Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster.

Flies display a sophisticated suite of aerial behaviours that require rapid sensory-motor processing. Like all insects, flight control in flies is mediated in part by motion-sensitive visual interneurons that project to steering motor circuitry within the thorax. Flies, however, possess a unique flight control equilibrium sense that is encoded by mechanoreceptors at the base of the halteres, small dumb-bell-shaped organs derived through evolutionary transformation of the hind wings. To study the input of the haltere system onto the flight control system, I constructed a mechanically oscillating flight arena consisting of a cylindrical array of light-emitting diodes that generated the moving image of a 30 degrees vertical stripe. The arena provided closed-loop visual feedback to elicit fixation behaviour, an orientation response in which flies maintain the position of the stripe in the front portion of their visual field by actively adjusting their wing kinematics. While flies orientate towards the stripe, the entire arena was swung back and forth while an optoelectronic device recorded the compensatory changes in wing stroke amplitude and frequency. In order to reduce the background changes in stroke kinematics resulting from the animal's closed-loop visual fixation behaviour, the responses to eight identical mechanical rotations were averaged in each trial. The results indicate that flies possess a robust equilibrium reflex in which angular rotations of the body elicit compensatory changes in both the amplitude and stroke frequency of the wings. The results of uni- and bilateral ablation experiments demonstrate that the halteres are required for these stability reflexes. The results also confirm that halteres encode angular velocity of the body by detecting the Coriolis forces that result from the linear motion of the haltere within the rotating frame of reference of the fly's thorax. By rotating the flight arena at different orientations, it was possible to construct a complete directional tuning map of the haltere-mediated reflexes. The directional tuning of the reflex is quite linear such that the kinematic responses vary as simple trigonometric functions of stimulus orientation. The reflexes function primarily to stabilize pitch and yaw within the horizontal plane.     

Haltere activity in a flightless hippoboscid fly, Crataerina pallida

The halteres of the subapterous fly parasite of swifts, Crataerina pallida, retain a full complement of sensilla. They beat during and for many minutes after wing extension, leg movements and other forms of activity. They can also be caused to beat by a variety of visual and mechanical stimuli, including sound pulses at up to 2 kHz, for several minutes in the absence of other movements. Fed flies show markedly reduced locomotory responsiveness compared to unfed flies, but the halteres of both groups appear to be equally responsive. Haltere extirpation or inactivation does not appear to reduce ocomotory responsiveness. The possibility that haltere activity depresses responsiveness is discussed.     

Angular acceleration,compensatory head movements and the halteres of flies (Lucilia serricata)

Summary Tethered flies were subjected to accelerations about their vertical axes while flying or walking. These accelerations were applied either suddenly to stationary animals or continuously by oscillating the animal from side to side. Head and wing movements resulting from the imposed angular accelerations were photographed with a camera and a stroboscopic flash.Analysis of the photographs shows that the wing movements act to counter the imposed angular accelerations and that during sinusoidal oscillations about the vertical axis, head turns are in antiphase with angular acceleration.Head turns do not occur when the halteres are absent or present and not oscillating. When oscillating, the halteres detect high values of angular acceleration, outside the known capabilities of the visual movement detection system.     

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.     

The initiation and control of rapid flight maneuvers in fruit flies

Fruit flies alter flight direction by generating rapid, stereotypedturns, called saccades. The successful implementation of thesequick turns requires a well-tuned orchestration of neural circuits,musculo-skeletal mechanics, and aerodynamic forces. The changesin wing motion required to accomplish a saccade are quite subtle,as dictated by the inertial dynamics of the fly's body. A flyfirst generates torque to begin accelerating in the intendeddirection, but then must quickly create counter-torque to decelerate.Several lines of evidence suggest that the initial turn is initiatedby visual expansion, whereas the subsequent counter-turn istriggered by the gyroscopic halteres. This integrated analysisindicates how the functional organization of neural circuitscontrolling behavior is rigidly constrained by the physicalinteraction between an animal and the external world.     

