Population Morphology Implies a Common Developmental Blueprint for Drosophila Motion Detectors

Detailed characterisation of neuronal morphology provides vital clues for understanding the wiring logic and development of neural circuits. As neuron arbours can both span large distances, and be densely interwoven, one major challenge is acquiring and quantifying fine structures for independent arbours over large spatial extents. Recent whole-brain electron microscopy (EM) connectomes of Drosophila melanogaster provide an ideal opportunity to study fly neuronal morphology at scale. Utilising this rich resource, we developed novel computational methods and morphological metrics to perform the most comprehensive morphological analysis of the dendrites of T4 and T5 neurons in the fly brain. T4 and T5 neurons are the first direction-selective neurons in the visual pathway. They are the most numerous cell types in the fly brain ([~] 6000 within each optic lobe) and as a population, their compact dendritic arbours span the entire visual field. They are classified into four subtypes (a, b, c, and d). Each subtype encodes one of four orthogonal motion directions (up, down, forwards, backwards). The dendrites of these neurons form in two distinct neuropils, the Medulla (T4) and the Lobula (T5), and respond to ON (light increments, T4) and OFF (light decrements, T5) motions. T4 and T5 neurons dendrites are oriented against their preferred direction of motion. However, the differences beyond their characteristic orientation, both between T4 and T5, as well as within subtypes, have remained poorly understood. Our analysis reveals a high degree of structural similarity between T4 and T5, and within their subtypes. Particularly, the geometry of branching, section orientation, and tree-graph structure of these dendrites show only minor variability, with no consistent separation between T4 and T5, or their subtypes. These results indicate that, despite forming in different neuropils, and serving distinct motion directions, T4 and T5 dendrites follow closely aligned morphological patterns. This suggests a shared developmental mechanism. Author summaryWith nm-resolution neuron morphologies available from recent electron microscopy-based reconstructions, we are able to extract and analyse the dendrites of all T4 and T5 neurons within the right optic lobe of a single adult Drosophila. Investigating elements of spatial embedding, geometry, and their graph-theoretical structure, we show brain region specific variability in the spatial occupancy of these dendrites, but high structural stereotypy. From these analyses, we conclude that although these dendrites originate in differing brain regions, with differing input partners, and perform differing, subtype-specific, detection of motion directions, the underlying developmental process is most likely shared across both T4 and T5 and their subtypes.