More homogeneous capillary flow and oxygenation in deeper cortical layers correlate with increased oxygen extraction

Author:

Li Baoqiang1ORCID,Esipova Tatiana V23,Sencan Ikbal1,Kılıç Kıvılcım4,Fu Buyin1,Desjardins Michele5,Moeini Mohammad67,Kura Sreekanth1,Yaseen Mohammad A1ORCID,Lesage Frederic67,Østergaard Leif8,Devor Anna145ORCID,Boas David A19,Vinogradov Sergei A23ORCID,Sakadžić Sava1ORCID

Affiliation:

1. Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States

2. Department of Biochemistry and Biophysics, University of Pennsylvania, Philadelphia, United States

3. Department of Chemistry, University of Pennsylvania, Philadelphia, United States

4. Department of Neurosciences, University of California, San Diego, La Jolla, United States

5. Department of Radiology, University of California, San Diego, La Jolla, United States

6. Institute of Biomedical Engineering, École Polytechnique de Montréal, Montréal, Canada

7. Research Centre, Montreal Heart Institute, Montréal, Canada

8. Center of Functionally Integrative Neuroscience and MINDLab, Institute of Clinical Medicine, Aarhus University, Aarhus, Denmark

9. Department of Biomedical Engineering, Boston University, Boston, United States

Abstract

Our understanding of how capillary blood flow and oxygen distribute across cortical layers to meet the local metabolic demand is incomplete. We addressed this question by using two-photon imaging of resting-state microvascular oxygen partial pressure (PO2) and flow in the whisker barrel cortex in awake mice. Our measurements in layers I-V show that the capillary red-blood-cell flux and oxygenation heterogeneity, and the intracapillary resistance to oxygen delivery, all decrease with depth, reaching a minimum around layer IV, while the depth-dependent oxygen extraction fraction is increased in layer IV, where oxygen demand is presumably the highest. Our findings suggest that more homogeneous distribution of the physiological observables relevant to oxygen transport to tissue is an important part of the microvascular network adaptation to local brain metabolism. These results will inform the biophysical models of layer-specific cerebral oxygen delivery and consumption and improve our understanding of the diseases that affect cerebral microcirculation.

Funder

National Institutes of Health

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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