Visual motion-sensitive neurons in the bumblebee brain convey information about landmarks during a navigational task

Mertes M, Dittmar L, Egelhaaf M, Boeddeker N (2014)
Frontiers in Behavioral Neuroscience 8: 335.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
OA 3.13 MB
Abstract / Bemerkung
Bees use visual memories to find the spatial location of previously learnt food sites. Characteristic learning flights help acquiring these memories at newly discovered foraging locations where landmarks-salient objects in the vicinity of the goal location-can play an important role in guiding the animal's homing behavior. Although behavioral experiments have shown that bees can use a variety of visual cues to distinguish objects as landmarks, the question of how landmark features are encoded by the visual system is still open. Recently, it could be shown that motion cues are sufficient to allow bees localizing their goal using landmarks that can hardly be discriminated from the background texture. Here, we tested the hypothesis that motion sensitive neurons in the bee's visual pathway provide information about such landmarks during a learning flight and might, thus, play a role for goal localization. We tracked learning flights of free-flying bumblebees (Bombus terrestris) in an arena with distinct visual landmarks, reconstructed the visual input during these flights, and replayed ego-perspective movies to tethered bumblebees while recording the activity of direction-selective wide-field neurons in their optic lobe. By comparing neuronal responses during a typical learning flight and targeted modifications of landmark properties in this movie we demonstrate that these objects are indeed represented in the bee's visual motion pathway. We find that object-induced responses vary little with object texture, which is in agreement with behavioral evidence. These neurons thus convey information about landmark properties that are useful for view-based homing.
Stichworte
electrophysiology; homing; motion sensing; insect; optic-flow
Erscheinungsjahr
2014
Zeitschriftentitel
Frontiers in Behavioral Neuroscience
Band
8
Seite(n)
335
ISSN
1662-5153
eISSN
1662-5153
Page URI
https://pub.uni-bielefeld.de/record/2701723

Zitieren

Mertes M, Dittmar L, Egelhaaf M, Boeddeker N. Visual motion-sensitive neurons in the bumblebee brain convey information about landmarks during a navigational task. Frontiers in Behavioral Neuroscience. 2014;8:335.
Mertes, M., Dittmar, L., Egelhaaf, M., & Boeddeker, N. (2014). Visual motion-sensitive neurons in the bumblebee brain convey information about landmarks during a navigational task. Frontiers in Behavioral Neuroscience, 8, 335. doi:10.3389/fnbeh.2014.00335
Mertes, Marcel, Dittmar, Laura, Egelhaaf, Martin, and Boeddeker, Norbert. 2014. “Visual motion-sensitive neurons in the bumblebee brain convey information about landmarks during a navigational task”. Frontiers in Behavioral Neuroscience 8: 335.
Mertes, M., Dittmar, L., Egelhaaf, M., and Boeddeker, N. (2014). Visual motion-sensitive neurons in the bumblebee brain convey information about landmarks during a navigational task. Frontiers in Behavioral Neuroscience 8, 335.
Mertes, M., et al., 2014. Visual motion-sensitive neurons in the bumblebee brain convey information about landmarks during a navigational task. Frontiers in Behavioral Neuroscience, 8, p 335.
M. Mertes, et al., “Visual motion-sensitive neurons in the bumblebee brain convey information about landmarks during a navigational task”, Frontiers in Behavioral Neuroscience, vol. 8, 2014, pp. 335.
Mertes, M., Dittmar, L., Egelhaaf, M., Boeddeker, N.: Visual motion-sensitive neurons in the bumblebee brain convey information about landmarks during a navigational task. Frontiers in Behavioral Neuroscience. 8, 335 (2014).
Mertes, Marcel, Dittmar, Laura, Egelhaaf, Martin, and Boeddeker, Norbert. “Visual motion-sensitive neurons in the bumblebee brain convey information about landmarks during a navigational task”. Frontiers in Behavioral Neuroscience 8 (2014): 335.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Copyright Statement:
Dieses Objekt ist durch das Urheberrecht und/oder verwandte Schutzrechte geschützt. [...]
Volltext(e)
Access Level
OA Open Access
Zuletzt Hochgeladen
2019-09-06T09:18:27Z
MD5 Prüfsumme
f8cf0aae4a4ffb31c4bd8d5617787a87


