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Abstract

Flies gain information about self-motion during free flight by processing images of the environment moving across their retina. The visual course control center in the brain of the blowfly contains, among others, a population of ten neurons, the so-called vertical system (VS) cells that are mainly sensitive to downward motion. VS cells are assumed to encode information about rotational optic flow induced by self-motion (Krapp and Hengstenberg 1996 Nature 384 463-6). Recent evidence supports a connectivity scheme between the VS cells where neurons with neighboring receptive fields are connected to each other by electrical synapses at the axonal terminals, whereas the boundary neurons in the network are reciprocally coupled via inhibitory synapses (Haag and Borst 2004 Nat. Neurosci. 7 628-34; Farrow et al 2005 J. Neurosci. 25 3985-93; Cuntz et al 2007 Proc. Natl Acad. Sci. USA). Here, we investigate the functional properties of the VS network and its connectivity scheme by reducing a biophysically realistic network to a simplified model, where each cell is represented by a dendritic and axonal compartment only. Eigenanalysis of this model reveals that the whole population of VS cells projects the synaptic input provided from local motion detectors on to its behaviorally relevant components. The two major eigenvectors consist of a horizontal and a slanted line representing the distribution of vertical motion components across the fly's azimuth. They are, thus, ideally suited for reliably encoding translational and rotational whole-field optic flow induced by respective flight maneuvers. The dimensionality reduction compensates for the contrast and texture dependence of the local motion detectors of the correlation-type, which becomes particularly pronounced when confronted with natural images and their highly inhomogeneous contrast distribution.