Flies compensate for unilateral wing damage through modular adjustments of wing and body kinematics.

Using high-speed videography, we investigated how fruit flies compensate for unilateral wing damage, in which loss of area on one wing compromises both weight support and roll torque equilibrium. Our results show that flies control for unilateral damage by rolling their body towards the damaged wing and by adjusting the kinematics of both the intact and damaged wings. To compensate for the reduction in vertical lift force due to damage, flies elevate wingbeat frequency. Because this rise in frequency increases the flapping velocity of both wings, it has the undesired consequence of further increasing roll torque. To compensate for this effect, flies increase the stroke amplitude and advance the timing of pronation and supination of the damaged wing, while making the opposite adjustments on the intact wing. The resulting increase in force on the damaged wing and decrease in force on the intact wing function to maintain zero net roll torque. However, the bilaterally asymmetrical pattern of wing motion generates a finite lateral force, which flies balance by maintaining a constant body roll angle. Based on these results and additional experiments using a dynamically scaled robotic fly, we propose a simple bioinspired control algorithm for asymmetric wing damage.

An Array of Descending Visual Interneurons Encoding Self-Motion in Drosophila.

The means by which brains transform sensory information into coherent motor actions is poorly understood. In flies, a relatively small set of descending interneurons are responsible for conveying sensory information and higher-order commands from the brain to motor circuits in the ventral nerve cord. Here, we describe three pairs of genetically identified descending interneurons that integrate information from wide-field visual interneurons and project directly to motor centers controlling flight behavior. We measured the physiological responses of these three cells during flight and found that they respond maximally to visual movement corresponding to rotation around three distinct body axes. After characterizing the tuning properties of an array of nine putative upstream visual interneurons, we show that simple linear combinations of their outputs can predict the responses of the three descending cells. Last, we developed a machine vision-tracking system that allows us to monitor multiple motor systems simultaneously and found that each visual descending interneuron class is correlated with a discrete set of motor programs. SIGNIFICANCE STATEMENT: Most animals possess specialized sensory systems for encoding body rotation, which they use for stabilizing posture and regulating motor actions. In flies and other insects, the visual system contains an array of specialized neurons that integrate local optic flow to estimate body rotation during locomotion. However, the manner in which the output of these cells is transformed by the downstream neurons that innervate motor centers is poorly understood. We have identified a set of three visual descending neurons that integrate the output of nine large-field visual interneurons and project directly to flight motor centers. Our results provide new insight into how the sensory information that encodes body motion is transformed into a code that is appropriate for motor actions.

Body saccades of Drosophila consist of stereotyped banked turns.

The flight pattern of many fly species consists of straight flight segments interspersed with rapid turns called body saccades, a strategy that is thought to minimize motion blur. We analyzed the body saccades of fruit flies (Drosophila hydei), using high-speed 3D videography to track body and wing kinematics and a dynamically scaled robot to study the production of aerodynamic forces and moments. Although the size, degree and speed of the saccades vary, the dynamics of the maneuver are remarkably stereotypic. In executing a body saccade, flies perform a quick roll and counter-roll, combined with a slower unidirectional rotation around their yaw axis. Flies regulate the size of the turn by adjusting the magnitude of torque that they produce about these control axes, while maintaining the orientation of the rotational axes in the body frame constant. In this way, body saccades are different from escape responses in the same species, in which the roll and pitch component of banking is varied to adjust turn angle. Our analysis of the wing kinematics and aerodynamics showed that flies control aerodynamic torques during the saccade primarily by adjusting the timing and amount of span-wise wing rotation.