A visual motion detection circuit suggested by Drosophila connectomics

Abstract

SummaryAnimal behavior arises from computations in neuronal circuits, but our understanding of these computations has been frustrated by the lack of detailed synaptic connection maps, or connectomes. For example, despite intensive investigations over half a century, the neuronal implementation of local motion detection in the insect visual system remains elusive. Here, we developed a semi-automated pipeline using electron microscopy to reconstruct a connectome, containing 379 neurons and 8,637 chemical synaptic contacts, within the Drosophila optic medulla. By matching reconstructed neurons to examples from light microscopy, we assigned neurons to cell types and assembled a connectome of the medulla's repeating module. Within this module, we identified cell types constituting a motion detection circuit and showed that the connections onto individual motion-sensitive neurons in this circuit were consistent with their direction selectivity. Our results identify cellular targets for future functional investigations, and demonstrate that connectomes can provide key insights into neuronal computations.

Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system

“…Studies using genetic methods for single-cell labeling have confirmed many of these cell types and newly identified others (8,9). For ∼60 cell types in two optic lobe subregions, the lamina and medulla, their synaptic connectivity has been revealed through serial-section electron microscopy (EM) (10)(11)(12)(13). Cell types that have arbors that span only one or a few medulla columns have been the easiest to characterize.…”

“…S3). We have previously used images from this collection, which will be further described and made available elsewhere, to validate shapes of EM-reconstructed optic lobe neurons (10). This dataset revealed several Dm neurons with processes in layers M1-M5, including cells that did not readily match previously described cell types, suggesting considerable uncharacterized Dm neuron diversity or variability.…”

“…How the processes of multicolumnar neurons, such as Dm cells, are distributed laterally across columns within medulla layers is largely unknown. Available Golgi drawings (3) primarily show side views, and EM reconstruction has so far been limited to volumes that are too small to reveal the full extent of most multicolumnar cells (10). Layer cross-section views of the arbors of individual cells of the different Dm cell types show a large diversity of size, orientation, and fine structure (Fig.…”

Connectome Networks: From Cells to Systems

“…In a more recent electron microscopic study, Takemura et al (2013) reconstructed a microscale circuit comprising 379 neurons and 8637 synapses within the optic medulla, a structure involved in visual motion detection. The circuit reconstruction revealed specific patterns of inter-neuronal connectivity that were consistent with the roles of individual neurons in generating direction selectivity.…”

A single-cell level and connectome-derived computational model of the Drosophila brain

“…While this is still a major challenge for large animals such as primates (Helmstaedter 2013), acquisition of single-cell level connectomes for small animals, such as the Drosophila melanogaster (fruit fly), has seen rapid progress (Chiang et al 2011;Takemura et al 2013;Shinomiya et al 2011). Therefore, we suggest that the Drosophila is currently one of the best model animals for developing a high-resolution full brain computational model due to the availability of extensive neuron databases and neuroinformatics tools (Chiang et al 2011;Shinomiya et al 2011;Osumi-Sutherland et al 2012;Parekh and Ascoli 2013;Ukani et al fly brain may enable us to investigate how different subsystems in the brain integrate and how high-level behavior is carried out.…”