Population morphology implies a common developmental blueprint for Drosophila motion detectors

Abstract

Abstract 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). Crucially, the dendrites of these neurons are oriented inversely to the functional direction of motion which they encode. This dendritic orientation is what ultimately determines their functional directional encoding. The development of these neurons is well characterised up to the point of neuropil innervation. However, the full population of these neurons innervate their target neuropil prior to the emergence of directionality within their dendrites. As it stands, development prior to the emergence of dendritic orientations, and the adult oriented dendrite are both well understood, but the key components relating to the emergence of orientation itself are missing. Recent whole-brain electron microscopy (EM) connectomes of Drosophila melanogaster provide an unprecedented level of resolution and completeness when considering the morphology of neurons. Utilising this, we isolate the dendritic arbour of every T4 and T5 neuron within a female adult Drosophila brain, made available through FAFB-FlyWire. In doing so we are able to rigorously quantify the morphology of these dendrites in order to understand their similarities and differences. In doing so we aim to shed light on the origins of dendritic directionality. We reason that either this emerges through a tightly controlled, subtype specific mechanism, or is the result of a subtype agnostic mechanism and external factors. In the former case, we would expect evidence of this in differences between the morphological structure of individual dendrites between T4 and T5, and their subtypes. Our analysis however 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 mechanism of directed outgrowth, as opposed to symmetry breaking emerging through neuron type or subtype specific mechanisms. Author summary The Dendrites of T4 and T5 neurons orient spatially in a direction inverse to the direction of motion which they encode. The development of these neurons is understood up to the point of neuropil innervation, however they remain unicolumnar. The window between the directed adult dendrite, and their unicolumnar neuropil innervation is not yet understood. In order to shed light on how directionality within these dendrites may emerge, we perform a rigorous quantification of the morphology of all T4 and T5 dendrites within a single female adult Drosophila brain using nm -resolution reconstructions available from recent electron microscopy. This allows for the characterisation of neuropil and directionally specific morphological similarities and differences within this population. Although insightful variability is observed at the level of spatial properties of these dendrites, their geometry and topology is highly conserved across T4 and T5 populations, and directions of outgrowth. 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 process of dendritic outgrowth and emergence of orientation is most likely shared across both T4 and T5 and their subtypes.