RobustCircuit Project 5

Project 5 focuses on the robustness of circuit function to variable and challenging environmental stimulation based on variable connectivity and physiological properties of the Tm9 interneuron in the Drosophila motion detection circuit.

Imprecision: The optic lobe OFF pathway interneuron Tm9 has the capacity to change its physiological properties depending on cell type-specific presynaptic input. Tm9 presynaptic input partners are variable and may thereby influence Tm9’s variable physiological properties.

Robustness: Motion detection is an essential and highly robust behavior based on the function of an intensely studied neural circuit. Tm9 is the most critical component for robust OFF pathway function, despite (or because of) its variability.

Hypothesis: Tm9 utilizes imprecise partner choice based on spatiotemporal vicinity to make distributed contacts. This leads to individually variable physiological properties at a single cell level and robustness of circuit function at the cell population level.

Project Summary

Flies can respond robustly to variable visual stimuli, but the neuronal substrate and computation underlying behavioral robustness are largely unknown. Tm9 neurons are retinotopically arranged columnar interneurons that are part of the core motion-detection circuitry, and are required for robust optomotor behavior in Drosophila. Recent work has shown that Tm9, unlike other Tm neurons, can receive a wide variety of presynaptic inputs, which may differ for individual Tm9 neurons. Our preliminary work has also revealed morphological and functional variability in one distinct cell type presynaptic to Tm9, the distal medulla neuron Dm4. Furthermore, our 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 Tm9 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 (1) robustness to developmental noise and perturbation as well as (2) functional robustness to variable visual inputs. In two parallel parts of the project, we will (1) quantify and manipulate the variable presynaptic columnar circuit architecture of Tm9, and we will (2) analyze the contribution of the Dm4 wide-field neuron as a major heterogeneous input to Tm9. When these studies are concluded, we will have tested the role of a genetically encoded ability to form synapses with variable partners and heterogeneous Tm9 functional properties for the robustness of motion detection to challenging stimulus conditions.

References

1. Henning M, Ramos-Traslosheros G, Gür B, Silies M. (2022). Populations of local direction-selective cells encode global motion patterns generated by self-motion. Sci Adv. 2022 Jan 21;8(3):eabi7112.
2. Ramos-Traslosheros G, Silies M. (2021). The physiological basis for contrast opponency in motion computation in Drosophila. Nat Commun. 2021 Aug 17;12(1):4987.
3. Ketkar MD, Sporar K, Gür B, Ramos-Traslosheros G, Seifert M, Silies M (2020). Luminance Information Is Required for the Accurate Estimation of Contrast in Rapidly Changing Visual Contexts. Current Biology, 30: 657-669
4. Gür B, Sporar K, Lopez-Behling A, Silies M (2020). Distinct expression of potassium channels regulates visual response properties of lamina neurons in Drosophila melanogaster. J Comp Phys A, 206: 273-287.
5. Molina-Obando S, Vargas-Fique JF, Henning M, Gür B, Schladt TM, Akhtar J, Berger TK, Silies M (2019). ON selectivity in Drosophila vision is a multisynaptic process involving both glutamatergic and GABAergic inhibition. eLife, pii: e49373. doi: 10.7554/eLife.49373
6. Fisher YE, Leong JCS, Sporar K, Ketkar MD, Gohl DM, Clandinin TR and Silies M. (2015) A visual pathway with wide field properties is required for elementary motion detection. Current Biology 25(24): 3178 – 3189.