In the visual system of the blowfly Calliphora vicina, neurons of the vertical system (VS cells) integrate wide-field motion information from a retinotopic array of local motion detectors. In vivo calcium imaging reveals two distinct and separate receptive fields in these cells: a narrow dendritic receptive field corresponding to feedforward input from the local motion detectors and a broad axon terminal receptive field that additionally incorporates input from neighboring cells mediated by lateral axo-axonal gap junctions. We show that the axon terminal responses are linear interpolations of the dendritic responses, resulting in a robust population coding of optic flow parameters as predicted by previous modeling studies. Compartmental modeling shows that spatially separating the axonal gap junctions from the conductive load of the dendritic synapses increases the coupling strength of the gap junctions, making this interpolation possible.