Diversity and wiring variability of visual local neurons in the Drosophila medulla M6 stratum

Abstract

Local neurons in the vertebrate retina are instrumental in transforming visual inputs to extract contrast, motion, and color information and in shaping bipolar-to-ganglion cell transmission to the brain. In Drosophila, UV vision is represented by R7 inner photoreceptor neurons that project to the medulla M6 stratum, with relatively little known of this downstream substrate. Here, using R7 terminals as references, we generated a 3D volume model of the M6 stratum, which revealed a retinotopic map for UV representations. Using this volume model as a common 3D framework, we compiled and analyzed the spatial distributions of more than 200 single M6-specific local neurons (M6-LNs). Based on the segregation of putative dendrites and axons, these local neurons were classified into two families, directional and nondirectional. Neurotransmitter immunostaining suggested a signal routing model in which some visual information is relayed by directional M6-LNs from the anterior to the posterior M6 and all visual information is inhibited by a diverse population of nondirectional M6-LNs covering the entire M6 stratum. Our findings suggest that the Drosophila medulla M6 stratum contains diverse LNs that form repeating functional modules similar to those found in the vertebrate inner plexiform layer. J. Comp. Neurol. 522:3795–3816, 2014. © 2014 Wiley Periodicals, Inc.

Modality-specific circuits for skylight orientation in the fly visual system

“…We found that the typical layer-specific targeting of R7 (to layer M6) and R8 (to M3) observed across the medulla 19 is different in DRA columns, where both R7 and R8 terminate in M6, with one cell always terminating slightly more distally ( Figure 1D). In agreement with previous reports 32 , we found that this layer targeting pattern could be ectopically induced by transforming all ommatidia into the DRA fate in flies via overexpression of the transcription factor Homothorax in all photoreceptors (GMR-Hth) 26,43 , ( Figure 1E). Quantification of the distance between R7 and R8 terminals in the medulla revealed a sharp boundary between DRA-specific and non-DRA layer targeting of inner photoreceptor cells ( Figure 1F).…”

“…Interestingly, R8 cells in DRA ommatidia (here referred to as DRA.R8) resemble R7 cells in that they express an R7 Rhodopsin (Rh3), and down-regulate the crucial R8-specific transcription factor Senseless (Sens) around mid-pupation 26,31 . Furthermore, only in the DRA, R8 axons target to the deeper medulla layer M6, known to be the R7 target layer across the medulla 32 , whereas non-DRA R8 always terminate in layer M3 19 . Differences in layer targeting are known to be crucial for correct synaptic partner choice by photoreceptors 33 .…”

Retinal perception and ecological significance of color vision in insects

“…Although X. peckii shows some preference for UV light, which is likely to be mediated by the UV-sensitive of one of the two Opsins found in the genome [67], it might only have basic color vision. Another reduction in connectivity can be observed in the fly medulla: While in the main eye, R7 and R8, the inner photoreceptors responsible for color detection, project to two different layers in the medulla (M6 and M3), the synapses collapse to one layer (M6) for monochromatic photoreceptors located in the dorsal rim area (DRA) [68] where the orientation of the vector of polarized light rather than colors is processed.…”

From the Eye to the Brain

“…The medulla neuropil is organized in repetitive columnar units, oriented perpendicular to the ten layers that are reminiscent of lamina cartridges (Fischbach and Dittrich 1989). Retinotopic connections between medulla columns, photoreceptors and lamina cartridges ensure an accurate representation of the visual world (Fischbach and Dittrich 1989, Meinertzhagen and Sorra 2001, Morante and Desplan 2008, Zhu 2013, Chin et al 2014). …”