The spatial frequency tuning of optic-flow-dependent behaviors in the bumblebee Bombus impatiens

SUMMARY Insects 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.

[1]  Erich Buchner,et al.  Behavioural Analysis of Spatial Vision in Insects , 1984 .

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

[3]  A. S. Edwards,et al.  Ontogeny of orientation flight in the honeybee revealed by harmonic radar , 2000, Nature.

[4]  Charles M. Higgins Nondirectional motion may underlie insect behavioral dependence on image speed , 2004, Biological Cybernetics.

[5]  S. W. Zhang,et al.  How honeybees measure their distance from objects of unknown size , 2004, Journal of Comparative Physiology A.

[6]  Zhang,et al.  Visually mediated odometry in honeybees , 1997, The Journal of experimental biology.

[7]  F. G. Barth,et al.  A stingless bee (Melipona seminigra) uses optic flow to estimate flight distances , 2003, Journal of Comparative Physiology A.

[8]  Mandyam V. Srinivasan,et al.  Honeybee navigation: properties of the visually driven `odometer' , 2003, Journal of Experimental Biology.

[9]  K. Hausen Motion sensitive interneurons in the optomotor system of the fly , 1982, Biological Cybernetics.

[10]  R. Menzel,et al.  Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts , 1996, Journal of Comparative Physiology A.

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

[12]  J. Fellous,et al.  The Processing of Color, Motion, and Stimulus Timing Are Anatomically Segregated in the Bumblebee Brain , 2008, The Journal of Neuroscience.

[13]  Andre J Riveros,et al.  Learning from learning and memory in bumblebees , 2009, Communicative & integrative biology.

[14]  Nicolas H. Franceschini,et al.  Bio-inspired optic flow sensors based on FPGA: Application to Micro-Air-Vehicles , 2007, Microprocess. Microsystems.

[15]  S. Laughlin,et al.  Insect motion detectors matched to visual ecology , 1996, Nature.

[16]  G. D. Mccann,et al.  Optomotor response studies of insect vision , 1965, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[17]  N. Strausfeld,et al.  Computational Modeling of Neurons Involved in Fly Motion Detection , 2005 .

[18]  H. A. McCartney,et al.  Compensation for wind drift by bumble-bees , 1999, Nature.

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

[20]  A. Borst,et al.  Comparison between the movement detection systems underlying the optomotor and the landing response in the housefly , 1987, Biological Cybernetics.

[21]  S. Hecht,et al.  THE VISUAL ACUITY OF THE HONEY BEE , 1929, The Journal of general physiology.

[22]  Alexander Borst,et al.  Correlation versus gradient type motion detectors: the pros and cons , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[23]  Mandyam V. Srinivasan,et al.  Visual Control of Flight Speed and Height in the Honeybee , 2006, SAB.

[24]  Charles M. Higgins,et al.  Biomimetic visual navigation architectures for autonomous intelligent systems , 2007 .

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

[26]  R O Dror,et al.  Accuracy of velocity estimation by Reichardt correlators. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[27]  Don R. Reynolds,et al.  A landscape‐scale study of bumble bee foraging range and constancy, using harmonic radar , 1999 .

[28]  Alberto Ugolini Visual information acquired during displacement and initial orientation in Polistes gallicus (L.) (Hymenoptera, Vespidae) , 1987, Animal Behaviour.

[29]  M. Wiener,et al.  Animal eyes. , 1957, The American orthoptic journal.

[30]  D. Grier,et al.  Methods of Digital Video Microscopy for Colloidal Studies , 1996 .

[31]  S. Zhang,et al.  Evidence for two distinct movement-detecting mechanisms in insect vision , 2005, Naturwissenschaften.

[32]  Clyde Young Kramer,et al.  Extension of multiple range tests to group means with unequal numbers of replications , 1956 .

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

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

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

[36]  H. Esch,et al.  Honeybees use optic flow to measure the distance of a food source , 2005, Naturwissenschaften.

[37]  A. Philippides,et al.  A model of visual detection of angular speed for bees. , 2009, Journal of theoretical biology.

[38]  Johannes M. Zanker,et al.  Speed tuning in elementary motion detectors of the correlation type , 1999, Biological Cybernetics.

[39]  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.

[40]  M. Srinivasan,et al.  Honeybee navigation: distance estimation in the third dimension , 2007, Journal of Experimental Biology.

[41]  R. Shapley,et al.  Photoreception and Vision in Invertebrates , 1984, NATO ASI Series.

[42]  Angelique C Paulk,et al.  Higher order visual input to the mushroom bodies in the bee, Bombus impatiens. , 2008, Arthropod structure & development.

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

[44]  M. Ibbotson Evidence for velocity–tuned motion-sensitive descending neurons in the honeybee , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.