During locomotion, the visual system is subjected to
continuous changes of the retinal images termed ‘optic flow’.
Turns to one side are accompanied by motion of the whole
retinal image in the opposite direction. Optic flow elicited
during rotation around a body axis is independent of the
distance of the objects in the visual surround. In contrast,
during translation, the retinal image of an object moves faster
than the retinal image of its background. Thus, the retinal
images of object and background move relative to each other.
Visual systems have developed strategies to use the
information provided by optic flow for different orientation
tasks. Many animals compensate global rotational image
motion around a body axis by eye, head and/or body
movements in the opposite direction. These optokinetic or
optomotor responses serve to stabilize the whole retinal image
or at least part of it (Miles and Wallman, 1993) and have been
interpreted in insects as a mechanism to compensate for
unintended deviations from a straight path of locomotion.
Compensatory optomotor responses have been studied in great
detail in the fly (e.g. Fermi and Reichardt, 1963; Götz, 1964,
1975; Wolf and Heisenberg, 1990). Relative motion in the
retinal image, in contrast, signals the presence of an object in
the visual field. Relative motion cues can therefore be used to
discriminate an object from its background. Detection and
fixation of objects solely defined by relative motion have been
investigated, for example, in humans (e.g. van Doorn and
Koenderink, 1982, 1983; Regan and Beverly, 1984), in
monkeys (e.g. Miles and Kawano, 1987), in bees (e.g.
Srinivasan et al., 1990; Kern et al., 1997) and in flies (Virsik
and Reichardt, 1976; Reichardt et al., 1983; Egelhaaf, 1985a;
Kimmerle et al., 1996, 1997).
In flies, flight control and visual orientation can be
investigated on different levels ranging from free-flight
behaviour to the neuronal and subcellular levels (for reviews,
see Egelhaaf and Borst, 1993; Egelhaaf and Warzecha, 1999).
Both optomotor turning behaviour and fixation responses can
be investigated under controlled stimulus conditions using
tethered flies in a flight simulator. In previous studies using the
flight simulator, flies were shown to fixate an object in the
frontal part of their visual field even if the object could be
discriminated from the background only by means of relative
motion (Virsik and Reichardt, 1976; Reichardt et al., 1983;
Egelhaaf, 1985a). These experiments were performed in a
cylindrical arena in which both the object and the background
could be rotated only around the fly’s vertical body axis. Hence,
flight situations in an environment were simulated in which no
translational optic flow was present, corresponding to a
situation in which object and background were at an infinite
distance from the fly. In a realistic stationary three-dimensional
environment, rotation of the animal around one of its body axes
alone does not provide any relative motion cues. Therefore, the
turning responses of tethered flies to objects defined by relative
motion were subsequently investigated during simulated
translational flight (Kimmerle et al., 1997). However, in these
1723 The Journal of Experimental Biology 203, 1723–1732 (2000)
Printed in Great Britain © The Company of Biologists Limited 2000
JEB2524
The ability of flies to detect and fixate objects moving
relative to their background was investigated in a flight
simulator during translational tethered flight. The fly
experienced optic flow that depended on its own actions
and reactions in a similar way as in free-flight (closed-loop)
conditions. Fixation of an object required turning
responses towards it. The simulated distances between the
fly, object and background were varied systematically by
changing the velocities with which the object and the
background pattern moved from the frontal to the back
part of the fly’s visual field. Fixation responses were only
elicited when the object was simulated to be closer than the
background. The fly’s fixation performance was better with
close than with more distant objects. Since, under many
stimulus conditions, fixation responses were either elicited
or entirely failed to be elicited, it is concluded that object
fixation behaviour is gated in the visuo-motor pathway.
Key words: flight, object fixation, vision, optic flow, closed loop,
blowfly, Lucilia sp.
Summary
Introduction
OBJECT FIXATION BY THE BLOWFLY DURING TETHERED FLIGHT IN A
SIMULATED THREE-DIMENSIONAL ENVIRONMENT
BERND KIMMERLE*, JUDITH EICKERMANN AND MARTIN EGELHAAF
Lehrstuhl für Neurobiologie, Fakultät für Biologie, Universität Bielefeld, Postfach 10 01 31, D-33501 Bielefeld,
Germany
*Present address: Institut für Neurobiologie, Freie Universität Berlin, Königin-Luise-Straße 28–30, D-14195 Berlin, Germany
(e-mail: kimmerle@zedat.fu-berlin.de)
Accepted 21 March; published on WWW 10 May 2000