Neural pathways underlying visually guided flight control in flies (Diptera): Evolutionary implications and phylogenetic consequences of cellular architecture

Abstract

In dipteran brains, a motion sensitive but color insensitive, pathway consists of large diameter neurons, organized as a precise retinotopic map. Several cell classes can be uniquely identified by their shapes, projections and relative positions in the neuropil. Morphological comparisons of small-field neurons in the second visual neuropil, the medulla, in 16 dipteran taxa reveal that those neurons that are involved in elementary motion computation are conserved in aspects that are expected to contribute to the functional pathway, but vary moderately in shape and cell decorations. On the other hand large-field neurons of the third visual neuropil, the lobula plate (LP), vary considerably in their numbers, shapes and positions within the mosaic. Those are neurons that integrate information from arrays of EMDs in a taxon-specific way. Because of the map-like organization of this neuropil, differences in cell size, architecture and cell number are of major functional consequence. Character evolution studies suggest that specific LP organizations are indeed tightly connected with specific functional properties; namely, differences that influence flight behavior. For example, the comparison of isomorphic vertical cells against hovering flight reveals multiple parallel origins of these two character traits. Other characters are closely associated with phylogenetic hypothesis, and no evolutionarily associated functional characteristics have been found. A parsimony analysis based on 32 neuroanatomical characters shows close similarities with conventional literature-derived hypotheses, suggesting the systematic value of neuroanatomical characters.