S, Reichold J, Schneider M, Szekely G, Weber B. 2012. Topology and hemodynamics of the cortical cerebrovascular system. J Cereb Blood Flow Metab. 32:952-967.
31. Horton JC. 1984. Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex. Philos Trans R Soc Lond B Biol Sci. 304:199-253.
32. Horton JC, Adams DL. 2005. The cortical column: a structure without a function. Philos Trans R Soc Lond B Biol Sci. 360:837-862.
33. Horton JC, Hocking DR. 1996. An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience. J Neurosci. 16:1791-1807.
34. Horton JC, Hubel DH. 1981. Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature. 292:762-764.
35. Hubel DH, Wiesel TN. 1969. Anatomical demonstration of columns in the monkey striate cortex. Nature. 221:747-750.
36. Hubel DH, Wiesel TN. 1977. The Ferrier Lecture: functional architecture of macaque monkey visual cortex. Proc R Soc Lond B Biol Sci. 198:1-59.
37. Hubel DH, Wiesel TN, Stryker MP. 1978. Anatomical demonstration of orientation columns in macaque monkey. J Comp Neurol. 177:361-380.
38. Hübener M, Shoham D, Grinvald A, Bonhoeffer T. 1997. Spatial relationships among three columnar systems in cat area 17. J Neurosci. 17:9270-9284.
39. Issa NP, Trepel C, Stryker MP. 2000. Spatial frequency maps in cat visual cortex. J Neurosci. 20:8504-8514.
40. Kamitani Y, Tong F. 2005. Decoding the visual and subjective contents of the human brain. Nat Neurosci. 8:679-685.
41. Kapralov A, Vlasova II, Feng W, Maeda A, Walson K, Tyurin VA, Huang Z, Aneja RK, Carcillo J, Bayir H et al. 2009. Peroxidase activity of hemoglobin-haptoglobin complexes: covalent aggregation and oxidative stress in plasma and macrophages. J Biol Chem. 284:30395-30407.
42. Keller AL, Schuz A, Logothetis NK, Weber B. 2011. Vascularization of cytochrome oxidase-rich blobs in the primary visual cortex of squirrel and macaque monkeys. J Neurosci. 31:1246-1253.
43. Kety SS. 1948. Quantitative determination of cerebral blood flow in man. Methods Med Res. 1:204-217.
44. Lawrence W. 1819. Lectures on the physiology, zoology, and the natural history of man. London: J. Callow, p. 105.
45. LeVay S, Nelson SB. 1991. Columnar organization of the visual cortex. In: Leventhal AG, editor. The neural basis of visual function. Boston: CRC Press, p. 266-p. 315.
46. Lierse W. 1963. Die Kapillardichte im Wirbeltiergehirn. Acta Anat (Basel). 54:1-31.
47. Logothetis NK, Wandell BA. 2004. Interpreting the BOLD signal. Annu Rev Physiol. 66:735-769.
48. Lu HD, Roe AW. 2008. Functional organization of color domains in V1 and V2 of macaque monkey revealed by optical imaging. Cereb Cortex. 18:516-533.
49. Marcelo KL, Goldie LC, Hirschi KK. 2013. Regulation of endothelial cell differentiation and specification. Circ Res. 112:1272-1287.
50. Mountcastle VB. 1997. The columnar organization of the neocortex. Brain. 120:701-722.
51. Peppiatt CM, Howarth C, Mobbs P, Attwell D. 2006. Bidirectional control of CNS capillary diameter by pericytes. Nature. 443:700-704.
52. Pfeifer RA. 1930. Grundlegende Untersuchungen für die Angioarchi-tektonik des menschlichen Gehirns. Berlin: von Julius Springer.
53. Purves D, LaMantia A. 1993. Development of blobs in the visual cortex of macaques. J Comp Neurol. 334:169-175.
54. Rowbotham GF, Little E. 1962. The circulations and reservoir of the brain. Br J Surg. 50:244-250.
55. Shen Z, Lu Z, Chhatbar PY, O'Herron P, Kara P. 2012. An artery-specific fluorescent dye for studying neurovascular coupling. Nat Methods. 9:273-276.
56. Shmuel A, Chaimow D, Raddatz G, Ugurbil K, Yacoub E. 2010. Mechanisms underlying decoding at 7 T: ocular dominance columns, broad structures, and macroscopic blood vessels in V1 convey information on the stimulated eye. Neuroimage. 49:1957-1964.
57. Sincich LC, Horton JC. 2005. Input to V2 thin stripes arises from V1 cytochrome oxidase patches. J Neurosci. 25:10087-10093.
58. Sun P, Gardner JL, Costagli M, Ueno K, Waggoner RA, Tanaka K, Cheng K. 2013. Demonstration of tuning to stimulus orientation in the human visual cortex: a high-resolution fMRI study with a novel continuous and periodic stimulation paradigm. Cereb Cortex. 23:1618-1629.
59. Swindale NV, Shoham D, Grinvald A, Bonhoeffer T, Hubener M. 2000. Visual cortex maps are optimized for uniform coverage. Nat Neu-rosci. 3:822-826.
60. Tootell RB, Silverman MS, De Valois RL. 1981. Spatial frequency columns in primary visual cortex. Science. 214:813-815.
61. Ts'o DY, Zarella M, Burkitt G. 2009. Whither the hypercolumn? J Physiol. 587:2791-2805.
62. Valverde Salzmann MF, Bartels A, Logothetis NK, Schuz A. 2012. Color blobs in cortical areas V1 and V2 of the new world monkey Calli-thrix jacchus, revealed by non-differential optical imaging. J Neu-rosci. 32:7881-7894.
63. Weber B, Keller AL, Reichold J, Logothetis NK. 2008. The microvascu-lar system of the striate and extrastriate visual cortex of the macaque. Cereb Cortex. 18:2318-2330.
64. Whiteus C, Freitas C, Grutzendler J. 2014. Perturbed neural activity disrupts cerebral angiogenesis during a postnatal critical period. Nature. 505:407-411.
65. Wiesel TN, Hubel DH. 1974. Ordered arrangement of orientation columns in monkeys lacking visual experience. J Comp Neurol. 158:307-318.
66. Wong-Riley MTT. 1979. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res. 171:11-28.
67. Woolsey TA, Rovainen CM, Cox SB, Henegar MH, Liang GE, Liu D, Moskalenko YE, Sui J, Wei L. 1996. Neuronal units linked to micro-vascular modules in cerebral cortex: response elements for imaging the brain. Cereb Cortex. 6:647-660.
68. Xu X, Bosking W, Sary G, Stefansic J, Shima D, Casagrande V. 2004. Functional organization of visual cortex in the owl monkey. J Neurosci. 24:6237-6247.
69. Yoshioka T, Blasdel GG, Levitt JB, Lund JS. 1996. Relation between patterns of intrinsic lateral connectivity, ocular dominance, and cyto-chrome oxidase-reactive regions in macaque monkey striate cortex. Cereb Cortex. 6:297-310.
70. Zheng D, LaMantia AS, Purves D. 1991. Specialized vascularization of the primate visual cortex. J Neurosci. 11:2622-2629.