Discriminating External and Internal Causes for Heading Changes in Freely Flying Drosophila

As animals move through the world in search of resources, they change course in reaction to both external sensory cues and internally-generated programs. Elucidating the functional logic of complex search algorithms is challenging because the observable actions of the animal cannot be unambiguously assigned to externally- or internally-triggered events. We present a technique that addresses this challenge by assessing quantitatively the contribution of external stimuli and internal processes. We apply this technique to the analysis of rapid turns (“saccades”) of freely flying Drosophila melanogaster. We show that a single scalar feature computed from the visual stimulus experienced by the animal is sufficient to explain a majority (93%) of the turning decisions. We automatically estimate this scalar value from the observable trajectory, without any assumption regarding the sensory processing. A posteriori, we show that the estimated feature field is consistent with previous results measured in other experimental conditions. The remaining turning decisions, not explained by this feature of the visual input, may be attributed to a combination of deterministic processes based on unobservable internal states and purely stochastic behavior. We cannot distinguish these contributions using external observations alone, but we are able to provide a quantitative bound of their relative importance with respect to stimulus-triggered decisions. Our results suggest that comparatively few saccades in free-flying conditions are a result of an intrinsic spontaneous process, contrary to previous suggestions. We discuss how this technique could be generalized for use in other systems and employed as a tool for classifying effects into sensory, decision, and motor categories when used to analyze data from genetic behavioral screens. Author Summary: Researchers have spent considerable effort studying how specific sensory stimuli elicit behavioral responses and how other behaviors may arise independent of external inputs in conditions of sensory deprivation. Yet an animal in its natural context, such as searching for food or mates, turns both in response to external stimuli and intrinsic, possibly stochastic, decisions. We show how to estimate the contribution of vision and internal causes on the observable behavior of freely flying Drosophila. We developed a dimensionality reduction scheme that finds a one-dimensional feature of the visual stimulus that best predicts turning decisions. This visual feature extraction is consistent with previous literature on visually elicited fly turning and predicts a large majority of turns in the tested environment. The rarity of stimulus-independent events suggests that fly behavior is more deterministic than previously suggested and that, more generally, animal search strategies may be dominated by responses to stimuli with only modest contributions from internal causes.