Visual control of straight flight in Drosophila melanogaster

Summary The optomotor system of Drosophila is investigated in a flight simulator in which the fly's yaw torque controls the angular velocity of the panorama (striped drum, negative feedback). Flies in the flight simulator maintain a stable orientation even in a homogeneously textured panorama without landmarks. During straight flight, torque is not zero. It consists of small pulses mostly alternating in polarity. The course is controlled by the duration (and possibly amplitude) of the pulses. The system operates under reafference control. By comparing the pulses with the visual input the system continuously measures and adjusts the efficacy of the torque output. The comparison, however, is not between angular velocity and yaw torque but, instead, between visual acceleration and pretorque, the first time derivative of torque. For comparison, the system first computes a cross-correlation. If the correlation coefficient is above a certain threshold the system calculates the external gain and adjusts its internal gain so as to keep the total gain constant. With the correlation coefficient below threshold, however, the system keeps the internal gain low despite the infinitely small external gain. We propose that for a reafferent optomotor system the coupling coefficient and the correlation coefficient of pretorque and visual acceleration are more relevant than the distinction between exafference and reafference.Abbreviation EMD elementary movement detector     

Visual flight control in naturalistic and artificial environments

Although the visual flight control strategies of flying insects have evolved to cope with the complexity of the natural world, studies investigating this behaviour have typically been performed indoors using simplified two-dimensional artificial visual stimuli. How well do the results from these studies reflect the natural behaviour of flying insects considering the radical differences in contrast, spatial composition, colour and dimensionality between these visual environments? Here, we aim to answer this question by investigating the effect of three- and two-dimensional naturalistic and artificial scenes on bumblebee flight control in an outdoor setting and compare the results with those of similar experiments performed in an indoor setting. In particular, we focus on investigating the effect of axial (front-to-back) visual motion cues on ground speed and centring behaviour. Our results suggest that, in general, ground speed control and centring behaviour in bumblebees is not affected by whether the visual scene is two- or three dimensional, naturalistic or artificial, or whether the experiment is conducted indoors or outdoors. The only effect that we observe between naturalistic and artificial scenes on flight control is that when the visual scene is three-dimensional and the visual information on the floor is minimised, bumblebees fly further from the midline of the tunnel. The findings presented here have implications not only for understanding the mechanisms of visual flight control in bumblebees, but also for the results of past and future investigations into visually guided flight control in other insects.     

Visual gaze control during peering flight manoeuvres in honeybees

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°. 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.     

Discontinuity of sarcoplasmic reticulum in the mid-sarcomere region in flight muscle of dragonflies

The sarcoplasmic reticulum organization of dragonfly flight muscles is analyzed, with particular reference to the doubling existing at H-band level. This doubling could be explained as a consequence of a regular discontinuity in the sarcoplasmic reticulum covering myofibrils. In each sarcomere, two sleeves of the sarcoplasmic reticulum seem to overlap forming a telescopic system which can slide outside each other during the lengthening and shortening movements of the fiber.     

Initiation of flight and pre-flight behaviour of anisopterous dragonflies Aeshna spp.

The start of flight of mature adult dragonflies (Aeshna spp.) was investigated using electrophysiological and photographic techniques already described. Flight begins with either an upwards or a downwards movement of the wings. Neuromuscular activity and wing vibrations resembling ‘warm-up’ in moths is reported in two species of Aeshna.     

Visual control of steering in locust flight: the effects of head movement on responses to roll stimuli

The contribution of head movement to the control of roll responses in flying locusts (Locusta migratoria) has been examined (i) on a flight balance, recording the angles through which the locust turns when following an artificial horizon; (ii) by recording activity in a pair of flight muscles in restrained conditions; and (iii) by observations on free flying locusts. Responses were compared when the head was free to turn about the thorax, as normal, and when the head was waxed to the thorax, blocking any relative motion between the two (head-fixed). These experiments suggest that the major signal generating corrective roll manoeuvres is the visual error between the angle of the head and the horizon, rather than a signal that includes a measure of the head-thorax angle.

