Steering a virtual blowfly: simulation of visual pursuit

The behavioural repertoire of male flies includes visually guided chasing after moving targets. The visuomotor control system for these pursuits belongs to the fastest found in the animal kingdom. We simulated a virtual fly, to test whether or not experimentally established hypotheses on the underlying control system are sufficient to explain chasing behaviour. Two operating instructions for steering the chasing virtual fly were derived from behavioural experiments: (i) the retinal size of the target controls the fly's forward speed and, thus, indirectly its distance to the target; and (ii) a smooth pursuit system uses the retinal position of the target to regulate the fly's flight direction. Low-pass filters implement neuronal processing time. Treating the virtual fly as a point mass, its kinematics are modelled in consideration of the effects of translatory inertia and air friction. Despite its simplicity, the model shows behaviour similar to that of real flies. Depending on its starting position and orientation as well as on target size and speed, the virtual fly either catches the target or follows it indefinitely without capture. These two behavioural modes of the virtual fly emerge from the control system for flight steering without implementation of an explicit decision maker.     

Characterisation of a blowfly male-specific neuron using behaviourally generated visual stimuli

The pursuit system controlling chasing behaviour in male blowflies has to cope with extremely fast and dynamically changing visual input. An identified male-specific visual neuron called Male Lobula Giant 1 (MLG1) is presumably one major element of this pursuit system. Previous behavioural and modelling analyses have indicated that angular target size, retinal target position and target velocity are relevant input variables of the pursuit system. To investigate whether MLG1 specifically represents any of these visual parameters we obtained in vivo intracellular recordings while replaying optical stimuli that simulate the visual signals received by a male fly during chasing manoeuvres. On the basis of these naturalistic stimuli we find that MLG1 shows distinct direction sensitivity and is depolarised if the target motion contains an upward component. The responses of MLG1 are jointly determined by the retinal position, the speed and direction, and the duration of target motimotion. Coherence analysis reveals that although retinal target size and position are in some way inherent in the responses of MLG1, we find no confirmation of the hypothesis that MLG1 encodes any of these parameters exclusively.     

Tracking and chasing in houseflies (Musca)

The flight trajectories of free flying female and male houseflies have been analyzed in 3 dimensions. Both female and male flies track other flies. The turning velocity α (around the vertical axis) is linearly dependent upon the horizontal angle ψ_F (that is the angle between the trajectory of the tracking fly and the target) for small values of ψ_F in females and for the whole range of ψ_F in males. The 3-dimensional velocity υ _xyz of the chasing fly is linearly dependent upon the distance between leading and chasing fly in males but not in females. Male chasing thus appears to be more efficient than female tracking. It is shown that earlier assumptions on visual control of flight in female flies derived from experiments on fixed flying flies are justified.     

雄蝇追逐飞行的加速度分析

本文报导了采用高速摄影技术,通过分析雄蝇追逐飞行的加速度对视觉制导问题所进行的研究.我们的结果如下:1.目标蝇的角位置与追逐蝇相应的角加速度分量之间,在追逐蝇的全视场中呈现非线性的关系.追逐蝇的水平角加速度分量与水平误差角在前视场中有较好的线性关系.追逐蝇的俯仰角加速度分量与俯仰误差角之间,当目标蝇位于前上半视场中时,呈现较好的线性关系.2.目标蝇相对追逐蝇的角运动对追逐蝇的相应角加速度分量也有影响,这种影响与目标蝇位置的关系不大.3.对于目标蝇在前后视场中的两种情况,两蝇间的距离对追逐蝇加速度大小影响的规律是不同的:当目标蝇在前视场中时,只经过较短的延迟时间两蝇间的距离与追逐蝇加速度大小出现了正的相关峰,而后视场中的情况不然,它需要较长的延迟时间.两蝇间距离的变化对追逐蝇加速度大小的影响也有类似的现象.4.在追逐过程中雄蝇利用背前区的小眼来追逐带头的目标雌蝇,而组织学研究在雄蝇背前区的小眼中发现了性特化的中心小网膜细胞,与行为研究的结果相呼应.5.文中最后对蝇视觉神经系统中如何获取目标绳的位置和运动参数的问题进行了讨论.     

雄蝇追逐行为的分析

本文报告了在自由飞行条件下雄蝇追逐的行为实验及其分析的初步结果.其结果如下:1.追逐雄蝇水平方向偏转的角速度dF_1线性地依赖于目标蝇水平方位误差角T_1的大小.当目标在前视场中,即空间误差角|G|<π/4时,线性回归直线的斜率约为37**;而当空间误差角|G|>π/4时,线性回归直线的斜率约为6.7.2.追逐雄蝇俯仰方向偏转角速度dF_2在(-(π/2),π/2)的范围内线性依赖于俯仰误差角T_2的大小,其回归直线的斜率约为14.3.雄蝇追逐行为中,水平方位误差角频数分布的直方图呈现为峰值在零点的对称型分布;而俯仰误差角T_2频数分布的直方图是非对称型的,即仰角出现的频数大大超过俯角出现的频数.4.雄蝇主要利用了两蝇间距离变化dD的信息以及目标误差角来控制向前飞行的速度V.当误差角小时(即目标在前视场中),dD一般为负值,说明两蝇间的距离减小,而雄蝇追逐飞行的加速度A却与dD呈现正的线性关系.当误差角大时(即目标位于后视场中),dD一般为正值,说明两蝇间的距离增加.     

