» Articles » PMID: 31305237

More Homogeneous Capillary Flow and Oxygenation in Deeper Cortical Layers Correlate with Increased Oxygen Extraction

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 (PO) 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.

Citing Articles

Reduced removal of waste products from energy metabolism takes center stage in human brain aging.

Mangia S, DiNuzzo M, Ponticorvo S, Dienel G, Behar K, Benveniste H Sci Rep. 2025; 15(1):8127.

PMID: 40057554 PMC: 11890754. DOI: 10.1038/s41598-025-90342-3.


Out-of-focus signal rejection for pO measurements using two-photon phosphorescence lifetime microscopy.

Pian Q, Li B, Sencan-Egilmez I, Cheng X, Dubb J, Huang X Biomed Opt Express. 2025; 16(1):159-176.

PMID: 39816157 PMC: 11729295. DOI: 10.1364/BOE.532084.


Depth-Dependent Contributions of Various Vascular Zones to Cerebral Autoregulation and Functional Hyperemia: An In-Silico Analysis.

Esfandi H, Javidan M, Anderson R, Pashaie R bioRxiv. 2024; .

PMID: 39416222 PMC: 11482864. DOI: 10.1101/2024.10.07.616950.


Cerebral microvascular changes in healthy carriers of the APOE-ɛ4 Alzheimer's disease risk gene.

Aamand R, Rasmussen P, Andersen K, de Paoli S, Weitzberg E, Christiansen M PNAS Nexus. 2024; 3(9):pgae369.

PMID: 39253395 PMC: 11382292. DOI: 10.1093/pnasnexus/pgae369.


Quantitative Optical Imaging of Oxygen in Brain Vasculature.

Rathbone E, Fu D J Phys Chem B. 2024; 128(29):6975-6989.

PMID: 38991095 PMC: 11821374. DOI: 10.1021/acs.jpcb.4c01277.


References
1.
Alkire M, Pomfrett C, Haier R, Gianzero M, Chan C, Jacobsen B . Functional brain imaging during anesthesia in humans: effects of halothane on global and regional cerebral glucose metabolism. Anesthesiology. 1999; 90(3):701-9. DOI: 10.1097/00000542-199903000-00011. View

2.
Braun R, Lanzen J, Dewhirst M . Fourier analysis of fluctuations of oxygen tension and blood flow in R3230Ac tumors and muscle in rats. Am J Physiol. 1999; 277(2):H551-68. DOI: 10.1152/ajpheart.1999.277.2.H551. View

3.
Sato Y, Nakajima S, Shiraga N, Atsumi H, Yoshida S, Koller T . Three-dimensional multi-scale line filter for segmentation and visualization of curvilinear structures in medical images. Med Image Anal. 2000; 2(2):143-68. DOI: 10.1016/s1361-8415(98)80009-1. View

4.
Raichle M, MacLeod A, Snyder A, Powers W, Gusnard D, Shulman G . A default mode of brain function. Proc Natl Acad Sci U S A. 2001; 98(2):676-82. PMC: 14647. DOI: 10.1073/pnas.98.2.676. View

5.
Attwell D, Laughlin S . An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab. 2001; 21(10):1133-45. DOI: 10.1097/00004647-200110000-00001. View