Contrary to the intense debate about brain oxygen dynamics and its uncoupling in mammals, very little is known in birds. In zebra finches, picosecond optical tomography with a white laser and a streak camera can measure in vivo oxyhemoglobin (HbO2) and deoxyhemoglobin (Hb) concentration changes following physiologic stimulation (familiar calls and songs). Picosecond optical tomography showed sufficient submicromolar sensitivity to resolve the fast changes in the hippocampus and auditory forebrain areas with 250 μm resolution. The time course is composed of (1) an early 2-second-long event with a significant decrease in Hb and HbO2 levels of −0.7 and −0.9 μmol/L, respectively, (2) a subsequent increase in blood oxygen availability with a plateau of HbO2 (+ 0.3 μmol/L), and (3) pronounced vasodilatation events immediately after the end of the stimulus. One of the findings of our study is the direct link between blood oxygen level-dependent signals previously published in birds and our results. Furthermore, the early vasoconstriction event and poststimulus ringing seem to be more pronounced in birds than in mammals. These results in birds, tachymetabolic vertebrates with a long lifespan, can potentially yield new insights, e.g., into brain aging.