4.8 Article

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

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2200205119

Keywords

neurovascular coupling; initial dip; oxygen

Funding

  1. Institut National de la Sante et de la Recherche Medicale (INSERM)
  2. European Research Council (ERC) [339513]
  3. Fondation pour la Recherche Medicale [EQU201903007811]
  4. Agence Nationale de la Recherche [NR-16-RHUS-0004]
  5. Fondation Leducq Transatlantic Networks of Excellence program [16CVD05]
  6. French state funds [ANR-18-IAHU-0001]
  7. European Research Council (ERC) [339513] Funding Source: European Research Council (ERC)

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This study investigates the initial dip in oxygen concentration in a specific neuronal network and finds that it is present in anesthetized mice but absent in awake mice. This finding contradicts previous research.
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 pO(2) measurements, we characterized this initial dip in pO(2) in mice chronically implanted with a glass cranial window, during both awake and anesthetized conditions. In anesthetized mice, a transient dip in vascular pO(2) was detected in this glomerulus when functional hyperemia was slightly delayed, but its amplitude was minute (0.3 SD of resting baseline). This vascular pO(2) dip was not observed in other glomeruli responding nonspecifically to ET, and it was poorly influenced by resting pO(2). In awakemice, the dip in pO(2) was absent in capillaries as well as, surprisingly, in the neuropil. These high-resolution pO(2) measurements demonstrate that in awake mice recovered from brain surgery, neurovascular coupling was too fast and efficient to reveal an initial dip in pO(2).

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