4 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

The role of spatial texture in visual control of bumblebee learning flights.
Linander N, Dacke M, Baird E, Hempel de Ibarra N., J Comp Physiol A Neuroethol Sens Neural Behav Physiol 204(8), 2018
PMID: 29980840
Neural mechanisms of insect navigation.
Webb B, Wystrach A., Curr Opin Insect Sci 15(), 2016
PMID: 27436729
Bumblebee Homing: The Fine Structure of Head Turning Movements.
Boeddeker N, Mertes M, Dittmar L, Egelhaaf M., PLoS One 10(9), 2015
PMID: 26352836

79 References

Daten bereitgestellt von Europe PubMed Central.

The fine structure of honeybee head and body yaw movements in a homing task.
Boeddeker N, Dittmar L, Sturzl W, Egelhaaf M., Proc. Biol. Sci. 277(1689), 2010
PMID: 20147329
Visual gaze control during peering flight manoeuvres in honeybees.
Boeddeker N, Hemmi JM., Proc. Biol. Sci. 277(1685), 2009
PMID: 20007175
Responses of blowfly motion-sensitive neurons to reconstructed optic flow along outdoor flight paths.
Boeddeker N, Lindemann JP, Egelhaaf M, Zeil J., J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 191(12), 2005
PMID: 16133502
Identifying prototypical components in behaviour using clustering algorithms.
Braun E, Geurten B, Egelhaaf M., PLoS ONE 5(2), 2010
PMID: 20179763
IVtools
Braun E., Lindemann J.., 2011
Walking modulates speed sensitivity in Drosophila motion vision.
Chiappe ME, Seelig JD, Reiser MB, Jayaraman V., Curr. Biol. 20(16), 2010
PMID: 20655222
Memory use in insect visual navigation.
Collett TS, Collett M., Nat. Rev. Neurosci. 3(7), 2002
PMID: 12094210
Navigational memories in ants and bees: memory retrieval when selecting and following routes.
Collett TS, Graham P, Harris RA, Hempel-De-Ibarra N., Advances in the study of behavior. 36(), 2006
PMID: IND43867117
Coordinating compass-based and nest-based flight directions during bumblebee learning and return flights.
Collett TS, de Ibarra NH, Riabinina O, Philippides A., J. Exp. Biol. 216(Pt 6), 2013
PMID: 23447669
Flights of learning
Collett T., Zeil J.., 1996
Horizontal movement detectors of honeybees: directionally-selective visual neurons in the lobula and brain
DeVoe R., Kaiser W., Ohm J., Stone L.., 1982
The behavioral relevance of landmark texture for honeybee homing.
Dittmar L, Egelhaaf M, Sturzl W, Boeddeker N., Front Behav Neurosci 5(), 2011
PMID: 21541258
Goal seeking in honeybees: matching of optic flow snapshots?
Dittmar L, Sturzl W, Baird E, Boeddeker N, Egelhaaf M., J. Exp. Biol. 213(Pt 17), 2010
PMID: 20709919
The neural computation of visual motion
Egelhaaf M.., 2006
Spatial vision in insects is facilitated by shaping the dynamics of visual input through behavioral action.
Egelhaaf M, Boeddeker N, Kern R, Kurtz R, Lindemann JP., Front Neural Circuits 6(), 2012
PMID: 23269913
A syntax of hoverfly flight prototypes.
Geurten BR, Kern R, Braun E, Egelhaaf M., J. Exp. Biol. 213(Pt 14), 2010
PMID: 20581276
Visual homing in the absence of feature-based landmark information.
Gillner S, Weiss AM, Mallot HA., Cognition 109(1), 2008
PMID: 18804202
Physiological and anatomical properties of optical input-fibres to the mushroom body in the bee brain
Gronenberg W.., 1986
Motion sensitive interneurons in the optomotor system of the fly. I. The horizontal cells: structure and signals
Hausen K.., 1982
