Oligodendrocytes (OLs) support axonal health by detecting axonal spiking and regulating metabolic coupling. This study shows that fast axonal spiking triggers calcium (Ca²⁺) signaling and glycolysis in OLs. OLs detect axonal activity through increases in extracellular potassium (K⁺) concentrations and activation of Kir4.1 channels, which regulate metabolite supply to axons. Pharmacological inhibition or OL-specific inactivation of Kir4.1 reduces activity-induced axonal lactate surges. Mice lacking oligodendroglial Kir4.1 exhibit lower resting lactate levels and altered glucose metabolism in axons, leading to late-onset axonopathy. These findings reveal that OLs detect fast axonal spiking through K⁺ signaling, enabling acute metabolic coupling and promoting axonal health. OLs produce and maintain myelin sheaths, essential for efficient neural communication. Axonal damage is a feature of aging and neurological disorders, and OLs play a crucial role in preserving neural circuits and long-term neuronal integrity. OLs support axonal energy metabolism through aerobic glycolysis, producing lactate that serves as an energy substrate for axons. OL-specific deletion of monocarboxylate transporter 1 (MCT1) leads to late-onset axonopathy, indicating the importance of lactate and/or pyruvate release from OLs for axonal health. Glutamatergic signaling stimulates glucose transporter 1 (GLUT1) expression in OLs, suggesting that axonal activity regulates OL metabolic support. Metabolite supply is facilitated by cytosolic channels within the myelin sheath, and disruptions in this system are associated with axonal damage. Mice deficient in the myelin proteolipid protein (PLP) develop severe axonal spheroids with age, possibly due to deficits in axonal transport, mitochondrial function, and energy homeostasis. OLs also provide antioxidant support and K⁺ buffering. Despite the known role of OLs in axonal energy metabolism, the molecular and cellular events involved in metabolic coupling remain unclear. Whether neuronal activity influences OLs to drive metabolic support is still unclear. Glutamatergic signaling may mediate long-term adjustment of oligodendroglial glucose uptake capacity, but what controls rapid and on-demand delivery of metabolites to axons remains unexplored. A key indicator of axonal activity is transient increases in extracellular K⁺ concentrations ([K⁺]ext), which depolarize OLs. The study hypothesized that activity-driven K⁺ signaling triggers rapid metabolic coupling between OLs and axons. Using optic nerve electrophysiology and two-photon imaging, the study found that high-frequency axonal spiking triggers a Ca²⁺ surge and accelerates glucose consumption in OLs. Axonal activity is detected by OLs through increases in [K⁺]ext and activation ofOligodendrocytes (OLs) support axonal health by detecting axonal spiking and regulating metabolic coupling. This study shows that fast axonal spiking triggers calcium (Ca²⁺) signaling and glycolysis in OLs. OLs detect axonal activity through increases in extracellular potassium (K⁺) concentrations and activation of Kir4.1 channels, which regulate metabolite supply to axons. Pharmacological inhibition or OL-specific inactivation of Kir4.1 reduces activity-induced axonal lactate surges. Mice lacking oligodendroglial Kir4.1 exhibit lower resting lactate levels and altered glucose metabolism in axons, leading to late-onset axonopathy. These findings reveal that OLs detect fast axonal spiking through K⁺ signaling, enabling acute metabolic coupling and promoting axonal health. OLs produce and maintain myelin sheaths, essential for efficient neural communication. Axonal damage is a feature of aging and neurological disorders, and OLs play a crucial role in preserving neural circuits and long-term neuronal integrity. OLs support axonal energy metabolism through aerobic glycolysis, producing lactate that serves as an energy substrate for axons. OL-specific deletion of monocarboxylate transporter 1 (MCT1) leads to late-onset axonopathy, indicating the importance of lactate and/or pyruvate release from OLs for axonal health. Glutamatergic signaling stimulates glucose transporter 1 (GLUT1) expression in OLs, suggesting that axonal activity regulates OL metabolic support. Metabolite supply is facilitated by cytosolic channels within the myelin sheath, and disruptions in this system are associated with axonal damage. Mice deficient in the myelin proteolipid protein (PLP) develop severe axonal spheroids with age, possibly due to deficits in axonal transport, mitochondrial function, and energy homeostasis. OLs also provide antioxidant support and K⁺ buffering. Despite the known role of OLs in axonal energy metabolism, the molecular and cellular events involved in metabolic coupling remain unclear. Whether neuronal activity influences OLs to drive metabolic support is still unclear. Glutamatergic signaling may mediate long-term adjustment of oligodendroglial glucose uptake capacity, but what controls rapid and on-demand delivery of metabolites to axons remains unexplored. A key indicator of axonal activity is transient increases in extracellular K⁺ concentrations ([K⁺]ext), which depolarize OLs. The study hypothesized that activity-driven K⁺ signaling triggers rapid metabolic coupling between OLs and axons. Using optic nerve electrophysiology and two-photon imaging, the study found that high-frequency axonal spiking triggers a Ca²⁺ surge and accelerates glucose consumption in OLs. Axonal activity is detected by OLs through increases in [K⁺]ext and activation of