A topographic visual pathway into the central brain of Drosophila

Abstract

The visual system is characterized by a strict topographic organization from the retina towards multiple layers of synaptic integration. Recent studies in Drosophila have shown that in the transition from the optic lobes to the central brain, due to convergence of columnar neurons onto optic glomeruli, distinct synaptic units employed in the computation of different visual features, the retinotopic representation is lost in these circuits. However, functional imaging revealed a spatial representation of visual cues in the Drosophila central complex, raising the question about the underlying circuitry, which bypasses optic glomerulus convergence.\n\nWhile characterizing afferent arborizations within Drosophila visual glomeruli, we discovered a spatial segregation of topographic and non-topographic projections from distinct molecular classes of medulla projection neurons, medullo-tubercular (MeTu) neurons, into a specific central brain glomerulus, the anterior optic tubercle (AOTu). Single cell analysis revealed that topographic information is organized by ensembles of MeTu neurons (type 1), forming parallel channels within the AOTu, while a separate class of MeTu neurons (type 2) displays convergent projection, associated with a loss of spatial resolution. MeTu afferents in the AOTu synapse onto a matching topographic field of output projection neurons, these tubercular-bulbar (TuBu) neurons relay visual information towards dendritic fields of central complex ring neurons in the bulb neuropil. Within the bulb, neuronal proximity of the topographic AOTu map as well as channel identity is maintained despite the absence of a stereotyped map organization, providing the structural basis for spatial representation of visual information in the central complex (CX). TuBu neurons project onto dendritic fields of efferent ring neurons, where distinct sectors of the bulb correspond to a distinct ring domain in the ellipsoid body. We found a stereotypic circuitry for each analyzed TuBu class, thus the individual channels of peripheral topography are maintained in the central complex structure. Together with previous data showing rough topography within the lobula AOTu domain, our results on the organization of medulla projection neurons define the AOTu neuropil as the main relay station for spatial information from the optic lobes into the central brain.