The bidirectional link between visual processing and optomotor flight behavior in Drosophila

Abstract

Animals that explore the world need to reliably move in a preplanned direction. With the optomotor response, flies stabilize a straight path during flight by visual feedback. Unintended deviations from a straight path are perceived as rotation of the scenery around the fly, and smooth syndirectional flight turns minimize the asymmetric optic flow. At the same time, voluntary turns cause optic flow that is indistinguishable from visual input due to involuntary, external causes. Therefore, a motor-command efference copy has been postulated to counteract reafferent sensory perceptions that arise from volitional actions, and to provide context to resolve the ambiguity in perception. In flies, HS (horizontal system) cells are thought to mediate optomotor responses to horizontal motion. During spontaneous flight saccades, HS cells have been shown to receive input that could function as an efference copy to mitigate stabilization reflexes. <br /> Here, I investigated how this putative efference copy suppresses the processing of visual motion in HS cells by recording intracellularly during tethered flight. First, it is shown that looming-elicited avoidance saccades exhibit similar effects as spontaneous saccades. Additionally, the visual experience of the looming stimulus influences the subsequent responses of HS cells. Importantly, an inhibitory efference copy suppresses the processing of excitatory optic flow during both left- and rightward saccadic turns. We found that this effect is limited to a subset of HS cells and does not markedly reduce responses to inhibitory optic flow. <br /> To refine our understanding of this efference copy mechanism and resolve the counter-intuitive findings, I reconstructed the reafferent visual input to each HS subtype during escape saccades. The reafference is biphasic and largely symmetric for left- and rightward saccades, and thus supports a functional role for reduced excitatory responses in both directions. In contrast, the reafference is not evidently different for HSS, which suggests a functional subdivision between subtypes. <br /> To improve our understanding of the efference copy function and flight control, I investigated the impact of DNp15, a descending neuron postsynaptic to HSN and HSE. Intracellular recordings show that DNp15 prefers rotational to translational optic flow by integrating binocular information and relays graded potentials. The connectome suggests that DNp15 controls head and flight turns during panoramic visual stimuli. Through silencing and activation experiments, it is found that this neuron is essential for slow optomotor turns of both the head and wings, but acts in conjunction with other descending neurons. <br /> This work contributes to our understanding of a feedforward pathway from vision to behavior and how visual processing is internally fine-tuned for behavioral context.