RESUMEN
Many animals, including humans, navigate their surroundings by visual input, yet we understand little about how visual information is transformed and integrated by the navigation system. In Drosophila melanogaster, compass neurons in the donut-shaped ellipsoid body of the central complex generate a sense of direction by integrating visual input from ring neurons, a part of the anterior visual pathway (AVP). Here, we densely reconstruct all neurons in the AVP using FlyWire, an AI-assisted tool for analyzing electron-microscopy data. The AVP comprises four neuropils, sequentially linked by three major classes of neurons: MeTu neurons, which connect the medulla in the optic lobe to the small unit of anterior optic tubercle (AOTUsu) in the central brain; TuBu neurons, which connect the anterior optic tubercle to the bulb neuropil; and ring neurons, which connect the bulb to the ellipsoid body. Based on neuronal morphologies, connectivity between different neural classes, and the locations of synapses, we identified non-overlapping channels originating from four types of MeTu neurons, which we further divided into ten subtypes based on the presynaptic connections in medulla and postsynaptic connections in AOTUsu. To gain an objective measure of the natural variation within the pathway, we quantified the differences between anterior visual pathways from both hemispheres and between two electron-microscopy datasets. Furthermore, we infer potential visual features and the visual area from which any given ring neuron receives input by combining the connectivity of the entire AVP, the MeTu neurons' dendritic fields, and presynaptic connectivity in the optic lobes. These results provide a strong foundation for understanding how distinct visual features are extracted and transformed across multiple processing stages to provide critical information for computing the fly's sense of direction.
RESUMEN
A catalog of neuronal cell types has often been called a "parts list" of the brain, and regarded as a prerequisite for understanding brain function. In the optic lobe of Drosophila, rules of connectivity between cell types have already proven essential for understanding fly vision. Here we analyze the fly connectome to complete the list of cell types intrinsic to the optic lobe, as well as the rules governing their connectivity. We more than double the list of known types. Most new cell types contain between 10 and 100 cells, and integrate information over medium distances in the visual field. Some existing type families (transmedullary, lobula intrinsic, and lobula plate intrinsic) at least double in number of types, with implications for perception of color, motion, and form. We introduce a new family, serpentine medulla intrinsic, which has more types than any other, and three new families of types that span multiple neuropils. We demonstrate self-consistency of our cell types through automatic assignment of cells by distance in high-dimensional feature space, and provide further validation by selection of small subsets of discriminative features. Our work showcases the advantages of connectomic cell typing: complete and unbiased sampling, a rich array of features based on connectivity, and reduction of the connectome to a drastically simpler wiring diagram of cell types, with immediate relevance for brain function and development.