Abstract
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. In the present study, we proposed a spiking neural circuit model of the EB and the protocerebral bridge(PB) based on recent anatomical studies of the central complex. Our data-driven model describes two coupled recurrent circuits formed by four classes of neurons. Our analysis showed that one recurrent circuit, the C ring, forms strong local feedback with a symmetric ring while the other recurrent circuit, the P ring, is characterized by an asymmetric ring. Computer simulations demonstrated distinct functions performed by the two ring circuits. The C ring circuit was able to sustain a stable activity bump that represents the orientation of a salient visual cue and the bump persisted after cue offset. The P ring circuit, on the other hand, shifted the activity bump in the absence of the visual cue when the PB receives a unilateral input. We argued that P ring circuit is capable of integrating the angular path and this bump shifting function represents the ability of the fly to maintain spatial orientation when it rotates in the dark. A further connectome analysis indicated that the auditory system, which hosts the gravitational sensory neurons, may provide the unilateral input to the PB. The present model reproduces several key features of the EB activity and makes experimentally testable predictions, providing new insight into how spatial orientation is maintained and tracked at the cellular level.