In many species, neurons responding to visual motion at higher processing stages are often specifically tuned to particular flow fields; however, the neural circuitry that leads to this selectivity is not yet understood. Here we have studied this problem in 'vertical system' (VS) cells of the blowfly lobula plate. These neurons possess distinctive local preferred directions in different parts of their receptive field. Dual recordings from pairs of VS cells show that they are electrically coupled. This coupling is responsible for the elongated horizontal extent of their receptive fields. VS cells with a lateral receptive field have additional connections to a VS cell with a frontal receptive field and to the horizontal system, tuning these cells to rotational flow fields. In summary, the receptive field of these cells consists of two components: one that they receive from local motion detectors on their dendrite, and one that they import from other large-field neurons.