Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly

The third visual neuropil (lobula plate) of the blowfly Calliphora erythrocephala is a center for processing motion information. Io contains, among others, 10 individually identifiable "vertical system" (VS) neurons responding to visual wide-field motions of arbitrary patterns. We demonstrate that each VS neuron is tuned to sense a particular aspect of optic flow that is generated during self-motion. Thus the VS neurons in the fly supply visual information for the control of head orientation, body posture, and flight steering. To reveal the functional organization of the receptive fields of the 10 VS neurons, we determined with a new method the distributions of local motion sensitivities and local preferred directions at 52 positions in the fly's visual field. Each neuron was identified by intracellular staining with Lucifer yellow and three-dimensional reconstructions from 10-mu m serial sections. Thereby the receptive-field organization of each recorded neuron could be correlated with the location and extent of its dendritic arborization in the retinotopically organized neuropil of the lobula plate. The response fields of the VS neurons, i.e., the distributions of local preferred directions and local motion sensitivities, are not uniform but resemble rotatory optic flow fields that would be induced by the fly during rotations around various horizontal axes. Theoretical considerations and quantitative analyses of the data, which will be presented in a subsequent paper, show that VS neurons are highly specialized neural filters for optic flow processing and thus for the visual sensation of self-motions in the fly.