Eye structure shapes neuron function inDrosophilamotion vision

Abstract

Many animals rely on vision to navigate through their environment. The pattern of changes in the visual scene induced by self-motion is the optic flow, which is first estimated in local patches by directionally selective (DS) neurons. But how should the arrays of DS neurons, each responsive to motion in a preferred direction at a specific retinal position, be organized to support robust decoding of optic flow by downstream circuits? Understanding this global organization is challenging because it requires mapping fine, local features of neurons across the animal's field of view. InDrosophila, the asymmetric dendrites of the T4 and T5 DS neurons establish their preferred direction, making it possible to predict DS responses from anatomy. Here we report that the preferred directions of fly DS neurons vary at different retinal positions and show that this spatial variation is established by the anatomy of the compound eye. To estimate the preferred directions across the visual field, we reconstructed hundreds of T4 neurons in a full brain EM volume and discovered unexpectedly stereotypical dendritic arborizations that are independent of location. We then used whole-head μCT scans to map the viewing directions of all compound eye facets and found a non-uniform sampling of visual space that explains the spatial variation in preferred directions. Our findings show that the organization of preferred directions in the fly is largely determined by the compound eye, exposing an intimate and unexpected connection between the peripheral structure of the eye, functional properties of neurons deep in the brain, and the control of body movements.

A comprehensive neuroanatomical survey of theDrosophilaLobula Plate Tangential Neurons with predictions for their optic flow sensitivity

“…We also found a group of LPT neurons whose axons pass through a tract frontal to the noduli of the central complex, just as they do in the blowfly brain. We therefore termed them the noduli group, which included the well-known H2 neuron (reconstruction reported in Zhao, et al (2022)), and 6 other cells, that we call Nod1-5 (2 of these cells have extremely similar morphology and connectivity, and so both are named as the type Nod1). We found all 4 neurons (vCal1-3, and dCal1) that Hausen (1987) described in the Calyx group, cells whose axons pass near the calyces of the mushroom bodies.…”

“…C. Top: a fly head model with lenses color-coded to illustrate retina positions. Bottom: viewing directions of all ommatidia in our reference compound eye (Zhao et al, 2022), presented as a Mollweide 2D projection. D. Anatomical positions in LOP mapped to ommatidia directions in ( C ) via set of reconstructed T4 neurons (Figure 2—figure supplement 1A).…”

Diversity of visual inputs to Kenyon cells of theDrosophilamushroom body

“…These are related to their receptive field size and position in the field of view of the animal. We used a newly developed 'eye-map', that allows the prediction of the receptive field of optic lobe neurons given the extent and location of their processes to extract receptive field size and position, to quantify these properties and relate them to their connectivity with KCγ-d's (Figure 4A) 50 . We first applied this methodology to direct and indirect VPNs from each neuropil to describe their individual receptive field properties and then extended our analysis to predict the visual receptive fields of individual KCγ-d's (Figure 4B, Figure 4 Supplement 1).…”

“…Only visual projection neurons with optic lobe processes in the left hemisphere were considered for receptive field analyses. Columnar markers (759 in total) as identified in 50 were used. Since most medulla VPNs considered in this study arborize between layers M6 and M8, we used M5 column markers that were previously identified through the reconstruction of Mi1 processes in layer M5.…”

“…Since most medulla VPNs considered in this study arborize between layers M6 and M8, we used M5 column markers that were previously identified through the reconstruction of Mi1 processes in layer M5. Lobular column markers were obtained by extension of the medulla column map to the lobula from interpolating the positions of 63 reconstructed TmY5a neurons, as described in Zhao et al 50 . Each columnar marker was mapped to an ommatidial viewing angle, directional vectors that were represented by points on a unit sphere (the "eyemap").…”