Evolution of the dynamic changes in functional cerebral oxidative metabolism from tissue mitochondria to blood oxygen

The dynamic properties of the cerebral metabolic rate of oxygen consumption (CMR _O2) during changes in brain activity remain unclear. Therefore, the spatial and temporal evolution of functional increases in CMR _O2 was investigated in the rat somato-sensory cortex during forelimb stimulation under a suppressed blood flow response condition. Temporally, stimulation elicited a fast increase in tissue mitochondria CMR _O2 described by a time constant of ∼1 second measured using flavoprotein autofluorescence imaging. CMR _O2-driven changes in the tissue oxygen tension measured using an oxygen electrode and blood oxygenation measured using optical imaging of intrinsic signal followed; however, these changes were slow with time constants of 5 and 10 seconds, respectively. This slow change in CMR _O2-driven blood oxygenation partly explains the commonly observed post-stimulus blood oxygen level-dependent (BOLD) undershoot. Spatially, the changes in mitochondria CMR _O2 were similar to the changes in blood oxygenation. Finally, the increases in CMR _O2 were well correlated with the evoked multi-unit spiking activity. These findings show that dynamic CMR _O2 calculations made using only blood oxygenation data (e.g., BOLD functional magnetic resonance imaging (fMRI)) do not directly reflect the temporal changes in the tissue's mitochondria metabolic rate; however, the findings presented can bridge the gap between the changes in cellular oxidative rate and blood oxygenation.