昆虫平衡棒的发育及功能

平衡棒(haltere)是双翅目昆虫后翅特化而成的结构,可在飞行中起重要作用。平衡棒基部的感受器可以检测到飞行中的惯性力,向运动神经元提供反馈,迅速地平衡身体并纠正航向。昆虫的平衡棒由成虫盘发育形成,其特化受HOX基因(Ultrabithorax, Ubx)调控。发育成熟的平衡棒由两层上皮细胞组成,末端球状结构内部充满高度空泡化的细胞,基部具有大量感器。平衡棒的运动由独立的肌肉控制,相对于同侧的翅反向移动,翅与平衡棒的协同运动对于昆虫起飞和维持平衡十分重要。近年来,平衡棒的导航原理越来越多地应用于仿生学研究中,基于果蝇平衡棒的结构和功能,研制出多种飞行器的导航设备。本文结合近年来相关领域的研究成果,就平衡棒的发育、形态结构、功能和仿生应用等方面的研究进展进行综述,为深入理解昆虫平衡棒的发育机制和生物学功能提供参考。     

Odour boosts visual object approach in flies

Multisensory integration is synergistic—input from one sensory modality might modulate the behavioural response to another. Work in flies has shown that a small visual object presented in the periphery elicits innate aversive steering responses in flight, likely representing an approaching threat. Object aversion is switched to approach when paired with a plume of food odour. The ‘open-loop’ design of prior work facilitated the observation of changing valence. How does odour influence visual object responses when an animal has naturally active control over its visual experience? In this study, we use closed-loop feedback conditions, in which a fly''s steering effort is coupled to the angular velocity of the visual stimulus, to confirm that flies steer toward or ‘fixate’ a long vertical stripe on the visual midline. They tend either to steer away from or ‘antifixate’ a small object or to disengage active visual control, which manifests as uncontrolled object ‘spinning’ within this experimental paradigm. Adding a plume of apple cider vinegar decreases the probability of both antifixation and spinning, while increasing the probability of frontal fixation for objects of any size, including a normally typically aversive small object.     

Operant Learning of Drosophila at the Torque Meter

For experiments at the torque meter, flies are kept on standard fly medium at 25°C and 60% humidity with a 12hr light/12hr dark regime. A standardized breeding regime assures proper larval density and age-matched cohorts. Cold-anesthetized flies are glued with head and thorax to a triangle-shaped hook the day before the experiment. Attached to the torque meter via a clamp, the fly''s intended flight maneuvers are measured as the angular momentum around its vertical body axis. The fly is placed in the center of a cylindrical panorama to accomplish stationary flight. An analog to digital converter card feeds the yaw torque signal into a computer which stores the trace for later analysis. The computer also controls a variety of stimuli which can be brought under the fly''s control by closing the feedback loop between these stimuli and the yaw torque trace. Punishment is achieved by applying heat from an adjustable infrared laser.     

Dynamic properties of large-field and small-field optomotor flight responses in <Emphasis Type="Italic">Drosophila</Emphasis>

Optomotor flight control in houseflies shows bandwidth fractionation such that steering responses to an oscillating large-field rotating panorama peak at low frequency, whereas responses to small-field objects peak at high frequency. In fruit flies, steady-state large-field translation generates steering responses that are three times larger than large-field rotation. Here, we examine the optomotor steering reactions to dynamically oscillating visual stimuli consisting of large-field rotation, large-field expansion, and small-field motion. The results show that, like in larger flies, large-field optomotor steering responses peak at low frequency, whereas small-field responses persist under high frequency conditions. However, in fruit flies large-field expansion elicits higher magnitude and tighter phase-locked optomotor responses than rotation throughout the frequency spectrum, which may suggest a further segregation within the large-field pathway. An analysis of wing beat frequency and amplitude reveals that mechanical power output during flight varies according to the spatial organization and motion dynamics of the visual scene. These results suggest that, like in larger flies, the optomotor control system is organized into parallel large-field and small-field pathways, and extends previous analyses to quantify expansion-sensitivity for steering reflexes and flight power output across the frequency spectrum.     

