Neuronal circuits integrating visual motion information in Drosophila

The detection of visual motion enables sophisticated animal navigation, and studies in flies have provided profound insights into the cellular and circuit basis of this neural computation. The fly's directionally selective T4 and T5 neurons respectively encode ON and OFF motion. Their axons terminate in one of four retinotopic layers in the lobula plate, where each layer encodes one of four cardinal directions of motion. While the input circuitry of the directionally selective neurons has been studied in detail, the synaptic connectivity of circuits integrating T4/T5 motion signals is largely unknown. Here we report a 3D electron microscopy reconstruction, wherein we comprehensively identified T4/T5's synaptic partners in the lobula plate, revealing a diverse set of new cell types and attributing new connectivity patterns to known cell types. Our reconstruction explains how the ON and OFF motion pathways converge. T4 and T5 cells that project to the same layer, connect to common synaptic partners symmetrically, that is with similar weights, and also comprise a core motif together with bilayer interneurons, detailing the circuit basis for computing motion opponency. We discovered pathways that likely encode new directions of motion by integrating vertical and horizontal motion signals from upstream T4/T5 neurons. Finally, we identify substantial projections into the lobula, extending the known motion pathways and suggesting that directionally selective signals shape feature detection there. The circuits we describe enrich the anatomical basis for experimental and computations analyses of motion vision and bring us closer to understanding complete sensory-motor pathways.

The complex optic lobe of dragonflies

SummaryDragonflies represent an ancient lineage of visual predators, which last shared a common ancestor with insect groups such as dipteran flies in the early Devonian, 406 million years ago [1,2]. Despite their important evolutionary status, and recent interest in them as a model for complex visual physiology and behavior, the most recent detailed description of the dragonfly optic lobe is itself more than a century old [3]. Many insects process visual information in optic lobes comprising 4 sequential, retinotopically organized neuropils: the lamina, medulla, lobula and a posterior lobula plate devoted to processing information about wide-field motion stimuli [4, 5]. Recent reports suggest that the dragonflies also follow this basic plan, with a divided lobula similar to those of flies, moths and butterflies [6, 7]. Here we refute this claim, showing that dragonflies have an unprecedentedly complex lobula comprising at least 4 sequential synaptic neuropils, in addition to two lobula plate like structures located on opposite sides of the brain. The second and third optic ganglia contain approximately twice as many synaptic layers as any other insect group yet studied. Using intracellular recording and labeling of neurons we further show that the most anterior lobe contains wide-field motion processing tangential neurons similar to those of the posterior lobula plate of dipteran flies. In addition to describing what is probably the most complex and unique optic lobe of any insect to date, our findings provide interesting insights to understanding the evolution of the insect optic lobe and serve as a reminder that the highly studied visual circuits of dipteran flies represent just a single derived form of these brain structures.

Spatio-temporal relays control layer identity of direction-selective neuron subtypes in Drosophila

Visual motion detection in sighted animals is essential to guide behavioral actions ensuring their survival. In Drosophila, motion direction is first detected by T4/T5 neurons. Their axons innervate one of four lobula plate layers. How T4/T5 neurons with layer-specific representation of motion-direction preferences are specified during development is unknown. We show that diffusible Wingless (Wg) between adjacent neuroepithelia induces its own expression to form secondary signaling centers. These activate Decapentaplegic (Dpp) signaling in adjacent lateral tertiary neuroepithelial domains dedicated to producing layer 3/4-specific T4/T5 neurons. T4/T5 neurons derived from the core domain devoid of Dpp signaling adopt the default layer 1/2 fate. Dpp signaling induces the expression of the T-box transcription factor Optomotor-blind (Omb), serving as a relay to postmitotic neurons. Omb-mediated repression of Dachshund transforms layer 1/2-into layer 3/4-specific neurons. Hence, spatio-temporal relay mechanisms, bridging the distances between neuroepithelial domains and their postmitotic progeny, implement T4/T5 neuron-subtype identity.