Maintaining spatial orientation when carrying out goal-directed movements requires an animal to perform angular path integration. Such functionality has been recently demonstrated in the ellipsoid body (EB) of fruit flies, though the precise circuitry and underlying mechanisms remain unclear. We analyze recently published cellular-level connectomic data and identify the unique characteristics of the EB circuitry, which features coupled symmetric and asymmetric rings. By constructing a spiking neural circuit model based on the connectome, we reveal that the symmetric ring initiates a feedback circuit that sustains persistent neural activity to encode information regarding spatial orientation, while the asymmetric rings are capable of integrating the angular path when the body rotates in the dark. The present model reproduces several key features of EB activity and makes experimentally testable predictions, providing new insight into how spatial orientation is maintained and tracked at the cellular level.Ellipsoid body (EB) neurons in the fruit fly represent the animal heading through a bump-like activity dynamics. Here the authors report a connectome-driven spiking neural circuit model of the EB and the protocerebral bridge (PB) that can maintain and update an activity bump related to the spatial orientation.