Characterisation of Predator‐Directed Displays in Tephritid Flies

Flies of the family Tephritidae are known to perform a display in front of their salticid spider predators. This display involves extending the wings while the fly moves from side to side. The wings of many of fly species are banded, and in some species, these bands are thought to deter their predators by mimicking the leg patterns of salticids. However, as this display is also seen in non‐mimicking flies, there is some uncertainty over the functional significance of these displays. In this study, we explored the efficacy of displays by the lightly banded but non‐mimicking Mexican fruit fly (Anastrepha ludens) in deterring attacks by the salticids Paraphidippus aurantius and Phidippus bidentatus. We tested the effect of band visibility and the fly's physiological condition on the production of these displays and the probability of attack by salticids. We filmed the interactions of flies and spiders and analysed fly displays in the presence of the salticid. We show that the fly's display deters salticids and promotes the fly's chances of survival and that the presence or absence of bands does not alter the possibility of attack. Flies fed on different quality diets showed similar rates of display. Our results suggest that tephritid flies deter attacks because of their display and not their appearance.     

Takeoff diversity in Diptera

The order Diptera (true flies) are named for their two wings because their hindwings have evolved into specialized mechanosensory organs called halteres. Flies use halteres to detect body rotations and maintain stability during flight and other behaviours. The most recently diverged dipteran monophyletic subsection, the Calyptratae, is highly successful, accounting for approximately 12% of dipteran diversity, and includes common families like house flies. These flies move their halteres independently from their wings and oscillate their halteres during walking. Here, we demonstrate that this subsection of flies uses their halteres to stabilize their bodies during takeoff, whereas non-Calyptratae flies do not. We find that flies of the Calyptratae are able to take off more rapidly than non-Calyptratae flies without sacrificing stability. Haltere removal decreased both velocity and stability in the takeoffs of Calyptratae, but not other flies. The loss of takeoff velocity following haltere removal in Calyptratae (but not other flies) is a direct result of a decrease in leg extension speed. A closely related non-Calyptratae species (D. melanogaster) also has a rapid takeoff, but takeoff duration and stability are unaffected by haltere removal. Haltere use thus allows for greater speed and stability during fast escapes, but only in the Calyptratae clade.     

Internal Desynchronisation in Blow Fly (Calliphora vicina) Locomotor Activity Rhythms: Evidence for a Complex Circadian Pacemaker

The majority of blow flies (Calliphora vicina) display circadian locomotor activity rhythms that free-run with an unchanging period (τ) in darkness (DD), or entrain to a light-dark cycle (LD 1:23). However, a minority produce more complex patterns (spontaneous changes in τ, arrhythmicity, or 'split' rhythms) in DD, or undergo rhythm dissociation ('internal desynchronisation') when the light pulses of LD 1:23 initially illuminate the subjective night. These patterns are interpreted as evidence for a complex, multioscillatory and multicellular, structure of the insects' circadian system, and this complexity is discussed in terms of the neuronal architecture of the fly's brain.     

Coding Efficiency of Fly Motion Processing Is Set by Firing Rate,Not Firing Precision

To comprehend the principles underlying sensory information processing, it is important to understand how the nervous system deals with various sources of perturbation. Here, we analyze how the representation of motion information in the fly''s nervous system changes with temperature and luminance. Although these two environmental variables have a considerable impact on the fly''s nervous system, they do not impede the fly to behave suitably over a wide range of conditions. We recorded responses from a motion-sensitive neuron, the H1-cell, to a time-varying stimulus at many different combinations of temperature and luminance. We found that the mean firing rate, but not firing precision, changes with temperature, while both were affected by mean luminance. Because we also found that information rate and coding efficiency are mainly set by the mean firing rate, our results suggest that, in the face of environmental perturbations, the coding efficiency is improved by an increase in the mean firing rate, rather than by an increased firing precision.     

Evidence for spatial clines and mixed geographic modes of speciation for North American cherry‐infesting Rhagoletis (Diptera: Tephritidae) flies

