The oxygen initial dip in the brain of anesthetized and awake mice

An ongoing controversy in brain metabolism is whether increases in neural activity cause a local and rapid decrease in oxygen concentration (i.e., the “initial dip”) preceding functional hyperemia. This initial dip has been suggested to cause a transient increase in vascular deoxyhemoglobin with sev...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2022-04, Vol.119 (14), p.e2200205119-e2200205119
Main Authors: Aydin, Ali-Kemal, Verdier, Camille, Chaigneau, Emmanuelle, Charpak, Serge
Format: Article
Language:English
Subjects:
Animals
Biological Sciences
Blood flow
Brain
Brain - blood supply
Brain - metabolism
Calcium (blood)
Capillaries
Energy consumption
Fluorescence
Glomerulus
Hyperemia
Imaging techniques
Metabolism
Mice
Nerve Net
Neural networks
Neuroimaging
Neurons - physiology
Neuropil
Neurovascular Coupling
Olfactory bulb
Olfactory Bulb - metabolism
Olfactory glomeruli
Oxygen
Oxygen - metabolism
Phosphorescence
Stimulation
Wakefulness
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Summary:An ongoing controversy in brain metabolism is whether increases in neural activity cause a local and rapid decrease in oxygen concentration (i.e., the “initial dip”) preceding functional hyperemia. This initial dip has been suggested to cause a transient increase in vascular deoxyhemoglobin with several imaging techniques and stimulation paradigms, but not consistently. Here, we investigate contributors to this initial dip in a distinct neuronal network, an olfactory bulb (OB) glomerulus most sensitive to a specific odorant (ethyl tiglate [ET]) and a site of strong activation and energy consumption upon ET stimulation. Combining two-photon fluorescence and phosphorescence lifetime microscopy, and calcium, blood flow, and pO2 measurements, we characterized this initial dip in pO2 in mice chronically implanted with a glass cranial window, during both awake and anesthetized conditions. In anesthetized mice, a transient dip in vascular pO2 was detected in this glomerulus when functional hyperemia was slightly delayed, but its amplitude was minute (0.3 SD of resting baseline). This vascular pO2 dip was not observed in other glomeruli responding nonspecifically to ET, and it was poorly influenced by resting pO2. In awake mice, the dip in pO2 was absent in capillaries as well as, surprisingly, in the neuropil. These high-resolution pO2 measurements demonstrate that in awake mice recovered from brain surgery, neurovascular coupling was too fast and efficient to reveal an initial dip in pO2.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2200205119