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- Title
Baseline oxygen consumption decreases with cortical depth.
- Authors
Mächler, Philipp; Fomin-Thunemann, Natalie; Thunemann, Martin; Sætra, Marte Julie; Desjardins, Michèle; Kılıç, Kıvılcım; Amra, Layth N.; Martin, Emily A.; Chen, Ichun Anderson; Şencan-Eğilmez, Ikbal; Li, Baoqiang; Saisan, Payam; Jiang, John X.; Cheng, Qun; Weldy, Kimberly L.; Boas, David A.; Buxton, Richard B.; Einevoll, Gaute T.; Dale, Anders M.; Sakadžić, Sava
- Abstract
The cerebral cortex is organized in cortical layers that differ in their cellular density, composition, and wiring. Cortical laminar architecture is also readily revealed by staining for cytochrome oxidase—the last enzyme in the respiratory electron transport chain located in the inner mitochondrial membrane. It has been hypothesized that a high-density band of cytochrome oxidase in cortical layer IV reflects higher oxygen consumption under baseline (unstimulated) conditions. Here, we tested the above hypothesis using direct measurements of the partial pressure of O2 (pO2) in cortical tissue by means of 2-photon phosphorescence lifetime microscopy (2PLM). We revisited our previously developed method for extraction of the cerebral metabolic rate of O2 (CMRO2) based on 2-photon pO2 measurements around diving arterioles and applied this method to estimate baseline CMRO2 in awake mice across cortical layers. To our surprise, our results revealed a decrease in baseline CMRO2 from layer I to layer IV. This decrease of CMRO2 with cortical depth was paralleled by an increase in tissue oxygenation. Higher baseline oxygenation and cytochrome density in layer IV may serve as an O2 reserve during surges of neuronal activity or certain metabolically active brain states rather than reflecting baseline energy needs. Our study provides to our knowledge the first quantification of microscopically resolved CMRO2 across cortical layers as a step towards better understanding of brain energy metabolism. The high density of cytochrome oxidase in cortical layer IV has been hypothesized to reflect higher basal oxygen consumption, but is this true? This study uses two-photon oxygen imaging technology and modeling to measure basal oxygen metabolism across cortical layers in awake mice; surprisingly, basal oxygen consumption decreases from layer I to layer IV.
- Subjects
OXYGEN consumption; CYTOCHROME oxidase; BASAL metabolism; MITOCHONDRIAL membranes; ELECTRON transport; CEREBRAL cortex
- Publication
PLoS Biology, 2022, Vol 20, Issue 10, p1
- ISSN
1544-9173
- Publication type
Article
- DOI
10.1371/journal.pbio.3001440