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To maintain stable flight, animals continuously perform trimming adjustments to compensate for internal and external perturbations. Whereas animals use many different sensory modalities to detect such perturbations, insects rely extensively on optic flow to modify their motor output and remain on course. We studied this behavior in the fruit fly, Drosophila melanogaster, by exploiting the optomotor response, a robust reflex in which an animal steers so as to minimize the magnitude of rotatory optic flow it perceives. Whereas the behavioral and algorithmic structure of the optomotor response has been studied in great detail, its neural implementation is not well-understood. In this paper, we present findings implicating a group of nearly homomorphic descending neurons, the DNg02s, as a core component for the optomotor response in flying Drosophila. Prior work on these cells suggested that they regulate the mechanical power to the flight system, presumably via connections to asynchronous flight motor neurons in the ventral nerve cord. When we chronically inactivated these cells, we observed that the magnitude of the optomotor response was diminished in proportion to the number of cells silenced, suggesting that the cells also regulate bilaterally asymmetric steering responses via population coding. During an optomotor response, flies coordinate changes in wing motion with movements of their head, abdomen, and hind legs, which are also diminished when the DNg02 cells are silenced. Using two-photon functional imaging, we show that the DNg02 cells respond most strongly to patterns of horizontal motion and that neuronal activity is closely correlated to motor output. However, unilateral optogenetic activation of DNg02 neurons does not elicit the asymmetric changes in wing motion characteristic of the optomotor response to a visual stimulus, but rather generates bilaterally symmetric increases in wingbeat amplitude. We interpret our experiments to suggest that flight maneuvers in flies require a more nuanced coordination of power muscles and steering muscles than previously appreciated, and that the physical flight apparatus of a fly might permit mechanical power to be distributed differentially between the two wings. Thus, whereas our experiments identify the DNg02 cells as a critical component of the optomotor reflex, our results suggest that other classes of descending cells targeting the steering muscle motor neurons are also required for the behavior.

Flapping, gliding, running, crawling, and swimming in animals have all been studied extensively in the past and have served as sources of inspiration for engineering designs. In this paper, we describe the aeromechanics of a mode of locomotion that straddles ground and air: jumping. The subject of our study is the spider cricket of the family Rhaphidophoridae, an animal that is among the most proficient of long-jumpers in nature. The focus of the study is to understand the aeromechanics of the aerial portion of the jump of this animal. The research employs high-speed videogrammetry to track the crickets’ posture and appendage orientation throughout their jumps. Experiments demonstrate that these insects employ carefully controlled and coordinated positioning of their limbs during their jumps so as to increase jump distance and stabilize body posture. Simple phenomenological models based on drag laws indicate that the conformation of the limbs during the latter portion of the jump is stable to pitch and enables these animals to land in a controllable manner. Insights from this study could be useful in the design of micro-robots that exploit jumping as a means of locomotion.

SUMMARYThe ability to keep track of one’s location in space is a critical behavior for animals navigating to and from a salient location, but its computational basis remains unknown. Here, we tracked flies in a ring-shaped channel as they executed bouts of search, triggered by optogenetic activation of sugar receptors. Flies centered their back-and-forth local search excursions near fictive food locations by closely matching the length of consecutive runs. We tested a set of agent-based models that incorporate iterative odometry to store and retrieve the distance walked between consecutive events, such as reversals in walking direction. In contrast to memoryless models such as Lévy flight, simulations employing reversal-to-reversal integration recapitulated flies’ centered search behavior, even during epochs when the food stimulus was withheld or in experiments with multiple food sites. However, experiments in which flies reinitiated local search after circumnavigating the arena suggest that flies can also integrate azimuthal heading to perform path integration. Together, this work provides a concrete theoretical framework and experimental system to advance investigations of the neural basis of path integration.

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