Flexible strategies for flight control: an active role for the abdomen

Dyhr, Jonathan P.; Morgansen, Kristi A.; Daniel, Thomas L.; Cowan, Noah J.

doi:10.1242/jeb.077644

Cited by 104 publications

(128 citation statements)

References 32 publications

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“…Hawk moths exhibit another possible example of this principle in which fast antennal feedback adds linearly to slower visual feedback to regulate the stabilizing motion of the abdomen during hovering flight (24,51). In the present study, we have shown that flies use this same principle in the context of translational flight control, which involves different constraints.…”

Section: Discussionmentioning

confidence: 50%

Flying Drosophila stabilize their vision-based velocity controller by sensing wind with their antennae

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Proc. Natl. Acad. Sci. U.S.A.

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Flies and other insects use vision to regulate their groundspeed in flight, enabling them to fly in varying wind conditions. Compared with mechanosensory modalities, however, vision requires a long processing delay (~100 ms) that might introduce instability if operated at high gain. Flies also sense air motion with their antennae, but how this is used in flight control is unknown. We manipulated the antennal function of fruit flies by ablating their aristae, forcing them to rely on vision alone to regulate groundspeed. Arista-ablated flies in flight exhibited significantly greater groundspeed variability than intact flies. We then subjected them to a series of controlled impulsive wind gusts delivered by an air piston and experimentally manipulated antennae and visual feedback. The results show that an antenna-mediated response alters wing motion to cause flies to accelerate in the same direction as the gust. This response opposes flying into a headwind, but flies regularly fly upwind. To resolve this discrepancy, we obtained a dynamic model of the fly's velocity regulator by fitting parameters of candidate models to our experimental data. The model suggests that the groundspeed variability of arista-ablated flies is the result of unstable feedback oscillations caused by the delay and high gain of visual feedback. The antenna response drives active damping with a shorter delay (~20 ms) to stabilize this regulator, in exchange for increasing the effect of rapid wind disturbances. This provides insight into flies' multimodal sensory feedback architecture and constitutes a previously unknown role for the antennae.stability | sensory fusion | feedback delay | system identification | turbulence A nimals rely on input from multiple sensory modalities to regulate their motor actions. For example, to quickly grasp an object, a human uses both vision and tactile sensing. The visual system can estimate how close the object is, but only touch can accurately determine when contact is made (1). Similarly, flying insects rely on multiple senses, including vision and mechanosensation to control their flight (2). This multimodal feedback enables them to perform aerial feats, such as chasing conspecifics (3) and rapid self-righting after takeoff (4). Our neurobiological and biomechanical understanding of these behaviors is incomplete, but physiological studies and physics-based models have helped reveal salient features (5-9).The flight paths of flies often are structured into bouts of straight segments of forward motion, punctuated by rapid changes in heading termed body saccades (3,(10)(11)(12). During the straight segments, flies tend to maintain constant groundspeed despite changes in wind speed, suggesting the presence of an active feedback regulator (13,14). Recent results provide some insight into the properties of this vision-based forward velocity controller, such as its dependence on the spatial and temporal frequency of the visual stimulus, and the magnitude of the underlying sensory-motor delay (15,16). Experiments w...

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Section: Discussionmentioning

confidence: 50%

Flying Drosophila stabilize their vision-based velocity controller by sensing wind with their antennae

Fuller

Straw

Peek

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…Nor did that study investigate other possible reasons for the changes in abdomen pitch that many flying insects display. Furthermore, Dyhr et al (2013) proposed and confirmed, for hawkmoths (Manduca sexta), that pitch reorientation rotates the thorax, resulting in redirection of the flight force, and assists in flight stabilisation. Also, by measuring the pitch response to a vertically oscillating visual stimulus under open-loop conditions, they found that the pitch control system can be adequately modelled as a firstorder high-pass filter, with an additional pure time delay of 41 ms. Tanaka and Kawachi (2006) conducted similar tethered flight experiments on bumblebees (Bombus terrestris), where a visual grating (generated by a panoramic matrix of LEDs surrounding the insect) was oscillated vertically in a sinusoidal manner.…”

Section: Introductionmentioning

confidence: 93%

Flight control of fruit flies: dynamic response to optic-flow and headwind

Lawson

Srinivasan

2017

Journal of Experimental Biology

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Insects are magnificent fliers that are capable of performing many complex tasks such as speed regulation, smooth landings and collision avoidance, even though their computational abilities are limited by their small brain. To investigate how flying insects respond to changes in wind speed and surrounding optic flow, the open-loop sensorimotor response of female Queensland fruit flies (Bactrocera tryoni) was examined. A total of 136 flies were exposed to stimuli comprising sinusoidally varying optic flow and air flow (simulating forward movement) under tethered conditions in a virtual reality arena. Two responses were measured: the thrust and the abdomen pitch. The dynamics of the responses to optic flow and air flow were measured at various frequencies, and modelled as a multicompartment linear system, which accurately captured the behavioural responses of the fruit flies. The results indicate that these two behavioural responses are concurrently sensitive to changes of optic flow as well as wind. The abdomen pitch showed a streamlining response, where the abdomen was raised higher as the magnitude of either stimulus was increased. The thrust, in contrast, exhibited a counter-phase response where maximum thrust occurred when the optic flow or wind flow was at a minimum, indicating that the flies were attempting to maintain an ideal flight speed. When the changes in the wind and optic flow were in phase (i.e. did not contradict each other), the net responses (thrust and abdomen pitch) were well approximated by an equally weighted sum of the responses to the individual stimuli. However, when the optic flow and wind stimuli were presented in counterphase, the flies seemed to respond to only one stimulus or the other, demonstrating a form of 'selective attention'.

