Visual gaze control during peering flight manoeuvres in honeybees

Böddeker N, Hemmi JM (2010)
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES 277(1685): 1209-1217.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
OA 666.92 KB
Autor*in
Böddeker, NorbertUniBi; Hemmi, Jan M.
Abstract / Bemerkung
As animals travel through the environment, powerful reflexes help stabilize their gaze by actively maintaining head and eyes in a level orientation. Gaze stabilization reduces motion blur and prevents image rotations. It also assists in depth perception based on translational optic flow. Here we describe side-to-side flight manoeuvres in honeybees and investigate how the bees' gaze is stabilized against rotations during these movements. We used high-speed video equipment to record flight paths and head movements in honeybees visiting a feeder. We show that during their approach, bees generate lateral movements with a median amplitude of about 20 mm. These movements occur with a frequency of up to 7 Hz and are generated by periodic roll movements of the thorax with amplitudes of up to +/-60 degrees. During such thorax roll oscillations, the head is held close to horizontal, thereby minimizing rotational optic flow. By having bees fly through an oscillating, patterned drum, we show that head stabilization is based mainly on visual motion cues. Bees exposed to a continuously rotating drum, however, hold their head fixed at an oblique angle. This result shows that although gaze stabilization is driven by visual motion cues, it is limited by other mechanisms, such as the dorsal light response or gravity reception.
Stichworte
visuomotor control; flight; bee; control; gaze stabilization; vision; behaviour
Erscheinungsjahr
2010
Zeitschriftentitel
PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
Band
277
Ausgabe
1685
Seite(n)
1209-1217
ISSN
0962-8452
eISSN
1471-2954
Page URI
https://pub.uni-bielefeld.de/record/1796503

Zitieren

Böddeker N, Hemmi JM. Visual gaze control during peering flight manoeuvres in honeybees. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES. 2010;277(1685):1209-1217.
Böddeker, N., & Hemmi, J. M. (2010). Visual gaze control during peering flight manoeuvres in honeybees. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 277(1685), 1209-1217. https://doi.org/10.1098/rspb.2009.1928
Böddeker, Norbert, and Hemmi, Jan M. 2010. “Visual gaze control during peering flight manoeuvres in honeybees”. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES 277 (1685): 1209-1217.
Böddeker, N., and Hemmi, J. M. (2010). Visual gaze control during peering flight manoeuvres in honeybees. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES 277, 1209-1217.
Böddeker, N., & Hemmi, J.M., 2010. Visual gaze control during peering flight manoeuvres in honeybees. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 277(1685), p 1209-1217.
N. Böddeker and J.M. Hemmi, “Visual gaze control during peering flight manoeuvres in honeybees”, PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, vol. 277, 2010, pp. 1209-1217.
Böddeker, N., Hemmi, J.M.: Visual gaze control during peering flight manoeuvres in honeybees. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES. 277, 1209-1217 (2010).
Böddeker, Norbert, and Hemmi, Jan M. “Visual gaze control during peering flight manoeuvres in honeybees”. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES 277.1685 (2010): 1209-1217.
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
2019-09-06T08:49:04Z
MD5 Prüfsumme
38c20dccd6784bf0053d92f5f84cc70d


17 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Complex gaze stabilization in mantis shrimp.
Daly IM, How MJ, Partridge JC, Roberts NW., Proc Biol Sci 285(1878), 2018
PMID: 29720419
The Dominant Role of Visual Motion Cues in Bumblebee Flight Control Revealed Through Virtual Reality.
Frasnelli E, Hempel de Ibarra N, Stewart FJ., Front Physiol 9(), 2018
PMID: 30108522
Regional differences in the preferred e-vector orientation of honeybee ocellar photoreceptors.
Ogawa Y, Ribi W, Zeil J, Hemmi JM., J Exp Biol 220(pt 9), 2017
PMID: 28213397
Honeybees in a virtual reality environment learn unique combinations of colour and shape.
Rusch C, Roth E, Vinauger C, Riffell JA., J Exp Biol 220(pt 19), 2017
PMID: 28751492
Neural basis of forward flight control and landing in honeybees.
Ibbotson MR, Hung YS, Meffin H, Boeddeker N, Srinivasan MV., Sci Rep 7(1), 2017
PMID: 29109404
How Wasps Acquire and Use Views for Homing.
Stürzl W, Zeil J, Boeddeker N, Hemmi JM., Curr Biol 26(4), 2016
PMID: 26877083
Advances and limitations of visual conditioning protocols in harnessed bees.
Avarguès-Weber A, Mota T., J Physiol Paris 110(3 pt a), 2016
PMID: 27998810
Controlling roll perturbations in fruit flies.
Beatus T, Guckenheimer JM, Cohen I., J R Soc Interface 12(105), 2015
PMID: 25762650
Visual motion-sensitive neurons in the bumblebee brain convey information about landmarks during a navigational task.
Mertes M, Dittmar L, Egelhaaf M, Boeddeker N., Front Behav Neurosci 8(), 2014
PMID: 25309374
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), 2013
PMID: 23197452
Tracking improves performance of biological collision avoidance models.
Pant V, Higgins CM., Biol Cybern 106(4-5), 2012
PMID: 22744199
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
Static and dynamic snapshots for goal localization in insects?
Dittmar L., Commun Integr Biol 4(1), 2011
PMID: 21509170
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

51 References

Daten bereitgestellt von Europe PubMed Central.