Preferred viewing directions of bumblebees (Bombus terrestris L.) when learning and approaching their nest site.
de Ibarra NH, Philippides A, Riabinina O, Collett TS., J. Exp. Biol. 212(Pt 20), 2009
PMID: 19801423
The physiology and morphology of centrally projecting visual interneurones in the honeybee brain
Hertel H., Maronde U.., 1987
The physiology and morphology of visual commissures in the honeybee brain
Hertel H., Schaefer S., Maronde U.., 1987
Visual response properties of neck motor neurons in the honeybee.
Hung YS, van Kleef JP, Ibbotson MR., J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 197(12), 2011
PMID: 21909972
Spectral inputs and ocellar contributions to a pitch-sensitive descending neuron in the honeybee.
Hung YS, van Kleef JP, Stange G, Ibbotson MR., J. Neurophysiol. 109(4), 2012
PMID: 23197452
A motion-sensitive visual descending neurone in Apis mellifera monitoring translatory flow-fields in the horizontal plane
Ibbotson M.., 1991
Wide-field motion-sensitive neurons tuned to horizontal movement in the honeybee, Apis mellifera
Ibbotson M.., 1991
Response characteristics of four wide-field motion-sensitive descending interneurons in Apis mellifera
Ibbotson M., Goodman L.., 1990
Flight activity alters velocity tuning of fly motion-sensitive neurons.
Jung SN, Borst A, Haag J., J. Neurosci. 31(25), 2011
PMID: 21697373
Encoding of naturalistic optic flow by a population of blowfly motion-sensitive neurons.
Karmeier K, van Hateren JH, Kern R, Egelhaaf M., J. Neurophysiol. 96(3), 2006
PMID: 16687623
Blowfly flight characteristics are shaped by environmental features and controlled by optic flow information.
Kern R, Boeddeker N, Dittmar L, Egelhaaf M., J. Exp. Biol. 215(Pt 14), 2012
PMID: 22723490
Function of a fly motion-sensitive neuron matches eye movements during free flight.
Kern R, van Hateren JH, Michaelis C, Lindemann JP, Egelhaaf M., PLoS Biol. 3(6), 2005
PMID: 15884977
Optic flow.
Koenderink JJ., Vision Res. 26(1), 1986
PMID: 3716209
Motion and vision: why animals move their eyes.
Land MF., J. Comp. Physiol. A 185(4), 1999
PMID: 10555268
Why do bees turn back and look?
Lehrer M.., 1993
Generalization of convex shapes by bees: what are shapes made of?
Lehrer M, Campan R., J. Exp. Biol. 208(Pt 17), 2005
PMID: 16109886
Approaching and departing bees learn different cues to the distance of a landmark
Lehrer M., Collett T.., 1994
Image-matching during ant navigation occurs through saccade-like body turns controlled by learned visual features.
Lent DD, Graham P, Collett TS., Proc. Natl. Acad. Sci. U.S.A. 107(37), 2010
PMID: 20805481
FliMax, a novel stimulus device for panoramic and highspeed presentation of behaviourally generated optic flow.
Lindemann JP, Kern R, Michaelis C, Meyer P, van Hateren JH, Egelhaaf M., Vision Res. 43(7), 2003
PMID: 12639604
Active flight increases the gain of visual motion processing in Drosophila.
Maimon G, Straw AD, Dickinson MH., Nat. Neurosci. 13(3), 2010
PMID: 20154683
Variations of box plots
McGill R., Tukey J., Larsen W.., 1978
Learning and memory in honeybees: from behavior to neural substrates.
Menzel R, Muller U., Annu. Rev. Neurosci. 19(), 1996
PMID: 8833448
Visual responses of interneurones in the posterior median protocerebrum and the central complex of the honeybee Apis mellifera
Milde J.., 1988
