Sleep is a crucial part of everyday life, but the neural networks that regulate behavioural manifestations of sleep are not fully understood. In the fruit fly Drosophila melanogaster, dorsal fan-shaped body neurons (dFBNs) sit at the centre of homeostatic sleep control: the neurons’ excitability increases with sleep drive, and their artificial activation induces sleep. Despite significant advances in understanding of the molecular events that regulate the activity of dFBNs, insight into how they impose sleep on the organism is still lagging. By combining optogenetics and in vivo patch-clamp recordings in the brain of the fly, we have identified two neuronal groups that show functional monosynaptic connections with dFBNs. These cells reside in the fan-shaped body, an area involved in navigation, which allows us to study the interaction between the encoding of sleep drive and cognitive computations in a tractable system. Understanding the behavioural relevance of these neurons, the computations that underly their role in behaviour, and the influence of dFBNs on these computations will enhance our understanding of the sleep control imposed by dFBNs, as well as form a crucial step towards a systems view of sleep.