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Glucose is the major source of energy utilized by the brain and is transported by the blood. However, it has been proposed that neurons obtain most of their energy from extracellular lactate, a glucose metabolite produced by astrocytes. Interestingly, astrocytes provide a physical link to the vasculature by their perivascular endfoot processes and are organized in network thanks to extensive intercellular communication through gap junctions. The aim of this work was to determine whether the connectivity of local astrocyte networks contributes to their metabolic supportive function to neurons. The expression of connexins 43 and 30 (Cx43, Cx30), the two main gap junction proteins in astrocytes, was particularly enriched in perivascular endfeet of astrocytes and delineated blood vessel walls in mouse hippocampal slices. Glucose trafficking dynamics was examined at the single-cell level using the fluorescent glucose derivative 2-NBDG (2- ([N-(7-nitrobenz-2-oxa-1,3-diazol-4-yl)amino]-2 deoxyglucose). When injected for 20 minutes by whole cell recordings in single astrocytes lining blood vessels, 2-NBDG diffused through the astrocyte gap junction-mediated network, with a preferential pathway along interconnected astrocyte endfeet around blood vessels. This traffic was activity dependent, being reduced in the presence of TTX and increased during repetitive synaptic stimulation or epileptic conditions, and involved the activation of glutamatergic AMPA receptors. Interestingly, the permeability of Cx43, but not Cx30, was selectively regulated by glutamatergic neuronal activity. In contrast 2-NBDG, dialysed in CA1 pyramidal cells or interneurons, did not diffuse to other cells. Exogenous glucose deprivation induces a slow depression of synaptic transmission in hippocampal slices, suggesting that intrinsic energy reserves sustain neurotransmission. To test whether glucose from astrocytic networks can sustain synaptic activity, fEPSPs were recorded during exogenous glucose deprivation, while dialysing intracellularly glucose in a single astrocyte via a patch pipette. Depression of fEPSP during exogenous glucose deprivation was inhibited when glucose was administered to the astrocytic network. This effect was not caused by leakage of glucose in the extracellular space, as it was not observed in the double knockout mice for Cx30 and Cx43, devoid of gap-junction coupling. Altogether these results indicate that gap junctions play a role in the metabolic supportive function of astrocytes by providing an activity-dependent intercellular route for glucose delivery from blood vessels to distal neurons.