Representations of optic flow are encoded in fly tangential neurons by pooling the signals of many retinotopically organized local motion‐sensitive inputs as well as of other tangential cells originating in the ipsi‐ and contralateral half of the brain. In the so called HSE cell, a neuron involved in optomotor course control, two contralateral input elements, the H1 and H2 cells, mediate distinct EPSPs. These EPSPs frequently elicit spike‐like depolarizations in the HSE cell. The synaptic transmission between the H2 and the HSE cell is analysed in detail and shown to be very reliable with respect to the amplitude and time‐course of the postsynaptic potential. As a consequence of its synaptic input, the HSE cell responds best to wide‐field motion, such as that generated on the eyes when the animal turns about its vertical body axis. It is shown that the specificity of the HSE cell for this type of optic flow is much enhanced if rapid membrane depolarizations, such as large‐amplitude EPSPs or spike‐like depolarizations, are taken into account rather than the average membrane potential.