The hippocampus is able to rapidly learn incoming information, even if that information is only observed once. Furthermore, this information can be replayed in a compressed format in either forward or reverse modes during Sharp-Wave–Ripples (SPWRs). We leveraged state-of-the-art techniques in training recurrent spiking networks to demonstrate how primarily interneuron networks can achieve the following: (1) generate internal theta sequences to bind externally elicited spikes in the presence of inhibition from the medial septum; (2) compress learned spike sequences in the form of a SPWR when septal inhibition is removed; (3) generate and refine high-frequency assemblies during SPWR-mediated compression; and (4) regulate the inter-SPW interval timing between SPWRs in ripple clusters. From the fast timescale of neurons to the slow timescale of behaviors, interneuron networks serve as the scaffolding for one-shot learning by replaying, reversing, refining, and regulating spike sequences