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“…Such collaborations have, for example, led to the discovery of two independent mechanisms that animals can use to overcome the trade-off between stability and maneuverability in locomotion. Fish use mutually opposing forces (Sefati et al 2013), whereas insects accomplish the same ends using flexible airframes (Dyhr et al 2012(Dyhr et al , 2013. These collaborations also led to advances in engineering.…”

Section: Challenge 1: Understanding Living Organisms As Multiscale Symentioning

confidence: 99%

“…This knowledge stimulated engineers and material scientists to develop novel types of dry adhesives (Ge et al 2007, Lee HS et al 2007, Lee JH et al 2009, Murphy et al 2009, Filippov et al 2011. Such collaborations have also led to new insight regarding the dynamic control of animal locomotion (e.g., Libby et al 2012, Dyhr et al 2013, Mongeau et al 2013, Sefati et al 2013, and new strategies for controlling complex and highly dynamic machines (e.g., Dyhr et al 2012). Combined biology, applied mathematics, and engineering approaches are presently being used to examine the role of feedback in the stability (or change) of dynamical systems, such as regulatory gene networks, cellular metabolic systems, sensorimotor dynamics of moving animals, and even ecological or evolutionary dynamics of organisms and populations (Cowan et al 2014).…”

Section: New Opportunitiesmentioning

confidence: 99%

Addressing Grand Challenges In Organismal Biology: The Need For Synthesis

Padilla¹,

Daniel²,

Dickinson³

et al. 2014

BioScience

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Animals are complex systems operating at multiple spatial and temporal scales, facing the challenge of how to change in appropriate ways, degrees, and times, in response to the diverse internal and external influences to which they are exposed. Discovering the system-level attributes of organisms that make them resilient or robust-or sensitive or fragile-to change presents a grand challenge for biology. Knowledge of these attributes and the underlying mechanisms controlling them is crucially needed to predict how organisms will respond to short-and long-term changes in internal and external environments, including those driven by climate change. Organismal biologists require novel approaches that extend beyond traditional disciplinary boundaries, especially when they partner with mathematicians and engineers. Pursuing this research enterprise will not only give us a deeper understanding of how organisms will face future challenges, but it will also reveal nature-inspired solutions in complex engineered systems, both of which will benefit science and society.Keywords: organismal biology, grand challenges, integrative biology, systems engineering, predictive modeling Animals are inherently complex and are composed of multiple interconnected elements. They and their component elements must have the capacity to maintain stability and to simultaneously change in response to internal and external stimuli. For example, young animals must be able to process neurosensory inputs as they move through the environment while their brains and nervous systems continue to develop. As they grow and develop, structures used for locomotion may simultaneously change in their function and control because of changes in size and morphology (Hale 2014). Those same animals must maintain the internal physiological function of all of their systems throughout ontogeny and as they experience shifting internal 1 Dianna K. Padilla (padilla@stonybrook.edu) is a professor in the Department of Ecology and Evolution at Stony Brook University, in Stony Brook, New York. Thomas L. Daniel is a professor, in the Department of Biology, Billie J. Swalla is the director of and a professor in the the Friday Harbor Laboratories and in the Department of Biology, and Daniel Grünbaum is an associate professor in the School of Oceanography at the University of Washington, in Seattle. Patsy Dickinson is a professor in the Department of Biology and in the Neuroscience Program at Bowdoin College, in Brunswick, Maine. Cheryl Hayashi is a professor in the Department of Biology at the University of California, Riverside. Donal T. Manahan is a professor in the Department of Biological Sciences at the University of Southern California, in Los Angeles. James H. Marden is a professor in the Department of Biology at Pennsylvania State University, in State College. Brian Tsukimura is a professor in the Department of Biology at California State University, Fresno. 2 and external environments. In addition, animals and animal systems exhibit many nonlinear and time-dependent ...

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Flexible strategies for flight control: an active role for the abdomen

Cited by 104 publications

References 32 publications

Flying Drosophila stabilize their vision-based velocity controller by sensing wind with their antennae

Flying Drosophila stabilize their vision-based velocity controller by sensing wind with their antennae

Flight control of fruit flies: dynamic response to optic-flow and headwind

Addressing Grand Challenges In Organismal Biology: The Need For Synthesis

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