Animals must operate under an enormous range of light intensities. Nocturnal and twilight flying insects are hypothesized to compensate for dim conditions by integrating light over longer times. This slowing of visual processing would increase light sensitivity but should also reduce movement response times. Using freely hovering moths tracking robotic moving flowers, we showed that the moth's visual processing does slow in dim light. These longer response times are consistent with models of how visual neurons enhance sensitivity at low light intensities, but they could pose a challenge for moths feeding from swaying flowers. Dusk-foraging moths avoid this sensorimotor tradeoff; their nervous systems slow down but not so much as to interfere with their ability to track the movements of real wind-blown flowers.

SUMMARYMoving animals orchestrate myriad motor systems in response to multimodal sensory inputs. Coordinating movement is particularly challenging in flight control, where animals deal with potential instability and multiple degrees of freedom of movement. Prior studies have focused on wings as the primary flight control structures, for which changes in angle of attack or shape are used to modulate lift and drag forces. However, other actuators that may impact flight performance are reflexively activated during flight. We investigated the visual-abdominal reflex displayed by the hawkmoth Manduca sexta to determine its role in flight control. We measured the open-loop stimulus-response characteristics (measured as a transfer function) between the visual stimulus and abdominal response in tethered moths. The transfer function reveals a 41ms delay and a high-pass filter behavior with a pass band starting at ~0.5Hz. We also developed a simplified mathematical model of hovering flight wherein articulation of the thoracic-abdominal joint redirects an average lift force provided by the wings. We show that control of the joint, subject to a high-pass filter, is sufficient to maintain stable hovering, but with a slim stability margin. Our experiments and models suggest a novel mechanism by which articulation of the body or ʻairframeʼ of an animal can be used to redirect lift forces for effective flight control. Furthermore, the small stability margin may increase flight agility by easing the transition from stable flight to a more maneuverable, unstable regime. Supplementary material available online at

Control theory arose from a need to control synthetic systems. From regulating steam engines to tuning radios to devices capable of autonomous movement, it provided a formal mathematical basis for understanding the role of feedback in the stability (or change) of dynamical systems. It provides a framework for understanding any system with regulation via feedback, including biological ones such as regulatory gene networks, cellular metabolic systems, sensorimotor dynamics of moving animals, and even ecological or evolutionary dynamics of organisms and populations. Here, we focus on four case studies of the sensorimotor dynamics of animals, each of which involves the application of principles from control theory to probe stability and feedback in an organism's response to perturbations. We use examples from aquatic (two behaviors performed by electric fish), terrestrial (following of walls by cockroaches), and aerial environments (flight control by moths) to highlight how one can use control theory to understand the way feedback mechanisms interact with the physical dynamics of animals to determine their stability and response to sensory inputs and perturbations. Each case study is cast as a control problem with sensory input, neural processing, and motor dynamics, the output of which feeds back to the sensory inputs. Collectively, the interaction of these systems in a closed loop determines the behavior of the entire system.

SUMMARYInsects use visual estimates of flight speed for a variety of behaviors, including visual navigation, odometry, grazing landings and flight speed control, but the neuronal mechanisms underlying speed detection remain unknown. Although many models and theories have been proposed for how the brain extracts the angular speed of the retinal image, termed optic flow, we lack the detailed electrophysiological and behavioral data necessary to conclusively support any one model. One key property by which different models of motion detection can be differentiated is their spatiotemporal frequency tuning. Numerous studies have suggested that optic-flow-dependent behaviors are largely insensitive to the spatial frequency of a visual stimulus, but they have sampled only a narrow range of spatial frequencies, have not always used narrowband stimuli, and have yielded slightly different results between studies based on the behaviors being investigated. In this study, we present a detailed analysis of the spatial frequency dependence of the centering response in the bumblebee Bombus impatiens using sinusoidal and square wave patterns.

Abstract-The sparse sensing and limited articulation that are characteristic of human-engineered robotic systems contrast dramatically with sensorimotor systems observed in nature. Animals are richly imbued with sensors, have many points of articulation and are heavily over-actuated. In fact, the compliant nature of the body (or Plant) of most animals requires constant control input to the muscles for postural maintenance. In this study, we show how flying insects use a compliant airframe to maintain flight stability via active articulation of the frame. We first derive the equations of motion for a model flying insect, inspired by the hawkmoth, a large fast flying and agile insect. By linearizing the equations of motion about a hovering equilibrium, we demonstrate that abdominal motions are sufficient to stabilize flight on a scale of 50ms. We then tested whether these insects use the abdomen for flight control by first measuring the open-loop transfer function between visual pitch rotations and abdominal movement in a tethered moth preparation. The measured transfer function was consistent with an abdominal control strategy. We then closed the loop and found that moths actively stabilize visual pitch rotations using abdominal motion as the only control input. The behavior was robust to variations in gain and to a variety of visual stimuli. These experiments establish airframe articulation as a plausible control mechanism for active flight.

Insect navigational behaviors including obstacle avoidance, grazing landings, and visual odometry are dependent on the ability to estimate flight speed based only on visual cues. In honeybees, this visual estimate of speed is largely independent of both the direction of motion and the spatial frequency content of the image. Electrophysiological recordings from the motion-sensitive cells believed to underlie these behaviors have long supported spatio-temporally tuned correlation-type models of visual motion detection whose speed tuning changes as the spatial frequency of a stimulus is varied. The result is an apparent conflict between behavioral experiments and the electrophysiological and modeling data. In this article, we demonstrate that conventional correlation-type models are sufficient to reproduce some of the speed-dependent behaviors observed in honeybees when square wave gratings are used, contrary to the theoretical predictions. However, these models fail to match the behavioral observations for sinusoidal stimuli. Instead, we show that non-directional motion detectors, which underlie the correlation-based computation of directional motion, can be used to mimic these same behaviors even when narrowband gratings are used. The existence of such non-directional motion detectors is supported both anatomically and electrophysiologically, and they have been hypothesized to be critical in the Dipteran elementary motion detector (EMD) circuit.

Insects are highly maneuverable fliers. Naturally, engineers have focused much of their efforts on understanding the role of insect wing design and actuation for maneuvering and control of bio-inspired micro air vehicles. However, many insects exhibit strong visually mediated abdominal reflexes. The hawkmoth, Manduca sexta, has a particularly large abdomen, and recent evidence suggests that these visuo-abdominal reflexes are used to inertially redirect thrust forces for control. In a biologically inspired control framework, we show that the stability of a quadrotor can be categorically improved by redirecting aerodynamic forces using appendage inertia.

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