Visual course control in flies relies on neuronal computation of object and background motion

Abstract

The spatial distribution of light intensity received by the eyes changes continually when an animal moves around in its environment. These retinal activity patterns contain a wealth of information on theVisual orientation greatly relies on the evaluation of the global visual motion patterns received by the eyes when an animal moves around. These motion patterns depend in a characteristic way on the trajectory described by the moving animal as well as on the particular three-dimensional structure of the visual environment z'2. Consider, for instance, two simple commonplace situations. In the first, a moving animal unintentionally deviates from its course. This results in a displacement of the entire visual scene, which contains a strong rotational component. When this rotational component is extracted from the retinal motion pattern, it can be used to control the compensatory optomotor responses of the animal. In this way, the course may be stabilized against internal and external disturbances. A different situation is encountered when the animal passes nearby objects located in front of a more distant background. The retinal images of these objects and their background then move relative to each other leading to discontinuities in the motion field. This relative motion may indicate the existence of nearby stationary or moving objects. This information can be used to discriminate objects from their background and might serve as the basic cue in various visual orientation tasks, such as fixation of stationary objects or pursuit of moving targets. These types of global retinal motion patterns do not only occur when the animal moves around bodily. Similar motion patterns may also arise during head and eye movements. This review concentrates on recent studies on the visual system of the fly, which has proved, during the past few decades, to be a suitable model system for the elucidation of the neuronal computations underlying various behavioural motion-dependent tasks 3'4. We analyse the basic mechanisms by which the nervous system of the fly processes coherent largefield motion, and relative motion between objects and background, and how these motion patterns are exploited in mediating optomotor course stabilization and object-induced orientation. Whether related mechanisms play a role in evaluating global retinal motion patterns in other species has yet to be established, although it is not unreasonable to expect that this will be the case. This has already been shown for the mechanisms underlying other motion information processing tasks. The basic mechanism of local movement detection for instance (see below), which was initially discovered in the insect visual system, was later also found in vertebrates, including iTlan ~8.

Detection of object motion by a fly neuron during simulated flight

“…Consequently, the turning responses were concluded to be mediated mainly by the object detection system. On the level of the lobula plate the object detection system is supposed to be represented by the FD-cells (Egelhaaf 1985a, b, c;Egelhaaf et al 1988;Reichardt et al 1989). In the behavioural experiments of Kimmerle et al (1997), the object was positioned in the most sensitive part of the FD1b-cell's receptive ®eld.…”

“…FD-cells are output elements of the lobula plate and project into the lateral protocerebrum where they probably synapse on descending neurons. FD-cells have been suggested to play a crucial role in mediating object-directed turning responses (Egelhaaf 1985a,b,c;Egelhaaf et al 1988;Reichardt et al 1989;Hausen and Wehrhahn 1990). It has been suggested recently that, in addition to the FD-cells described by Egelhaaf (1985b), further types of¯y TCs exist which also exhibit small-®eld-tuning (Gauck and Borst 1999).…”

Visual afferences to flight steering muscles controlling optomotor responses of the fly

“…Behavioral response components as expressed in free (Land and Collett 1974;Collett 1980a, b;Wehrhahn etal. 1982;Wagner 1986a, b) and tethered flight (Reichardt and Poggio 1976;Reichardt et al 1983;Reichardt 1986;tteisenberg and Wolf 1984;Wehrhahn 1985;Egelhaaf et al 1988) were studied, as well as the response properties of visual interneurons (Hausen 1984;Egelhaaf et al 1988;Hausen and Egelhaaf 1989). Moreover, there are various studies concentrating on motor and mechanical aspects of flight control in flies (for review see Nachtigall 1983).…”

“…The FD-cells, on the other hand, signal retinal image displacements of relatively small objects against the background. Their functional significance could, therefore, involve orientation towards objects (Egelhaaf 1985 a, b;Egelhaaf et al 1988).…”

Photo-ablation of single neurons in the fly visual system reveals neural circuit for the detection of small moving objects

“…This appears to be all the more interesting as we know the functional context of this circuit. By comparing behavioral responses of tethered flies with the response characteristics of the FDl-cell, the FDl-cell has been concluded to play a decisive role in discriminating moving objects from their background and mediating orientation turns towards them [7,8,11,27]. Hence, the circuit established in the present study is one of the very few examples where it has been possible to link visual orientation behavior to network interactions at the cellular level.…”