Control of Escape Behavior by Descending Neurons in Drosophila Melanogaster

To avoid predation, nervous systems detect looming motion cues from a predator's approach to generate evasive responses . Looming-sensitive visual neurons and escape-evoking giant neurons have been identified in mobile species across the animal kingdom (Eaton, 1984). In flies, escape is composed of a sequence of movements to initiate flight: freezing, postural adjustment, wing elevation and wing depression with leg extension. These sub-behaviors determine critical properties of the escape. Postural shifts determine escape direction (Card, 2008b). The giant fiber (GF) neuron's role in leg extension and wing depression for rapid takeoff has been well-characterized (Vonreyn, 2014), indicating that additional, unknown descending neurons must contribute to the control of the other sub-behaviors in the sequence. In this study, we characterize a group of eight descending neurons (LC4DNs) which may control escape by serving as parallel signaling pathways, connecting the same regions in the brain and ventral nerve cord (VNC) as the GF. Specifically, this group of neurons extends dendrites to an optic glomerulus formed by the axon terminals of a looming-sensitive (Vonreyn, 2017) visual projection neuron cell type called lobula columnar type 4 (LC4) (Namiki, 2018). In behavioral experiments, optogenetic activation of cell type-specific lines shows that select LC4DNs can evoke long-mode escapes, distinct from the GF-driven short-mode escapes. Whole-cell patch clamp recordings a subset of LC4DNs demonstrates similar looming-sensitivity and speed tuning, as would be expected from a common looming-sensitive input, like LC4. Finer analysis of LC4DN-activation reveals induced postural shifts that control escape direction, comparable to looming-evoked behavior. DNp11 activation generated forward jumps, whereas DNp02 and DNp04 co-activation induced backwards jumps. To determine a sensory input basis for directionality, we analyzed synaptic connectivity in an electron microscopy dataset (Zheng, 2018) to find inequalities in the number of synaptic connections between LC4 neurons and LC4DNs. Visualization of the LC4 dendrites reveals spatial gradients that are in opposite polarity to the activation-induced jump direction. These findings suggest a rapid feed-forward control mechanism by LC4DNs in which looming features are encoded by LC4 neurons and then filtered through a synaptic gradient that determines spatial selectivity of those features in specific DNs such that the fly generates postural shifts for escape away from the looming location