A comparison of visual and haltere-mediated equilibrium reflexes in the fruit fly Drosophila melanogaster

SUMMARY Flies exhibit extraordinary maneuverability, relying on feedback from multiple sensory organs to control flight. Both the compound eyes and the mechanosensory halteres encode angular motion as the fly rotates about the three body axes during flight. Since these two sensory modalities differ in their mechanisms of transduction, they are likely to differ in their temporal responses. We recorded changes in stroke kinematics in response to mechanical and visual rotations delivered within a flight simulator. Our results show that the visual system is tuned to relatively slow rotation whereas the haltere-mediated response to mechanical rotation increases with rising angular velocity. The integration of feedback from these two modalities may enhance aerodynamic performance by enabling the fly to sense a wide range of angular velocities during flight.

[1]  A. G. Greenhill Kinematics and Dynamics , 1888, Nature.

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

[3]  S. Bäckström,et al.  The inhibitory effect of glutathione on some processes of animalization. , 1958 .

[4]  H. Autrum,et al.  Electrophysiological analysis of the visual systems in insects. , 1958, Experimental cell research.

[5]  W. Nachtigall,et al.  Neuro-muscular control of dipteran flight. , 1967, The Journal of experimental biology.

[6]  K G Götz,et al.  Principles of optomotor reactions in insects. , 1972, Bibliotheca ophthalmologica : supplementa ad ophthalmologica.

[7]  W Reichardt,et al.  Visual control of orientation behaviour in the fly: Part I. A quantitative analysis , 1976, Quarterly Reviews of Biophysics.

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

[9]  C. Taylor Contribution of Compound Eyes and Ocelli to Steering Of Locusts in Flight: I. Behavioural Analysis , 1981 .

[10]  W. Kutsch,et al.  Dipteran flight motor pattern: invariabilities and changes during postlarval development. , 1981, Journal of neurobiology.

[11]  C. Taylor Contribution of Compound Eyes and Ocelli to Steering of Locusts in Flight: II. Timing Changes in Flight Motor Units , 1981 .

[12]  K. Götz Course-control, metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster , 1987 .

[13]  Alexander Borst,et al.  Principles of visual motion detection , 1989, Trends in Neurosciences.

[14]  Roland Hengstenberg,et al.  Gaze control in the blowfly Calliphora: a multisensory, two-stage integration process , 1991 .

[15]  F. A. Miles,et al.  Visual Motion and Its Role in the Stabilization of Gaze , 1992 .

[16]  A. Borst,et al.  A look into the cockpit of the fly: visual orientation, algorithms, and identified neurons , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  G. Nalbach,et al.  Extremely non-orthogonal axes in a sense organ for rotation: Behavioural analysis of the dipteran haltere system , 1994, Neuroscience.

[18]  Neta Sokolovsky Motion Detection , 1994 .

[19]  M. Dickinson,et al.  Haltere Afferents Provide Direct, Electrotonic Input to a Steering Motor Neuron in the Blowfly, Calliphora , 1996, The Journal of Neuroscience.

[20]  R. Hengstenberg,et al.  Estimation of self-motion by optic flow processing in single visual interneurons , 1996, Nature.

[21]  K. Götz,et al.  Optomotor control of course and altitude in Drosophila melanogaster is correlated with distinct activities of at least three pairs of flight steering muscles. , 1996, The Journal of experimental biology.

[22]  M. Dickinson,et al.  The changes in power requirements and muscle efficiency during elevated force production in the fruit fly Drosophila melanogaster. , 1997, The Journal of experimental biology.

[23]  R. Murphey,et al.  The shaking-B2 Mutation Disrupts Electrical Synapses in a Flight Circuit in AdultDrosophila , 1997, The Journal of Neuroscience.

[24]  W P Chan,et al.  Visual input to the efferent control system of a fly's "gyroscope". , 1998, Science.

[25]  R Hengstenberg,et al.  Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly. , 1998, Journal of neurophysiology.

[26]  E. Eguchi,et al.  Atlas of arthropod sensory receptors : dynamic morphology in relation to function , 1999 .

[27]  Mandyam V. Srinivasan,et al.  Motion detection in insect orientation and navigation , 1999, Vision Research.

[28]  M. Dickinson,et al.  Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  Michael H Dickinson,et al.  The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster. , 2002, The Journal of experimental biology.

[30]  F. A. Miles Multisensory control in insect oculomotor systems , 2003 .

[31]  E. Buchner Elementary movement detectors in an insect visual system , 1976, Biological Cybernetics.

[32]  S. B. Laughlin,et al.  Fast and slow photoreceptors — a comparative study of the functional diversity of coding and conductances in the Diptera , 1993, Journal of Comparative Physiology A.

[33]  M. Heisenberg,et al.  Flight control during ‘free yaw turns’ inDrosophila melanogaster , 1988, Journal of Comparative Physiology A.

[34]  Nicholas J. Strausfeld,et al.  Descending pathways connecting the male-specific visual system of flies to the neck and flight motor , 1991, Journal of Comparative Physiology A.

[35]  M. S. Tu,et al.  The control of wing kinematics by two steering muscles of the blowfly (Calliphora vicina) , 1996, Journal of Comparative Physiology A.

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

[37]  D. Sandeman,et al.  Angular acceleration, compensatory head movements and the halteres of flies (Lucilia serricata) , 1980, Journal of comparative physiology.

[38]  Gert Stange,et al.  The ocellar component of flight equilibrium control in dragonflies , 1981, Journal of comparative physiology.

[39]  Jochen Zeil,et al.  The territorial flight of male houseflies (Fannia canicularis L.) , 1986, Behavioral Ecology and Sociobiology.

[40]  Martin Heisenberg,et al.  The three-dimensional optomotor torque system ofDrosophila melanogaster , 1982, Journal of comparative physiology.

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

[42]  Peter Diehl,et al.  Radiotelemetric monitoring of heart-rate responses to song playback in blackbirds (Turdus merula) , 2004, Behavioral Ecology and Sociobiology.

[43]  G. Nalbach The halteres of the blowfly Calliphora , 1993, Journal of Comparative Physiology A.

[44]  N. J. Strausfeld,et al.  Convergence of visual, haltere, and prosternai inputs at neck motor neurons of Calliphora erythrocephala , 1985, Cell and Tissue Research.

[45]  T. Collett,et al.  Visual control of flight behaviour in the hoverflySyritta pipiens L. , 1975, Journal of comparative physiology.