The Organization of the Second Optic Chiasm of the Drosophila Optic Lobe.

Kazunori Shinomiya,Meagan Wiederman,Sari Mclin,Jane Anne Horne,Ian A Meinertzhagen,Aljoscha Nern,Stephen M Plaza

doi:10.3389/fncir.2019.00065

Kazunori Shinomiya, Meagan Wiederman + Show 5 more

Open Access

https://doi.org/10.3389/fncir.2019.00065

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Abstract

Visual pathways from the compound eye of an insect relay to four neuropils, successively the lamina, medulla, lobula, and lobula plate in the underlying optic lobe. Among these neuropils, the medulla, lobula, and lobula plate are interconnected by the complex second optic chiasm, through which the anteroposterior axis undergoes an inversion between the medulla and lobula. Given their complex structure, the projection patterns through the second optic chiasm have so far lacked critical analysis. By densely reconstructing axon trajectories using a volumetric scanning electron microscopy (SEM) technique, we reveal the three-dimensional structure of the second optic chiasm of Drosophila melanogaster, which comprises interleaving bundles and sheets of axons insulated from each other by glial sheaths. These axon bundles invert their horizontal sequence in passing between the medulla and lobula. Axons connecting the medulla and lobula plate are also bundled together with them but do not decussate the sequence of their horizontal positions. They interleave with sheets of projection neuron axons between the lobula and lobula plate, which also lack decussations. We estimate that approximately 19,500 cells per hemisphere, about two thirds of the optic lobe neurons, contribute to the second chiasm, most being Tm cells, with an estimated additional 2,780 T4 and T5 cells each. The chiasm mostly comprises axons and cell body fibers, but also a few synaptic elements. Based on our anatomical findings, we propose that a chiasmal structure between the neuropils is potentially advantageous for processing complex visual information in parallel. The EM reconstruction shows not only the structure of the chiasm in the adult brain, the previously unreported main topic of our study, but also suggest that the projection patterns of the neurons comprising the chiasm may be determined by the proliferation centers from which the neurons develop. Such a complex wiring pattern could, we suggest, only have arisen in several evolutionary steps.

Highlights

Visual input from photoreceptors in the fly’s compound eye is relayed to four neuropils (Figure 1A), the lamina and medulla, between which the visual field undergoes an anteroposterior inversion, and two deeper neuropils, the lobula and lobula plate, which face each other at right angles to the medulla
The FIB-scanning electron microscopy (SEM) image volume we used for this study covers the entire depth of the medulla, lobula, and lobula plate, as well as the proximal part of the lamina (Figure 2A; Shinomiya et al, 2019)
We report the presence and organization of the two patterns of axon trajectory, in sheets and bundles, respectively, within the second optic chiasm of Drosophila, and the cell types that contribute these

Summary

Introduction

Visual input from photoreceptors in the fly’s compound eye is relayed to four neuropils (Figure 1A), the lamina and medulla, between which the visual field undergoes an anteroposterior inversion, and two deeper neuropils, the lobula and lobula plate, which face each other at right angles to the medulla. In Drosophila, each column of the medulla contains a fixed group of 27 columnar neurons that includes 17 medulla cells and 10 input terminals from the lamina (Shinomiya et al, 2015; Takemura et al, 2015), the latter projecting to the medulla through the first (or outer) optic chiasm (OCH1; Figure 1B; Meinertzhagen and O’Neil, 1991). Axons of the lamina neurons invert their antero-posterior positions by crossing in the first chiasm, resulting in information from the anterior visual field projecting to the posterior side of the medulla, and vice versa. Axon sheets pass between lobula and lobula plate, while axon bundles connect the proximal medulla with the distal lobula, inverting the retinal topology in an antero-posterior plane. The deepest columns of the lobula and lobula plate receive signals from the posterior eye field, in consequence of the two topological crossings in the consecutive chiasmata

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