Variability and robustness of functional neuronal properties in visual motion-detection circuitry

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Flies can respond robustly to variable visual stimuli, but the neuronal substrate and computation underlying behavioral robustness are largely unknown. Neurons of the ON and OFF pathways of core-motion detection circuitry have been mapped in Drosophila. Of these, Tm9 neurons are retinotopically arranged columnar interneurons of the OFF pathway, and guide optomotor behavior. Recent work has shown that Tm9, unlike other Tm neurons, can receive a wide variety of presynaptic inputs, whose identity may differ for individual Tm9 neurons. Our preliminary work has also revealed morphological and functional variability in one non-columnar, wide-field cell type presynaptic to Tm9, the distal medulla neuron Dm4. Furthermore, optical functional recordings revealed a corresponding variability of individual Tm9 functional properties. These findings give rise to two hypotheses to be tested in P5: (1) variable synaptic inputs are essential to determine heterogeneous functional properties of Tm9 neurons, which (2) are in turn required for circuit function and lead to behavioral robustness to challenging stimulus conditions. Hence, the goal of P5 is to understand to what extent imprecisions in the presynaptic circuitry facilitates robustness to developmental noise as well as functional robustness to variable visual inputs. In two parallel parts of the project, we will first quantify and manipulate the variable presynaptic columnar circuit architecture of Tm9, and we will analyze the contribution of the Dm4 wide-field neuron as a major heterogeneous input to Tm9. To do so, we will combine anatomical studies with physiological measurements across the fly eye. We will genetically manipulate variable inputs and measure Tm9 physiology as well as behavioral responses to a range of visual stimuli. When concluded, we will have tested the role of imprecise synapse formation and heterogeneous Tm9 functional properties for the robustness of motion detection to challenging stimulus conditions.