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The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow

Nature Neuroscience volume 16, pages 889–897 (2013)Cite this article

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Abstract

What is the nature of the vascular architecture in the cortex that allows the brain to meet the energy demands of neuronal computations? We used high-throughput histology to reconstruct the complete angioarchitecture and the positions of all neuronal somata of multiple cubic millimeter regions of vibrissa primary sensory cortex in mouse. Vascular networks were derived from the reconstruction. In contrast with the standard model of cortical columns that are tightly linked with the vascular network, graph-theoretical analyses revealed that the subsurface microvasculature formed interconnected loops with a topology that was invariant to the position and boundary of columns. Furthermore, the calculated patterns of blood flow in the networks were unrelated to location of columns. Rather, blood sourced by penetrating arterioles was effectively drained by the penetrating venules to limit lateral perfusion. This analysis provides the underpinning to understand functional imaging and the effect of penetrating vessels strokes on brain viability.

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Figure 1: Examples of the vectorized data sets.
Figure 2: Analysis of the local geometry and topology of the microvasculature.
Figure 3: Community analysis of the global topology of the microvasculature.
Figure 4: Calculated fluid flow and domains of common input in complete vectorized networks.
Figure 5: Relation of penetrating vessels to cortical columns.
Figure 6: Relation of images of the intrinsic optical signal (IOS) to the centroids of the cortical columns.
Figure 7: Calculated loss of lateral flow under numerically imposed pathological conditions in comparison with experimental observations.
Figure 8: Lattice models of the angiome.

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Acknowledgements

We thank J. Lee for assistance in the analysis of the surface vasculature, J.D. Driscoll for assistance with the imaging acquisition software, N. Nishimura and C.B. Schaffer for sharing their data logs, S. Chien, W. Denk, P.J. Drew, A.L. Fairhall, B. Friedman, R.D. Frostig, H.J. Karten, H.S. Seung, T.W. Secomb, A.Y. Shih and B. Weber for critical discussions. This work was supported by the Israeli Science Foundation (Bikura fellowship to P.B.) and the US National Institutes of Health (grants EB003832, MH085499, MH072570 and OD006831).

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Author notes

  1. Pablo Blinder & John P Kaufhold

    Present address: Present addresses: Department of Neuroscience, Tel Aviv University, Tel Aviv, Israel (P.B.), and Circuit Dynamics and Connectivity Unit, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland, USA (J.P.K.).,

  2. Pablo Blinder and Philbert S Tsai: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Physics, University of California at San Diego, La Jolla, California, USA

    Pablo Blinder, Philbert S Tsai, Per M Knutsen, Harry Suhl & David Kleinfeld

  2. Science Applications International Corporation Intelligent Systems Division, Arlington, Virginia, USA

    John P Kaufhold

  3. Section of Neurobiology, University of California at San Diego, La Jolla, California, USA

    David Kleinfeld

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Contributions

P.B., D.K. and P.S.T. designed the study. P.B., P.M.K. and P.S.T. carried out the experiments and analyzed and summarized the data with input from J.P.K., D.K. and H.S. D.K. wrote the manuscript.

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Correspondence to David Kleinfeld.

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Blinder, P., Tsai, P., Kaufhold, J. et al. The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow. Nat Neurosci 16, 889–897 (2013). https://doi.org/10.1038/nn.3426

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