Neural organization and visual processing in the anterior optic tubercle of the honeybee brain.
Mota T, Yamagata N, Giurfa M, Gronenberg W, Sandoz JC., J. Neurosci. 31(32), 2011
PMID: 21832175
The free-flight response of Drosophila to motion of the visual environment.
Mronz M, Lehmann FO., J. Exp. Biol. 211(Pt 13), 2008
PMID: 18552291
Visual place learning in Drosophila melanogaster.
Ofstad TA, Zuker CS, Reiser MB., Nature 474(7350), 2011
PMID: 21654803
Visual processing in the central bee brain.
Paulk AC, Dacks AM, Phillips-Portillo J, Fellous JM, Gronenberg W., J. Neurosci. 29(32), 2009
PMID: 19675233
Higher order visual input to the mushroom bodies in the bee, Bombus impatiens
Paulk AngeliqueC, Gronenberg Wulfila., Arthropod structure & development. 37(6), 2008
PMID: IND44182131
The processing of color, motion, and stimulus timing are anatomically segregated in the bumblebee brain.
Paulk AC, Phillips-Portillo J, Dacks AM, Fellous JM, Gronenberg W., J. Neurosci. 28(25), 2008
PMID: 18562602
Bumblebee calligraphy: the design and control of flight motifs in the learning and return flights of Bombus terrestris.
Philippides A, de Ibarra NH, Riabinina O, Collett TS., J. Exp. Biol. 216(Pt 6), 2013
PMID: 23447668
Behavioural state affects motion-sensitive neurones in the fly visual system.
Rosner R, Egelhaaf M, Warzecha AK., J. Exp. Biol. 213(2), 2010
PMID: 20038668
Blowfly flight and optic flow. I. Thorax kinematics and flight dynamics
Schilstra C, Hateren JH., J. Exp. Biol. 202 (Pt 11)(), 1999
PMID: 10229694
Interindividual variation of eye optics and single object resolution in bumblebees.
Spaethe J, Chittka L., J. Exp. Biol. 206(Pt 19), 2003
PMID: 12939375
Visual motor computations in insects.
Srinivasan MV, Zhang S., Annu. Rev. Neurosci. 27(), 2004
PMID: 15217347
Honeybee navigation: nature and calibration of the "odometer".
Srinivasan MV, Zhang S, Altwein M, Tautz J., Science 287(5454), 2000
PMID: 10657298
Visual navigation in flying insects.
Srinivasan MV, Zhang SW., Int. Rev. Neurobiol. 44(), 2000
PMID: 10605642
How honeybees make grazing landings on flat surfaces.
Srinivasan MV, Zhang SW, Chahl JS, Barth E, Venkatesh S., Biol Cybern 83(3), 2000
PMID: 11007294
The visual control of landing and obstacle avoidance in the fruit fly Drosophila melanogaster.
van Breugel F, Dickinson MH., J. Exp. Biol. 215(Pt 11), 2012
PMID: 22573757
Blowfly flight and optic flow. II. Head movements during flight
Hateren JH, Schilstra C., J. Exp. Biol. 202 (Pt 11)(), 1999
PMID: 10229695
Odometry and insect navigation.
Wolf H., J. Exp. Biol. 214(Pt 10), 2011
PMID: 21525309
Orientation flights of solitary wasps (Cerceris, Sphecidae, Hymenoptera). I. Description of flights
Zeil J.., 1993
Orientation flights of solitary wasps (Cerceris; Sphecidae; Hymenoptera). II. Similarities between orientation and return flights and the use of motion parallax
Zeil J.., 1993
Visual homing: an insect perspective.
Zeil J., Curr. Opin. Neurobiol. 22(2), 2012
PMID: 22221863
Visual homing in insects and robots
Zeil J., Boeddeker N., Stürzl W.., 2009
Structure and function of learning flights in ground-nesting bees and wasps
Zeil J, Kelber A, Voss R., J. Exp. Biol. 199(Pt 1), 1996
PMID: 9317729
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 25309374
PubMed | Europe PMC

Suchen in

Google Scholar