Age-related decline in brain glucose utilization might stem from noradrenergic system dysfunction, which governs brain metabolism and could play a role in age-related cognitive decline. Noradrenaline released from these neurons triggers intracellular Ca2+ and cAMP signals in astrocytes, facilitating glucose uptake, glycogen degradation, and aerobic glycolysis, producing lactate as an end-product. During heightened brain activity, lactate is transferred from astrocytes to neurons to serve as fuel. The extent to which noradrenergic regulation of brain cell metabolism is impaired in aged brains and contributes to locomotion and cognitive decline remains poorly understood. To explore this, we utilized fluorescent sensors for Ca2+, cAMP, glucose, and lactate in young and aged Drosophila brains to monitor changes in intracellular second messengers and metabolites following octopamine stimulation (an invertebrate analogue of noradrenaline). Octopamine triggered Ca2+ signals in neurons and glial cells in young brains, but not in aged brains. Furthermore, octopamine induced intracellular cAMP signalling and lactate increases exclusively in neurons, suggesting that cAMP-mediated aerobic glycolysis predominantly occurs in neurons. This was unaffected by aging. In contrast, octopamine increased cytosolic glucose levels (glucose uptake) only in astrocytes, a response absent in aged brains. Upon exposure to elevated extracellular glucose or lactate levels, both neurons and glial cells could uptake nutrients, although glucose uptake in neurons was reduced in aged brains. Our findings imply impaired octopaminergic Ca2+ signalling in brain cells, reduced glucose uptake in astrocytes, and reduced glucose delivery to neurons in aged Drosophila brains, likely contributing to age-related locomotion and cognitive deficits.