Embodied linearity of speed control in Drosophila melanogaster

Fruitflies regulate flight speed by adjusting their body angle. To understand how low-level posture control serves an overall linear visual speed control strategy, we visually induced free-flight acceleration responses in a wind tunnel and measured the body kinematics using high-speed videography. Subsequently, we reverse engineered the transfer function mapping body pitch angle onto flight speed. A linear model is able to reproduce the behavioural data with good accuracy. Our results show that linearity in speed control is realized already at the level of body posture-mediated speed control and is therefore embodied at the level of the complex aerodynamic mechanisms of body and wings. Together with previous results, this study reveals the existence of a linear hierarchical control strategy, which can provide relevant control principles for biomimetic implementations, such as autonomous flying micro air vehicles.

[1]  Steven N Fry,et al.  Frequency response of lift control in Drosophila , 2010, Journal of The Royal Society Interface.

[2]  C. David,et al.  The dynamics of height stabilization in Drosophila , 1984 .

[3]  R. Hengstenberg.  Mechanosensory control of compensatory head roll during flight in the blowflyCalliphora erythrocephala Meig. , 1988, Journal of Comparative Physiology A.

[4]  Mandyam V. Srinivasan,et al.  A visually-evoked roll response in the housefly , 2004, Journal of comparative physiology.

[5]  H. Markl,et al.  Head Movements in Flies ( Calliphora ) Produced by Deflexion of the Halteres , 1980 .

[6]  Karl Georg Götz,et al.  Flight control in Drosophila by visual perception of motion , 1968, Kybernetik.

[7]  S. N. Fry,et al.  Context-dependent stimulus presentation to freely moving animals in 3D , 2004, Journal of Neuroscience Methods.

[8]  T. Hedrick,et al.  Wingbeat Time and the Scaling of Passive Rotational Damping in Flapping Flight , 2009, Science.

[9]  S. Vogel.  Flight in Drosophila : I. Flight Performance of Tethered Flies , 1966 .

[10]  Mao Sun,et al.  Dynamic flight stability of hovering insects , 2007 .

[11]  R.M. Murray,et al.  Vision as a compensatory mechanism for disturbance rejection in upwind flight , 2004, Proceedings of the 2004 American Control Conference.

[12]  G K Taylor,et al.  Mechanics and aerodynamics of insect flight control , 2001, Biological reviews of the Cambridge Philosophical Society.

[13]  K E Weber,et al.  Aerial performance of Drosophila melanogaster from populations selected for upwind flight ability. , 1997, The Journal of experimental biology.

[14]  John Guckenheimer,et al.  Discovering the flight autostabilizer of fruit flies by inducing aerial stumbles , 2010, Proceedings of the National Academy of Sciences.

[15]  M. Dickinson,et al.  The effect of advance ratio on the aerodynamics of revolving wings , 2004, Journal of Experimental Biology.

[16]  David C. O'Carroll,et al.  Motion blur applied to eliminate artifacts in apparent motion displays , 2010 .

[17]  John Guckenheimer,et al.  Paddling mode of forward flight in insects. , 2011, Physical review letters.

[18]  C. Ellington.  The Aerodynamics of Hovering Insect Flight. III. Kinematics , 1984 .

[19]  M. Dickinson,et al.  Summation of visual and mechanosensory feedback in Drosophila flight control , 2004, Journal of Experimental Biology.

[20]  Xinyan Deng,et al.  Translational and Rotational Damping of Flapping Flight and Its Dynamics and Stability at Hovering , 2011, IEEE Transactions on Robotics.

[21]  M. Srinivasan,et al.  Visual motor computations in insects. , 2004, Annual review of neuroscience.

[22]  D. Varjú,et al.  The response of the hovering hawk moth Macroglossum stellatarum to translatory pattern motion , 1995, Journal of Comparative Physiology A.

[23]  M. Srinivasan,et al.  Visual control of flight speed in honeybees , 2005, Journal of Experimental Biology.

[24]  S.N. Fry,et al.  A 6000 Hz Computer Vision System for Real-Time Wing Beat Analysis of Drosophila , 2006, The First IEEE/RAS-EMBS International Conference on Biomedical Robotics and Biomechatronics, 2006. BioRob 2006..

[25]  Imraan A. Faruque,et al.  Dipteran insect flight dynamics. Part 1 Longitudinal motion about hover. , 2010, Journal of theoretical biology.

[26]  M. Srinivasan,et al.  Range perception through apparent image speed in freely flying honeybees , 1991, Visual Neuroscience.

[27]  Michael H. Dickinson,et al.  TrackFly: Virtual reality for a behavioral system analysis in free-flying fruit flies , 2008, Journal of Neuroscience Methods.

[28]  Mark A Frye,et al.  Dynamics of optomotor responses in Drosophila to perturbations in optic flow , 2010, Journal of Experimental Biology.

[29]  J. Pringle.  The gyroscopic mechanism of the halteres of Diptera , 1948, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[30]  Michael H. Dickinson,et al.  Integrative Model of Drosophila Flight , 2008 .

[31]  M. Heisenberg,et al.  The sensory-motor link in motion-dependent flight control of flies. , 1993, Reviews of oculomotor research.

[32]  M. Dickinson,et al.  The control of flight force by a flapping wing: lift and drag production. , 2001, The Journal of experimental biology.

[33]  J. Kennedy.  The Visual Responses of Flying Mosquitoes. , 2009 .

[34]  S. N. Fry,et al.  The Aerodynamics of Free-Flight Maneuvers in Drosophila , 2003, Science.

[35]  S. N. Fry,et al.  Aerodynamic damping during rapid flight maneuvers in the fruit fly Drosophila , 2010, Journal of Experimental Biology.

[36]  H. Nalbach,et al.  Visual stabilization in arthropods. , 1993, Reviews of oculomotor research.

[37]  H. Krapp,et al.  Sensory Systems and Flight Stability: What do Insects Measure and Why? , 2007 .

[38]  R. Hengstenberg,et al.  The halteres of the blowfly Calliphora , 1994, Journal of Comparative Physiology A.

[39]  T. Hedrick,et al.  The mechanics and control of pitching manoeuvres in a freely flying hawkmoth (Manduca sexta) , 2011, Journal of Experimental Biology.

[40]  Zhang,et al.  Honeybee navigation en route to the goal: visual flight control and odometry , 1996, The Journal of experimental biology.

[41]  F. Lehmann,et al.  Turning behaviour depends on frictional damping in the fruit fly Drosophila , 2007, Journal of Experimental Biology.

[42]  Nicola Rohrseitz,et al.  Behavioural system identification of visual flight speed control in Drosophila melanogaster , 2011, Journal of The Royal Society Interface.

[43]  K Hausen,et al.  Decoding of retinal image flow in insects. , 1993, Reviews of oculomotor research.

[44]  S. N. Fry,et al.  Visual control of flight speed in Drosophila melanogaster , 2009, Journal of Experimental Biology.

[45]  S. N. Fry,et al.  The aerodynamics of hovering flight in Drosophila , 2005, Journal of Experimental Biology.

[46]  C. David.  The relationship between body angle and flight speed in free‐flying Drosophila , 1978 .

[47]  C. David.  Compensation for height in the control of groundspeed byDrosophila in a new, ‘barber's pole’ wind tunnel , 1982, Journal of comparative physiology.

[48]  Z. Jane Wang,et al.  DISSECTING INSECT FLIGHT , 2005 .

[49]  M. Srinivasan,et al.  Visual regulation of ground speed and headwind compensation in freely flying honey bees (Apis mellifera L.) , 2006, Journal of Experimental Biology.