Comparison of Visually Guided Flight in Insects and Birds

Over the last half century, work with flies, bees, and moths have revealed a number of visual guidance strategies for controlling different aspects of flight. Some algorithms, such as the use of pattern velocity in forward flight, are employed by all insects studied so far, and are used to control multiple flight tasks such as regulation of speed, measurement of distance, and positioning through narrow passages. Although much attention has been devoted to long-range navigation and homing in birds, until recently, very little was known about how birds control flight in a moment-to-moment fashion. A bird that flies rapidly through dense foliage to land on a branch—as birds often do—engages in a veritable three-dimensional slalom, in which it has to continually dodge branches and leaves, and find, and possibly even plan a collision-free path to the goal in real time. Each mode of flight from take-off to goal could potentially involve a different visual guidance algorithm. Here, we briefly review strategies for visual guidance of flight in insects, synthesize recent work from short-range visual guidance in birds, and offer a general comparison between the two groups of organisms.

[1]  Douglas R. Wylie,et al.  Processing of visual signals related to self-motion in the cerebellum of pigeons , 2013, Front. Behav. Neurosci..

[2]  Barrie J Frost,et al.  A Taxonomy of Different Forms of Visual Motion Detection and Their Underlying Neural Mechanisms , 2010, Brain, Behavior and Evolution.

[3]  K. Zimmer,et al.  Der Schwirrflug des Kolibri im Zeitlupenfilm , 2005, Journal für Ornithologie.

[4]  Alexander Borst,et al.  ON and OFF pathways in Drosophila motion vision , 2010, Nature.

[5]  Michael H. Dickinson,et al.  Flies Evade Looming Targets by Executing Rapid Visually Directed Banked Turns , 2014, Science.

[6]  Douglas L. Altshuler,et al.  Neurons Responsive to Global Visual Motion Have Unique Tuning Properties in Hummingbirds , 2017, Current Biology.

[7]  Hendrik Eckert On the landing response of the blowfly, Calliphora erythrocephala , 2004, Biological Cybernetics.

[8]  M. Srinivasan,et al.  Strategies for Pre-Emptive Mid-Air Collision Avoidance in Budgerigars , 2016, PloS one.

[9]  K. Hoffmann,et al.  A quantitative analysis of the direction-specific response of neurons in the cat's nucleus of the optic tract , 2004, Experimental Brain Research.

[10]  A. Fuchs,et al.  Discharge patterns of neurons in the pretectal nucleus of the optic tract (NOT) in the behaving primate. , 1990, Journal of neurophysiology.

[11]  V. Tucker Respiratory Exchange and Evaporative Water Loss in the Flying Budgerigar , 1968 .

[12]  Svetha Venkatesh,et al.  How honeybees make grazing landings on flat surfaces , 2000, Biological Cybernetics.

[13]  B. Hassenstein,et al.  Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus , 1956 .

[14]  Josh Wallman,et al.  Identification of avian brain regions responsive to retinal slip using 2-deoxyglucose , 1981, Brain Research.

[15]  N. H. Barmack,et al.  A comparison of the horizontal and vertical optokinetic reflexes of the rabbit , 1980, Experimental Brain Research.

[16]  Martin Egelhaaf,et al.  Gaze Strategy in the Free Flying Zebra Finch (Taeniopygia guttata) , 2008, PloS one.

[17]  Mandyam V. Srinivasan,et al.  Optic Flow Cues Guide Flight in Birds , 2011, Current Biology.

[18]  D. J. Wells MUSCLE PERFORMANCE IN HOVERING HUMMINGBIRDS , 1993 .

[19]  K. Hoffmann,et al.  Variability in the effects of monocular deprivation on the optokinetic reflex of the non-deprived eye in the cat , 2004, Experimental Brain Research.

[20]  Michael H. Dickinson,et al.  Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds , 2017, Front. Neurosci..

[21]  David N. Lee General Tau Theory: evolution to date. , 2009, Perception.

[22]  Andrew A Biewener,et al.  Through the eyes of a bird: modelling visually guided obstacle flight , 2014, Journal of The Royal Society Interface.