An important criterion for understanding speciation is the geographic context of population divergence. Three major modes of allopatric, parapatric, and sympatric speciation define the extent of spatial overlap and gene flow between diverging populations. However, mixed modes of speciation are also possible, whereby populations experience periods of allopatry, parapatry, and/or sympatry at different times as they diverge. Here, we report clinal patterns of variation for 21 nuclear‐encoded microsatellites and a wing spot phenotype for cherry‐infesting Rhagoletis (Diptera: Tephritidae) across North America consistent with these flies having initially diverged in parapatry followed by a period of allopatric differentiation in the early Holocene. However, mitochondrial DNA (mtDNA) displays a different pattern; cherry flies at the ends of the clines in the eastern USA and Pacific Northwest share identical haplotypes, while centrally located populations in the southwestern USA and Mexico possess a different haplotype. We hypothesize that the mitochondrial difference could be due to lineage sorting but more likely reflects a selective sweep of a favorable mtDNA variant or the spread of an endosymbiont. The estimated divergence time for mtDNA suggests possible past allopatry, secondary contact, and subsequent isolation between USA and Mexican fly populations initiated before the Wisconsin glaciation. Thus, the current genetics of cherry flies may involve different mixed modes of divergence occurring in different portions of the fly''s range. We discuss the need for additional DNA sequencing and quantification of prezygotic and postzygotic reproductive isolation to verify the multiple mixed‐mode hypothesis for cherry flies and draw parallels from other systems to assess the generality that speciation may commonly involve complex biogeographies of varying combinations of allopatric, parapatric, and sympatric divergence.     

Looking for Myself: Current Multisensory Input Alters Self-Face Recognition

How do I know the person I see in the mirror is really me? Is it because I know the person simply looks like me, or is it because the mirror reflection moves when I move, and I see it being touched when I feel touch myself? Studies of face-recognition suggest that visual recognition of stored visual features inform self-face recognition. In contrast, body-recognition studies conclude that multisensory integration is the main cue to selfhood. The present study investigates for the first time the specific contribution of current multisensory input for self-face recognition. Participants were stroked on their face while they were looking at a morphed face being touched in synchrony or asynchrony. Before and after the visuo-tactile stimulation participants performed a self-recognition task. The results show that multisensory signals have a significant effect on self-face recognition. Synchronous tactile stimulation while watching another person''s face being similarly touched produced a bias in recognizing one''s own face, in the direction of the other person included in the representation of one''s own face. Multisensory integration can update cognitive representations of one''s body, such as the sense of ownership. The present study extends this converging evidence by showing that the correlation of synchronous multisensory signals also updates the representation of one''s face. The face is a key feature of our identity, but at the same time is a source of rich multisensory experiences used to maintain or update self-representations.     

Coordinates of Human Visual and Inertial Heading Perception

Heading estimation involves both inertial and visual cues. Inertial motion is sensed by the labyrinth, somatic sensation by the body, and optic flow by the retina. Because the eye and head are mobile these stimuli are sensed relative to different reference frames and it remains unclear if a perception occurs in a common reference frame. Recent neurophysiologic evidence has suggested the reference frames remain separate even at higher levels of processing but has not addressed the resulting perception. Seven human subjects experienced a 2s, 16 cm/s translation and/or a visual stimulus corresponding with this translation. For each condition 72 stimuli (360° in 5° increments) were delivered in random order. After each stimulus the subject identified the perceived heading using a mechanical dial. Some trial blocks included interleaved conditions in which the influence of ±28° of gaze and/or head position were examined. The observations were fit using a two degree-of-freedom population vector decoder (PVD) model which considered the relative sensitivity to lateral motion and coordinate system offset. For visual stimuli gaze shifts caused shifts in perceived head estimates in the direction opposite the gaze shift in all subjects. These perceptual shifts averaged 13 ± 2° for eye only gaze shifts and 17 ± 2° for eye-head gaze shifts. This finding indicates visual headings are biased towards retina coordinates. Similar gaze and head direction shifts prior to inertial headings had no significant influence on heading direction. Thus inertial headings are perceived in body-centered coordinates. Combined visual and inertial stimuli yielded intermediate results.     

