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Yet how metabolic supply adapts to shifting computational demands across brain states remains unclear. Using wide-field fluorescence imaging through the intact skull of live mice, we simultaneously monitored brain blood volume (BBV), astrocytic pyruvate, and neuronal ATP levels during natural sleep. We found that large-scale metabolic dynamics are coupled to neuronal activity but reorganize in a state-dependent manner. During non-rapid eye movement (NREM) sleep, theta-band electrocorticogram (ECoG) activity predicted subsequent blood volume changes, accompanied by rapid anterior-to-posterior vascular waves. In contrast, REM sleep was marked by a pronounced increase in BBV, originating in the posterior cortex and slowly propagating across the brain. This was accompanied by elevated astrocytic pyruvate; paradoxically, however, neuronal ATP levels declined sharply. 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