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Color vision is an important sensory capability that enhances the detection of contrast in retinal images. Monochromatic animals exclusively detect temporal and spatial changes in luminance, whereas two or more types of photoreceptors and neuronal circuitries for the comparison of their responses enable animals to differentiate spectral information independent of intensity. Much of what we know about the cellular and physiological mechanisms underlying color vision comes from research on vertebrates including primates. In insects, many important discoveries have been made, but direct insights into the physiology and circuit implementation of color vision are still limited. Recent advances inDrosophilasystems neuroscience suggest that a complete insect color vision circuitry, from photoreceptors to behavior, including all elements and computations, can be revealed in future. Here, we review fundamental concepts in color vision alongside our current understanding of the neuronal basis of color vision inDrosophila,including side views to selected other insects.

Motion vision is a major function of all visual systems, yet the underlying neural mechanisms and circuits are still elusive. In the lamina, the first optic neuropile of Drosophila melanogaster, photoreceptor signals split into five parallel pathways, L1-L5. Here we examine how these pathways contribute to visual motion detection by combining genetic block and reconstitution of neural activity in different lamina cell types with whole-cell recordings from downstream motion-sensitive neurons. We find reduced responses to moving gratings if L1 or L2 is blocked; however, reconstitution of photoreceptor input to only L1 or L2 results in wild-type responses. Thus, the first experiment indicates the necessity of both pathways, whereas the second indicates sufficiency of each single pathway. This contradiction can be explained by electrical coupling between L1 and L2, allowing for activation of both pathways even when only one of them receives photoreceptor input. A fundamental difference between the L1 pathway and the L2 pathway is uncovered when blocking L1 or L2 output while presenting moving edges of positive (ON) or negative (OFF) contrast polarity: blocking L1 eliminates the response to moving ON edges, whereas blocking L2 eliminates the response to moving OFF edges. Thus, similar to the segregation of photoreceptor signals in ON and OFF bipolar cell pathways in the vertebrate retina, photoreceptor signals segregate into ON-L1 and OFF-L2 channels in the lamina of Drosophila.

The nervous system of seeing animals derives information about optic flow in two subsequent steps. First, local motion vectors are calculated from moving retinal images, and second, the spatial distribution of these vectors is analyzed on the dendrites of large downstream neurons. In dipteran flies, this second step relies on a set of motion-sensitive lobula plate tangential cells (LPTCs), which have been studied in great detail in large fly species. Yet, studies on neurons that convey information to LPTCs and neuroanatomical investigations that enable a mechanistic understanding of the underlying dendritic computations in LPTCs are rare. We investigated the subcellular distribution of nicotinic acetylcholine receptors (nAChRs) on two sets of LPTCs: vertical system (VS) and horizontal system (HS) cells in Drosophila melanogaster. In this paper, we describe that both cell types express Dalpha7-type nAChR subunits specifically on higher order dendritic branches, similar to the expression of gamma aminobutyric acid (GABA) receptors. These findings support a model in which directional selectivity of LPTCs is achieved by the dendritic integration of excitatory, cholinergic, and inhibitory GABA-ergic input from local motion detectors with opposite preferred direction. Nonetheless, whole-cell recordings in mutant flies without Dalpha7 nAChRs revealed that direction selectivity of VS and HS cells is largely retained. In addition, mutant LPTCs were responsive to acetylcholine and remaining nAChR receptors were labeled by alpha-bungarotoxin. These results in LPTCs with genetically manipulated excitatory input synapses suggest a robust cellular implementation of dendritic processing that warrants direction selectivity. The underlying mechanism that ensures appropriate nAChR-mediated synaptic currents and the functional implications of separate sets or heteromultimeric nAChRs can now be addressed in this system.

SummaryThe crystalline-like structure of the optic lobes of the fruit fly Drosophila melanogaster has made them a model system for the study of neuronal cell-fate determination, axonal path finding, and target selection. For functional studies, however, the small size of the constituting visual interneurons has so far presented a formidable barrier. We have overcome this problem by establishing in vivo whole-cell recordings [1] from genetically targeted visual interneurons of Drosophila. Here, we describe the response properties of six motion-sensitive large-field neurons in the lobula plate that form a network consisting of individually identifiable, directionally selective cells most sensitive to vertical image motion (VS cells [2, 3]). Individual VS cell responses to visual motion stimuli exhibit all the characteristics that are indicative of presynaptic input from elementary motion detectors of the correlation type [4, 5]. Different VS cells possess distinct receptive fields that are arranged sequentially along the eye's azimuth, corresponding to their characteristic cellular morphology and position within the retinotopically organized lobula plate. In addition, lateral connections between individual VS cells cause strongly overlapping receptive fields that are wider than expected from their dendritic input. Our results suggest that motion vision in different dipteran fly species is accomplished in similar circuitries and according to common algorithmic rules. The underlying neural mechanisms of population coding within the VS cell network and of elementary motion detection, respectively, can now be analyzed by the combination of electrophysiology and genetic intervention in Drosophila.

The Journal of Neurogenetics presents this special issue to honor the lifelong contributions of Karl-Friedrich Fischbach on the occasion of his retirement from university duties in March 2014. Karl...

Motion vision is essential for navigating through the environment. Due to its genetic amenability, the fruit fly Drosophila has been serving for a lengthy period as a model organism for studying optomotor behavior as elicited by large-field horizontal motion. However, the neurons underlying the control of this behavior have not been studied in Drosophila so far. Here we report the first whole cell recordings from three cells of the horizontal system (HSN, HSE, and HSS) in the lobula plate of Drosophila. All three HS cells are tuned to large-field horizontal motion in a direction-selective way; they become excited by front-to-back motion and inhibited by back-to-front motion in the ipsilateral field of view. The response properties of HS cells such as contrast and velocity dependence are in accordance with the correlation-type model of motion detection. Neurobiotin injection suggests extensive coupling among ipsilateral HS cells and additional coupling to tangential cells that have their dendrites in the contralateral hemisphere of the brain. This connectivity scheme accounts for the complex layout of their receptive fields and explains their sensitivity both to ipsilateral and to contralateral motion. Thus the main response properties of Drosophila HS cells are strikingly similar to the responses of their counterparts in the blowfly Calliphora, although we found substantial differences with respect to their dendritic structure and connectivity. This long-awaited functional characterization of HS cells in Drosophila provides the basis for the future dissection of optomotor behavior and the underlying neural circuitry by combining genetics, physiology, and behavior.