Connectome-based biophysical modeling of a figure-ground discrimination circuit

Figure-ground discrimination via relative motion represents a highly conserved visual computation essential for uncovering camouflage \citep{reichardt1983figure,Egelhaaf1985}. Over forty years ago, the Reichardt-Poggio-Hausen (RPH) model proposed a circuit architecture to explain this phenomenon, relying on an inhibitory wide-field pool cell to aggregate global motion and subsequently inhibit elementary motion detectors. Here we combine a whole-brain connectome of Drosophila with biophysical simulations to identify a reciprocal connection between T4a motion detectors and the wide-field ventral Centrifugal Horizontal cell. The anatomical feedback from vCH lands on T4a axon terminals; simulated dendrites generate local direction-selective responses, whereas the terminals become selective for relative motion. The isolated reciprocal circuit is sufficient for this selectivity which is abolished by removing the return inhibition. Opponent-motion and interocular pathways strengthen the same computation. Thus, a single neuron using the biophysical mechanism of shunting inhibition, corresponding to an equilibrium potential close to the resting potential, can support distinct visual operations in separate compartments: local motion in its dendrites and relative motion in its axon.