The relationship between metabolism of neuronal activity, microvascular organization and blood flow dynamics is critical for interpreting functional brain imaging. Here we used the rat dorsal olfactory bulb as a model to determine in vivo the correlation between action potential propagation, synaptic transmission, oxygen consumption and capillary density during odor stimulation. We find that capillaries are extremely dense in layers of intense synaptic interactions like the glomerular layer while it is very low in the overlying nerve layer, devoid of capillaries. In glomeruli, odor triggers a local early decrease in tissue oxygen partial pressure that results principally from dendritic activation rather than from firing of axon terminals, transmitter release or astrocyte activation. In the nerve layer, action potential propagation does not generate local changes in tissue oxygen partial pressure. We also show that under strong peripheral stimulation, i.e. high odor concentration, glomerular neuronal and metabolic responses are shaped by peripheral adaptation of olfactory sensory neurons. Eventually, we show the importance of oxygen diffusion processes from brain capillaries to neuronal tissue. We characterize how transient changes in blood flow are precisely influencing the oxygen tissue level.