Visual stabilization dynamics are enhanced by standing flight velocity

A flying insect must travel to find food, mates and sites for oviposition, but for a small animal in a turbulent world this means dealing with frequent unplanned deviations from course. We measured a fly''s sensory-motor impulse response to perturbations in optic flow. After an abrupt change in its apparent visual position, a fly generates a compensatory dynamical steering response in the opposite direction. The response dynamics, however, may be influenced by superimposed background velocity generated by the animal''s flight direction. Here we show that constant forward velocity has no effect on the steering responses to orthogonal sideslip perturbations, whereas constant parallel sideslip substantially shortens the lags and relaxation times of the linear dynamical responses. This implies that for flies stabilizing in sideslip, the control effort is strongly affected by the direction of background motion.     

Characteristics of dispersal in sexually mature dragonflies

Abstract.

• 1 The population dynamics of a natural population of Sympetrum danae (Sulzer) were studied, by means of a mark—release—recapture method, to find indications of dispersal by mature adults. Additional information on orientation and the influence of phenotype (including age), density and weather was obtained by observations under natural conditions and in a large outdoor field cage.
• 2 80% of all mature adults caught around the natural pond were estimated to be immigrants. Considerable immigration was confirmed by the abdomen length of unmarked matures which did not accord with that expected from the locally emerged population. Total numbers captured and the minimum number known to be alive fell sharply at the time when most individuals were mature. At the same time, new matures continued to enter and disappear from the study area at an increasing rate.
• 3 Dispersive behaviour (escape flights) in the field enclosure was primarily age dependent in both sexes: it occurred from an age of 25–30 days onwards. This coincides with the time-lag between the emergence peak and increased dispersal in the field. Secondary effects on escape flights suggested that males tended to abandon low density areas.
• 4 Males flew relatively more southward than females.

     

The ocelli control the flight course in honeybees

Abstract Fully-sighted honeybees and bees with all ocelli occluded were trained to fly through an arena to arrive at a feeding place. After training, the bees were exposed to side-light flashes during their feeding flights. The flight paths were recorded on video and analysed frame by frame at 40 ms intervals with reference to the main parameters, the coordinates of the thorax and the yaw angle of the bee. Course angles, translational course velocities and accelerations were calculated, and the responses to side light flashes evaluated with respect to 'on' and 'off.
Immediately after light on, fully-sighted bees respond slightly positively by yawing and flying toward the side light. Bees in which all ocelli are occluded are greatly disturbed and respond with negative yawing and flight path directions.
The ocelli apparently help to control phototactic alertness in the bee. They determine whether phototactic orienting or pattern-induced orienting behaviour is more important in a particular state of motivation. They help to minimize the level of disturbance in flight course control, obviously by activating a neuronal circuit with comparator attributes. It is assumed that this kind of compensation or suppression of phototactically guided reflexes occurs only for a few 100 ms. Consequently, the biological significance of light flashes shorter than 400 ms is very slight.
Fully-sighted bees decelerate strongly when a side light is switched on. Bees in which the ocelli are occluded behave less cautiously: they generally fly faster and need more reaction time. Thus, the ocelli help the bee to react photokinetically to photic stimuli in a much shorter time than do the compound eyes alone.     

Territorial behaviour in some Nigerian dragonflies

Males of seven species of Odonata were studied at a small pool (3.25 m²) in the grounds of the University of Ife. Each species had its characteristic time of arrival at the pool; those arriving early stayed late, and those arriving late left early.
The territories held by the males can be divided into two categories-, perch and patrol and continuous short term aerial. With the perchers and patrollers it is possible to distinguish a patrol area and a somewhat larger defended area. Forms with red bodies ( Trithemis and Crocothemis ) defended larger areas than the blue bodied Orthetrum microstigma. This last species showed variation in the size of territory with the number of males present.
No feeding activities were seen in the territories, which appeared to be held only for reproductive purposes. Although there was much intraspecific interaction over the pool there was little or no interspecific interaction, and the territories of different species overlapped considerably in space and time.     