Visual system of the stalk-eyed fly,Cyrtodiopsis quinqueguttata (Diopsidae,Diptera): an anatomical investigation of unusual eyes

Diopsid flies have eye stalks up to a centimeter in length, displacing the retina laterally from the rest of the head. This bizarre condition, called hypercephaly, is rare, but has evolved independently among several insect orders and is most common in flies (Diptera). Earlier studies of geometrical optics and behavior have led to various hypotheses about possible adaptive advantages of eye stalks, such as enhanced stereoscopic vision while other hypothesis suggest that eye stalks are an outcome of sexual selection. Here, we focus on how these curious distortions of head/eye morphology are accompanied by changes in the neural organization of the visual system of Cyrtodiopsis quinqueguttata. Histological examinations reveal that the optic lobes, lamina (La), medulla (Me), lobula (Lo), and lobula plate (LP) are contained entirely within the fly's eye bulbs, which are located at the distal ends of the eye stalks. We report that the organization of the peripheral visual system (La and Me) is similar to that of other Diptera (e.g., Musca and Drosophila), but deeper visual areas (Lo and LP) have been more strongly modified. For example, in both the lobula and lobula plate, fewer but larger giant collector neurons are found. The most pronounced difference is the reduction in the number of wide-field vertical cells of the lobula plate, where there are only four relatively large fibers, as opposed to 11 in Musca. The “fewer but larger” neural organization may enhance the conduction velocities of these cells, but may result in a loss of spatial resolution. At the base of the eye bulb, axon bundles collect and form a long optic nerve that extends the length of the eye stalk. We suggest that this organization of the diopsid visual system provides evidence for the costs of possessing long eye stalks. © 1998 John Wiley & Sons, Inc. J Neurobiol 37: 449–468, 1998     

The drosophila aeroplane mutant is caused by an I-element insertion into a tissue-specific teashirt enhancer motif.

In Drosophila melanogaster, aeroplane (ae) is a regulatory allele of teashirt (tsh), and the mutant wing posture phenotype of homozygous ae flies is caused by a defect in the hinge region of the wing, whereby the base of the wing at the proximal ventral radius is fused to the thorax in the region of the pleural wing process. The apparent paralysis of the wings and the drooping halteres are caused by an I-element insertion into a 3' noncoding sequence of tsh. The cis-acting regulatory element interrupted by the I element is required, to drive tsh expression in the regions of the developing adult that give rise to proximal wing and haltere tissues. Loss of this expression results in the fusion of the proximal structures of the wing and halteres to the thoracic cuticle. Further characterization of this tsh regulatory motif has now identified an additional enhancer activity directing tsh expression in tissues forming portions of the midgut. Subdivision of this midgut enhancer activity has identified putative negatively acting motifs.     

Properties of a motor output system involved in the optomotor response in flies

1. The optomotor response of tethered flying houseflies (Musca domestica) has been studied at the level of the neural output which controls the activities of some non-fibrillar flight muscles (N-muscles).-a) During visually induced turning responses in a given direction some N-muscles on the right side of the thorax are synergistically active together with other N-muscles on the left side of the thorax. The same muscles are inactive during turning reactions in the opposite direction while the corresponding antagonists are now active (synopsis in Table 1).-b) The response activities of the N-mussles show a considerable variation during the course of time in spite of constant visual input.-c) There is a strong tendency for N-muscle spikes to be phase-locked with respect to the wingbeat period.-d) The findings obtained fromMusca are in accordance with the corresponding results obtained fromCalliphora (Heide, 1971b).
2. TheN-muscle activities have also been investigated in tethered flying blowflies (Calliphora erythrocephala) which tried to yaw spontaneously with both wings beating. In spontaneous left (right) turn reactions the features of the observed neural output are nearly identical with the features of the motor output showing up during visually induced left (right) turn reactions.-A different motor output pattern has been found in flies with only one wing beating.
3. The wingbeat synchronous rhythm observed in spike trains from activeN-muscles is produced in the thorax without the participation of higher stages of the fly's CNS. On the other hand no distinct rhythms can be found in spike trains fromN-muscles of non-flying flies when their motoneurons are artificially activated by non-rhythmic stimuli. Afferent information from thoracic sense organs seems to be essential for the production of the rhythm observed during flight.
4. The results about the production of the wingbeat synchronous rhythm in spike trains fromN-muscles suggest that the information derived from the motion detectors only acts to gate the output needed to achieve yaw-turn reactions. The strength of the influence of signals from the motion detectors on the output producing system can be modified by the animals “state of excitement”.
5. A model is presented which summarizes some features of information processing in the output systems supplying theN-muscles of flies. Available physiological data are discussed in relation to the model.