Early visual experience and the receptive-field organization of optic flow processing interneurons in the fly motion pathway

The distribution of local preferred directions and motion sensitivities within the receptive fields of so-called tangential neurons in the fly visual system was previously found to match optic flow fields as induced by certain self-motions. The complex receptive-field organization of the tangential neurons and the recent evidence showing that the orderly development of the fly's peripheral visual system depends on visual experience led us to investigate whether or not early visual input is required to establish the functional receptive field properties of such tangential neurons. In electrophysiological investigations of two identified tangential neurons, it turned out that dark-hatched flies which were kept in complete darkness for 2 days develop basically the same receptive-field organization as flies which were raised under seasonal light/dark conditions and were free to move in their cages. We did not find any evidence that the development of the sophisticated receptive-field organization of tangential neurons depends on sensory experience. Instead, the input to the tangential neurons seems to be "hardwired" and the specificity of these cells to optic flow induced during self-motions of the animal may have evolved on a phylogenetical time scale.