[23]  H. Tiebout,et al.  Daytime Energy Management by Tropical Hummingbirds: Responses to Foraging Constraint , 1991 .

[24]  Bence P. Ölveczky,et al.  Motor circuits are required to encode a sensory model for imitative learning , 2012, Nature Neuroscience.

[25]  J. Wallman,et al.  Directional asymmetries of optokinetic nystagmus: developmental changes and relation to the accessory optic system and to the vestibular system , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  Mandyam V Srinivasan,et al.  Budgerigar flight in a varying environment: flight at distinct speeds? , 2016, Biology Letters.

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

[28]  Partha S. Bhagavatula,et al.  Edge Detection in Landing Budgerigars (Melopsittacus undulatus) , 2009, PloS one.

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

[30]  Benjamin Goller,et al.  Hummingbirds control hovering flight by stabilizing visual motion , 2014, Proceedings of the National Academy of Sciences.

[31]  Mandyam V Srinivasan,et al.  Visual control of navigation in insects and its relevance for robotics , 2011, Current Opinion in Neurobiology.

[32]  K. Fite,et al.  Single-unit responses to whole-field visual stimulation in the pretectum of Rana pipiens , 1996, Neuroscience Letters.

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

[34]  D. R. Wylie,et al.  Spatiotemporal properties of fast and slow neurons in the pretectal nucleus lentiformis mesencephali in pigeons. , 2000, Journal of neurophysiology.

[35]  Mandyam V. Srinivasan,et al.  Visual edge detection in the honeybee and its chromatic properties , 1990, Proceedings of the Royal Society of London. B. Biological Sciences.

[36]  Andrew A Biewener,et al.  Rules to fly by: pigeons navigating horizontal obstacles limit steering by selecting gaps most aligned to their flight direction , 2017, Interface Focus.

[37]  E. Marg A VISION OF THE BRAIN , 1994 .

[38]  Michael H Dickinson,et al.  The visual control of landing and obstacle avoidance in the fruit fly Drosophila melanogaster , 2012, Journal of Experimental Biology.

[39]  Mandyam V. Srinivasan,et al.  Anticipatory Manoeuvres in Bird Flight , 2016, Scientific reports.

[40]  M V Srinivasan,et al.  Visual control of honeybee flight. , 1997, EXS.

[41]  W. Reichardt Movement perception in insects , 1969 .

[42]  David N. Lee,et al.  Plummeting gannets: a paradigm of ecological optics , 1981, Nature.

[43]  H. Collewijn Direction-selective units in the rabbit's nucleus of the optic tract , 1975, Brain Research.

[44]  Damon A. Clark,et al.  Processing properties of ON and OFF pathways for Drosophila motion detection , 2014, Nature.

[45]  Mandyam V Srinivasan,et al.  Honeybees as a model for the study of visually guided flight, navigation, and biologically inspired robotics. , 2011, Physiological reviews.

[46]  M. V. Srinivasan,et al.  Freely flying honeybees use image motion to estimate object distance , 1989, Naturwissenschaften.

[47]  T. K. Fellows,et al.  Visual resolution of Anna's hummingbirds (Calypte anna) in space and time , 2015 .

[48]  Andrew A Biewener,et al.  Optic flow stabilizes flight in ruby-throated hummingbirds , 2016, Journal of Experimental Biology.

[49]  A. Duchon,et al.  A Visual Equalization Strategy for Locomotor Control: Of Honeybees, Robots, and Humans , 2002, Psychological science.

[50]  T X Fan,et al.  Visual responses and connectivity in the turtle pretectum. , 1995, Journal of neurophysiology.

[51]  D. R. Wylie,et al.  Neural specialization for hovering in hummingbirds: Hypertrophy of the pretectal nucleus lentiformis mesencephali , 2007, The Journal of comparative neurology.

[52]  G. Manteuffel,et al.  Electrophysiology and anatomy of direction-specific pretectal units in Salamandra salamandra , 2004, Experimental Brain Research.

