Male flies of several genera chase females in high-speed acrobatic flight manoeuvres in the context of mating behaviour. The behavioural components of chasing behaviour belong to the fastest existing visually controlled systems. The males of investigated dipterean flies which exhibit chasing behaviour (Calliphora, Fannia, Lucilia, Musca, Sarcophaga) fixate the pursuit target in the frontal part of their eyes. In order to maintain the fixation in the frontal visual field, males pursue females in virtuosic flights, constantly compensating the course deviations during the chase. If the female is caught, the male will try to copulate and both animals will fall to the ground. (Land & Collett, 1974; Collett & Land, 1975; Wehrhahn, 1979; Wehrhahn et al., 1982; Zeil, 1983; Wagner, 1986a; Land, 1993)
A number of visual interneurons which only exist in males have been described in the brain of Calliphora and Sarcophaga. According to previous investigations, these male-specific neurons seem to be involved in the control of chasing behaviour. (Strausfeld, 1991; Gilbert & Strausfeld, 1991; Gronenberg & Strausfeld, 1991).
Behavioural, anatomical and physiological background of this project:
Behaviour:
Male flies pursue targets of different size and speed, fixating the image of the target in the frontal region of the retina. Flying animals have six degrees of freedom, three of rotation and
three of translation. At least two control systems, controlling forward speed and yaw rotations of the pursuer, are assumed to steer the flight muscles.
(Land & Collett, 1974; Wagner, 1986a,b).
The visual cues, which are used for chasing control have been analysed in behavioural experiments and in a phenomenologic model of the control system. The variation of the
relevant chase parameters - the speed and the velocity of the pursuit target - led to the following conclusions: The forward velocity of the chasing fly is controlled by the
angular size of the target. The pursuer continuously adapts its forward speed in order to maintain a certain retinal size of the target. The yaw rotations of the chasing fly
depend on the deviation of the target from the frontal midline of the pursuer. At the beginning of a chase, a turning reaction is performed in the direction of the detected target.
Thereby, it is fixated in the frontal region of the visual field. Course deviations during the chase are represented in varying target positions on the retina and compensated by
respective yaw rotations. (Boeddeker et al., 2003; Boeddeker & Egelhaaf, 2003a,b).
Anatomy and physiology of male-specific neurons:
The frontal retinal region which is used for image fixation, the "acute zone", shows male-specific specialisations at the retinal and neuronal levels: The resolution of the photoreceptor
cells is higher than in the residual retina. In the lobula (which is the frontal part of the third visual neuropile in the brain) of Calliphora and Sarcophaga, 12 types of visual
interneurons have been identified which only exist in males: Columnar elements (Mcol, male columnar) and 9 large non-columnar elements (MLG, male lobula giant) project from the
dorsal lobula to premotor descending neurons. The receptive fields of 10 of the 12 male-specific neurons subtend areas of the retina associated with the male acute zone.
The male lobula giant neuron 1, MLG1, is best investigated so far:
- Its receptive field subtends a large area of the dorsofrontal visual field and includes the region of binocular overlap. The maximum sensitivity lies within the acute
zone.
- Its directional sensitivity varies within the receptive field. The preferred directions are upwards movements and horizontal movements.
Male flies chase targets from below and behind. When approaching the target, the components of the retinal image are mainly upwards movements and horizontal movements.
Therefore, the directional selectivity of MLG1 could help to detect a small approaching target, like a female fly.
- The maximum velocity sensitivity lies between 150°-600°/s, which corresponds the actual retinal image velocities of Musca during a chase.
- Size characteristics: The response of MLG1 shows a preference for small objects, but activation also takes place on wide-field stimuli. The size characteristics of MLG1
correspond to the actual distribution of retinal image sizes during a chase. The MLG1 could therefore be involved in the control of forward speed.
We do not know much about the other male-specific neurons. Four MLGs show responses on motion, MLG1 and MLG2 show directional sensitivities.
Projections of the male-specific neurons:
The MLGs terminate in the lateral deutocerebrum on neurons, which descend in the thoracic ganglia. Such descending neurons reveal connections with motor neurons of the neck
muscles, of direct and indirect flight muscles and of the TTM (Tergotrochanter-muscle) which is involved in flight initiation.
(Strausfeld, 1991; Gilbert & Strausfeld, 1991;
Gronenberg & Strausfeld, 1991; Wachenfeld, 1994).
The aim of this project (start in April 2003):
The components of chasing behaviour have been elaborately investigated on the behavioural level. Additionally, anatomic and physiological data of the male-specific neurons
indicate that they are part of the neuronal control system for chasing behaviour. The aim of this project is to connect the previous studies. The male-specific neurons will be
stimulated with "natural" visual cues, as they occur on the eyes while males pursue artificial targets or females in the context of mating behaviour. To assess the responses of the
neurons, I use intracellular recordings from single neurons which are analysed in terms of their aptitude for participating in a control system of chasing behaviour.
References:
- Boeddeker N, Egelhaaf M (2003a) Steering a model fly: Simulations on visual pursuit in blowflies. Proc R Soc Lond B.
- Boeddeker N, Egelhaaf M (2003b) Chasing behaviour of blowflies: A smooth pursuit system generates saccades. Submitted.
- Boeddeker N, Kern R, Egelhaaf M (2003) Chasing a dummy target: Smooth pursuit and velocity control in male blowflies. Proc R Soc Lond B 270: 393-399.
- Collett TS, Land MF (1975) Visual control of flight behaviour in the hoverfly Syritta pipiens L. J Comp Physiol 99: 1-66.
- Gilbert C, Strausfeld NJ (1991) The functional organization of male-specific visual neurons in flies. J Comp Physiol A 169: 395-411.
- Gronenberg W, Strausfeld NJ (1991) Descending pathways connecting the male-specific visual system of flies to the neck and flight motor. J Comp Physiol A 169: 413-426.
- Land MF (1993) Chasing and pursuit in the dolichopodid fly Poecilobothrus nobilitatus. J Comp Physiol A 173: 605-613.
- Land MF, Collett TS (1974) Chasing behaviour of houseflies (Fannia canicularis). A description and analysis. J Comp Physiol 89: 331-357.
- Strausfeld NJ (1991) Structural organisation of male-specific visual neurons in calliphorid optic lobes. J Comp Physiol A 169: 379-393.
- Wachenfeld A, (1994) Elektrophysiologische Untersuchungen und funktionelle Charakterisierung männchenspezifischer visueller Interneurone der Schmeißfliege Calliphora erythrocephala (Meig.). Doctoral Dissertation. Universität Köln, Germany.
- Wagner H (1986a) Flight performance and visual control of the flight of the free-flying housefly (Musca domestica). II. Pursuit of targets. Phil Trans R Soc Lond B 312: 553-579.
- Wagner H (1986b) Flight performance and visual control of flight of the free-flying housefly (Musca domestica). III. Interactions between angular movement induced by wide- and smallfield stimuli. Phil Trans R Soc Lond B 312: 581-595.
- Wehrhahn C (1979) Sex-specific differences in the chasing behaviour of houseflies (Musca). Biol Cybern 32: 239-241.
- Wehrhahn C, Poggio T, Bülthoff H (1982) Tracking and chasing in houseflies (Musca). Biol Cybern 45: 123-130.
- Zeil J (1983) Sexual dimorphism in the visual system of flies: The free flight behaviour of male Bibionidae (Diptera). J Comp Physiol [A] 150: 395-412.
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