Neurons in the visual system of the blowfly have large receptive fields that are selective for specific optic flow fields. Here, we studied the neural mechanisms underlying flow–field selectivity in proximal Vertical System (VS)-cells, a particular subset of tangential cells in the fly. These cells have local preferred directions that are distributed such as to match the flow field occurring during a rotation of the fly. However, the neural circuitry leading to this selectivity is not fully understood. Through dual intracellular recordings from proximal VS cells and other tangential cells, we characterized the specific wiring between VS cells themselves and between proximal VS cells and horizontal sensitive tangential cells. We discovered a spiking neuron (Vi) involved in this circuitry that has not been described before. This neuron turned out to be connected to proximal VS cells via gap junctions and, in addition, it was found to be inhibitory onto VS1.