[53]  Han Collewijn,et al.  Directional asymmetries of human optokinetic nystagmus , 2004, Experimental Brain Research.

[54]  W. N. Hayes,et al.  Effects of monocular vision and midbrain transection on movement detection in the turtle. , 1969, Journal of comparative and physiological psychology.

[55]  M. Ibbotson,et al.  Spatiotemporal response properties of direction-selective neurons in the nucleus of the optic tract and dorsal terminal nucleus of the wallaby, Macropus eugenii. , 1994, Journal of neurophysiology.

[56]  R. Dudley,et al.  Limits to vertebrate locomotor energetics suggested by hummingbirds hovering in heliox , 1995, Nature.

[57]  Charles M Higgins,et al.  The spatial frequency tuning of optic-flow-dependent behaviors in the bumblebee Bombus impatiens , 2010, Journal of Experimental Biology.

[58]  Roslyn Dakin,et al.  Visual guidance of forward flight in hummingbirds reveals control based on image features instead of pattern velocity , 2016, Proceedings of the National Academy of Sciences.

[59]  Mandyam V Srinivasan,et al.  Minding the gap: in-flight body awareness in birds , 2014, Frontiers in Zoology.

[60]  B. Frost,et al.  Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons , 1998, Nature Neuroscience.

[61]  Michael H Dickinson,et al.  Collision-avoidance and landing responses are mediated by separate pathways in the fruit fly, Drosophila melanogaster. , 2002, The Journal of experimental biology.

[62]  David N. Lee,et al.  VISUAL CONTROL OF VELOCITY OF APPROACH BY PIGEONS WHEN LANDING , 1993 .

[63]  G. Rubin,et al.  A directional tuning map of Drosophila elementary motion detectors , 2013, Nature.

[64]  R. Mooney,et al.  Identification of a motor to auditory pathway important for vocal learning , 2017, Nature Neuroscience.

[65]  B. J. M. Hess,et al.  Horizontal optokinetic ocular nystagmus in the pigmented rat , 1985, Neuroscience.

[66]  David N. Lee,et al.  A Theory of Visual Control of Braking Based on Information about Time-to-Collision , 1976, Perception.

[67]  J. Wallman,et al.  Accessory optic system and pretectum of birds: comparisons with those of other vertebrates. , 1985, Brain, behavior and evolution.

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

[69]  R. C. Lasiewski Oxygen Consumption of Torpid, Resting, Active, and Flying Hummingbirds , 1963, Physiological Zoology.

[70]  A. Borst Drosophila's View on Insect Vision , 2009, Current Biology.

[71]  Mandyam V. Srinivasan,et al.  Direct Evidence for Vision-based Control of Flight Speed in Budgerigars , 2015, Scientific Reports.

[72]  Andrew A Biewener,et al.  Pigeons trade efficiency for stability in response to level of challenge during confined flight , 2015, Proceedings of the National Academy of Sciences.

[73]  Norbert Boeddeker,et al.  A universal strategy for visually guided landing , 2013, Proceedings of the National Academy of Sciences.

[74]  K. Hoffmann,et al.  Direction specific neurons in the pretectum of the frog (Rana esculenta) , 1980, Journal of comparative physiology.

[75]  S. E. Brauth,et al.  Direction-selective single units in the nucleus lentiformis mesencephali of the pigeon (Columba livia) , 2004, Experimental Brain Research.

[76]  N. Strausfeld,et al.  Dissection of the Peripheral Motion Channel in the Visual System of Drosophila melanogaster , 2007, Neuron.

[77]  H. Wagner Flow-field variables trigger landing in flies , 1982, Nature.

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

[79]  A. Borst,et al.  What kind of movement detector is triggering the landing response of the housefly? , 1986, Biological Cybernetics.

[80]  D. Saucier,et al.  Enriched childhood experiences moderate age-related motor and cognitive decline , 2012, Front. Behav. Neurosci..

[81]  D. N. Lee,et al.  Aerial docking by hummingbirds , 1991, Naturwissenschaften.