Olfaction in dragonflies: electrophysiological evidence

The problem of olfaction in Paleoptera (Odonata, Ephemeroptera) cannot be considered fully elucidated until now. These insects have been traditionally considered anosmic, because their brain lacks glomerular antennal lobes, typically involved in Neoptera odor perception. In order to understand if the presumed coeloconic olfactory receptors described on the antennal flagellum of adult Odonata are really functioning, we performed an electrophysiological investigation with electroantennogram (EAG) and single cell recordings (SCR), using Libellula depressa L. (Odonata, Libellulidae) as a model species. Odors representing different chemical classes such as (Z)-3-hexenyl acetate (acetate ester), (E)-2-hexenal, octanal (aldehydes), (Z)-3-hexen-1-ol (alcohol), propionic acid, butyric acid (carboxylic acids), and 1,4-diaminobutane (amine) were tested. Most of the tested chemicals elicited depolarizing EAG responses in both male and female antennae; SCR show unambiguously for the first time the presence of olfactory neurons in the antennae of L. depressa and strongly support the olfactory function of the coeloconic sensilla located on the antennal flagellum of this species. Electrophysiological activity may not necessarily indicate behavioral activity, and the biological role of olfactory responses in Odonata must be determined in behavioral bioassays. This study represents a starting point for further behavioral, electrophysiological, neuroanatomical and molecular investigation on Odonata olfaction, a research field particularly interesting owing to the basal position of Paleoptera, also for tracing evolutionary trends in insect olfaction.     

Flight of the dragonflies and damselflies

This work is a synthesis of our current understanding of the mechanics, aerodynamics and visually mediated control of dragonfly and damselfly flight, with the addition of new experimental and computational data in several key areas. These are: the diversity of dragonfly wing morphologies, the aerodynamics of gliding flight, force generation in flapping flight, aerodynamic efficiency, comparative flight performance and pursuit strategies during predatory and territorial flights. New data are set in context by brief reviews covering anatomy at several scales, insect aerodynamics, neuromechanics and behaviour. We achieve a new perspective by means of a diverse range of techniques, including laser-line mapping of wing topographies, computational fluid dynamics simulations of finely detailed wing geometries, quantitative imaging using particle image velocimetry of on-wing and wake flow patterns, classical aerodynamic theory, photography in the field, infrared motion capture and multi-camera optical tracking of free flight trajectories in laboratory environments. Our comprehensive approach enables a novel synthesis of datasets and subfields that integrates many aspects of flight from the neurobiology of the compound eye, through the aeromechanical interface with the surrounding fluid, to flight performance under cruising and higher-energy behavioural modes.This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’.     

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

Summary In tethered flying house-flies (Musca domestica) visually induced turning reactions were monitored under open-loop conditions simultaneously with the spike activity of four types of steering muscles (M.b1, M.b2, M.I1, M.III1). Specific behavioral response components are attributed to the activity of particular muscles. Compensatory optomotor turning reactions to large-field image displacements mainly occur when the stimulus pattern oscillates at low frequencies. In contrast, turning responses towards objects are preferentially induced by motion of relatively small stimuli at high oscillation frequencies. The different steering muscles seem to be functionally specialized in that they contribute to the control of these behavioral responses in different ways. The muscles I1, III1 and b2 are preferentially active during small-field motion at high oscillation frequencies. They are much less active during small-field motion at low oscillation frequencies and large-field motion at all oscillation frequencies which were tested. M.b2 is most extreme in this respect. These steering muscles thus mediate mainly turns towards objects. In contrast, M.b1 responds best during large-field motion at low oscillation frequencies and, thus, is appropriate to control compensatory optomotor responses. However, the activity of this muscle is also strongly modulated during small-field motion at high oscillation frequencies and, therefore, may be involved also in the control of turns towards objects. These functional specializations of the different steering muscles in mediating different behavioral response components are related to the properties of two parallel visual pathways that are selectively tuned to large-field and small-field motion, respectively.Abbreviations FD (cell) figure detection (cell) - HS (cell) horizontal (cell)     

Visual control of wing beat frequency in Drosophila

The present study shows that the wing beat frequency of Drosophila is visually controlled and modulated in response to different optomotor stimuli.Whereas rotational large field stimuli do not appear to modulate wing beat frequency, single rotating vertical stripes increase or decrease wing beat frequency when moving back-to-front or front-to-back, respectively. Maximal modulations occur at lateral stripe positions.Expansion stimuli eliciting the landing response cause a marked increase in wing beat frequency. Parameters of this frequency response depend in a graded fashion on certain stimulus properties, and the frequency response co-habituates with the landing response. Several results indicate that the frequency response is an integral component of the landing response, although it can also occur when the characteristic front leg extension is not observed. The complex spatial input integration underlying the frequency response and other motor components of the landing response cannot easily be explained by a system of large field integration units, but might indicate the existence of local expansion detectors.