Significance Noninvasive brain imaging of humans identifies prominent networks related to sensory and cognitive functions in the resting state; however, the signaling hierarchy and directionality among these networks remain largely unknown. Integrating simultaneously recorded measures for network identification and regional energy metabolism, we propose metabolic connectivity mapping (MCM) as a novel measure to reveal signaling directionality in the human brain. Comparing simple “eyes closed” and “eyes open” conditions in healthy subjects, MCM revealed stable bidirectional signaling among visual cortices and top-down signaling from parietal control regions. Additional top-down signaling from a salience network occurs only during the eyes open condition. We propose MCM as a measure for investigating signaling directions among brain networks in healthy and diseased brains.