Anticipation of moving stimuli by the retina.
Berry MJ 2nd, Brivanlou IH, Jordan TA, Meister M., Nature 398(6725), 1999
PMID: 10192333
Peering—a locust behaviour pattern for obtaining motion parallax information
Collett T.., 1978
How ladybirds approach nearby stalks: a study of visual selectivity and attention
Collett T.., 1988
Depth vision in animals
Collett T., Harkness L.., 1982
Relative motion parallax and target localization in the locust,
Collett T., Paterson C.., 1991
Extracting egomotion from optic flow: limits of accuracy and neural matched filters
Dahmen H., Franz M., Krapp H.., 2001

Gibson J.., 1950
Effects of male age and cervical proprioceptors on sexual aerial pursuit by male flesh flies, (Diptera: Sarcophagidae)
Gilbert C., Kim M.., 2007
The role of certain optomotor reactions in regulating stability in the rolling plane during flight in the desert locust,
Goodman L.., 1965
The photoreceptor array of the dipteran retina
Hardie R.., 1986
Mechanosensory control of compensatory head roll during flight in the blowfly Meig
Hengstenberg R.., 1988
Multisensory control in insect oculomotor systems
Hengstenberg R.., 1993
Compensatory head roll in the blowfly during flight
Hengstenberg R., Sandeman D., Hengstenberg B.., 1986
A theory of insect vision: velocity parallax
Horridge G.., 1986
Object detection by relative motion in freely flying flies
Kimmerle B., Srinivasan M., Egelhaaf M.., 1996
Motion parallax as a source of distance information in locusts and mantids
Kral K., Poteser M.., 1997
Head movements of flies during visually guided flight
Land M.., 1973
Visual tracking and pursuit: humans and arthropods compared
Land M.., 1992
A survey of active vision in invertebrates
Land M., Collett T.., 1997

Lappe M.., 2000
Bees which turn back and look
Lehrer M.., 1991
Motion cues provide the bee's visual world with a third dimension
Lehrer M., Srinivasan M., Zhang S., Horridge G.., 1988
Ein Schweresinnesorgan der Honigbiene
Lindauer M., Nedel J.., 1959
The influence of head position on the flight behaviour of the fly,
Liske E.., 1977
Behavioral evidence for within-eyelet resolution in twisted-winged insects (Strepsiptera).
Maksimovic S, Layne JE, Buschbeck EK., J. Exp. Biol. 210(Pt 16), 2007
PMID: 17690229
Borstenfelder an den Gelenken als Schweresinnesorgane bei Ameisen und anderen Hymenopteren
Markl H.., 1962
Physiologie des Gleichgewichtssinnes bei fliegenden Libellen
Mittelstaedt H.., 1950
Mechanisms of visual distance perception in the hawk moth
Pfaff M., Varjú D.., 1991
Structure and kinematics of the prosternal organs and their influence on head position in the blowfly
Preuss T., Hengstenberg R.., 1992
Head movements in flies () produced by deflexion of the halteres
Sandeman D., Markl H.., 1980
Stabilizing gaze in flying blowflies.
Schilstra C, van Hateren JH., Nature 395(6703), 1998
PMID: 9790186
Summation of visual and mechanosensory feedback in Drosophila flight control.
Sherman A, Dickinson MH., J. Exp. Biol. 207(Pt 1), 2004
PMID: 14638840
The locust's use of motion parallax to measure distance.
Sobel EC., J. Comp. Physiol. A 167(5), 1990
PMID: 2074547
Active navigation with a monocular robot
Sobey P.., 1994
How insects infer range from visual motion
Srinivasan M.., 1993
Visual motor computations in insects.
Srinivasan MV, Zhang S., Annu. Rev. Neurosci. 27(), 2004
PMID: 15217347
The ocellar component of flight equilibrium control in dragonflies
Stange G.., 1981
Sensory systems and flight stability: what do insects measure and why?
Taylor G., Krapp H.., 2007
Blowfly flight and optic flow. II. Head movements during flight
Hateren JH, Schilstra C., J. Exp. Biol. 202 (Pt 11)(), 1999
PMID: 10229695
Active vision in insects: an analysis of object-directed zig-zag flights in wasps (, Eumenidae)
Voss R., Zeil J.., 1998
Visual scanning in the desert locust Forskal
Wallace G.., 1959
Visual fixation in freely flying bees
Wehner R., Flatt I.., 1977
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
Convergent processing in honeybee vision: multiple channels for the recognition of shape.
Zhang SW, Srinivasan MV, Collett T., Proc. Natl. Acad. Sci. U.S.A. 92(7), 1995
PMID: 11607523
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 20007175
PubMed | Europe PMC

Suchen in

Google Scholar