Visual recognition of the host in the parasitoid fly Exorista japonica

We presented the tachinid fly Exorista japonica with moving host models: a freeze-dried larva of the common armyworm Mythimna separata, a black rubber tube, and a black rubber sheet, to examine the effects of size, curvature, and velocity on visual recognition of the host. The host models were moved around the fly on a metal arm driven by motor. The size of the larva, the velocity of movement, and the length and diameter of the rubber tube were varied. During the presentation of the host model, fixation, approach, and examination behaviours of the flies were recorded. The fly fixated on, approached, and examined the black rubber tube as well as the freeze-dried larva. Furthermore, the fly detected the black rubber tube at a greater distance than the larva. The rubber tube elicited higher rates of approach and examination responses than the rubber sheet, suggesting that curvature affects the responses of the flies. The length, diameter, and velocity of host models had little effect on response rates of the flies. During host pursuit, the fly appeared to walk towards the ends of the tube. These results suggest that the flies respond to the leading or trailing edges of a moving object and ignore the length and diameter of the object.     

Frame of reference transformations in motion perception during smooth pursuit eye movements

Smooth pursuit eye movements change the retinal image velocity of objects in the visual field. In order to change from a retinocentric frame of reference into a head-centric one, the visual system has to take the eye movements into account. Studies on motion perception during smooth pursuit eye movements have measured either perceived speed or perceived direction during smooth pursuit to investigate this frame of reference transformation, but never both at the same time. We devised a new velocity matching task, in which participants matched both perceived speed and direction during fixation to that during pursuit. In Experiment 1, the velocity matches were determined for a range of stimulus directions, with the head-centric stimulus speed kept constant. In Experiment 2, the retinal stimulus speed was kept approximately constant, with the same range of stimulus directions. In both experiments, the velocity matches for all directions were shifted against the pursuit direction, suggesting an incomplete transformation of the frame of reference. The degree of compensation was approximately constant across stimulus direction. We fitted the classical linear model, the model of Turano and Massof (2001) and that of Freeman (2001) to the velocity matches. The model of Turano and Massof fitted the velocity matches best, but the differences between de model fits were quite small. Evaluation of the models and comparison to a few alternatives suggests that further specification of the potential effect of retinal image characteristics on the eye movement signal is needed.     

Visual ground pattern modulates flight speed of male Oriental fruit moth Grapholita molesta

Insects flying in a horizontal pheromone plume must attend to visual cues to ensure that they make upwind progress. Moreover, it is suggested that flying insects will also modulate their flight speed to maintain a constant retinal angular velocity of terrestrial contrast elements. Evidence from flies and honeybees supports such a hypothesis, although tests with male moths and beetles flying in pheromone plumes are not conclusive. These insects typically fly faster at higher elevations above a high‐contrast ground pattern, as predicted by the hypothesis, although the increase in speed is not sufficient to demonstrate quantitatively that they maintain constant visual angular velocity of the ground pattern. To test this hypothesis more rigorously, the flight speed of male oriental fruit moths (OFM) Grapholita molesta Busck (Lepidoptera: Tortricidae) flying in a sex pheromone plume in a laboratory wind tunnel is measured at various heights (5–40 cm) above patterns of different spatial wavelength (1.8–90°) in the direction of flight. The OFM modulate their flight speed three‐fold over different patterns. They fly fastest when there is no pattern in the tunnel or the contrast elements are too narrow to resolve. When the spatial wavelength of the pattern is sufficiently wide to resolve, moths fly at a speed that tends to maintain a visual contrast frequency of 3.5 ± 3.2 Hz rather than a constant angular velocity, which varies from 57 to 611° s^?1. In addition, for the first time, it is also demonstrated that the width of a contrast pattern perpendicular to the flight direction modulates flight speed.     

Crossmodal visual input for odor tracking during fly flight

Flies generate robust and high-performance olfactory and visual behaviors. Adult fruit flies can distinguish small differences in odor concentration across antennae separated by less than 1 mm [1], and a single olfactory sensory neuron is sufficient for near-normal gradient tracking in larvae [2]. During flight a male housefly chasing a female executes a corrective turn within 40 ms after a course deviation by its target [3]. The challenges imposed by flying apparently benefit from the tight integration of unimodal sensory cues. Crossmodal interactions reduce the discrimination threshold for unimodal memory retrieval by enhancing stimulus salience [4], and dynamic crossmodal processing is required for odor search during free flight because animals fail to locate an odor source in the absence of rich visual feedback [5]. The visual requirements for odor localization are unknown. We tethered a hungry fly in a magnetic field, allowing it to yaw freely, presented odor plumes, and examined how visual cues influence odor tracking. We show that flies are unable to use a small-field object or landmark to assist plume tracking, whereas odor activates wide-field optomotor course control to enable accurate orientation toward an attractive food odor.     

Tuning Properties of MT and MSTd and Divisive Interactions for Eye-Movement Compensation

The primate brain intelligently processes visual information from the world as the eyes move constantly. The brain must take into account visual motion induced by eye movements, so that visual information about the outside world can be recovered. Certain neurons in the dorsal part of monkey medial superior temporal area (MSTd) play an important role in integrating information about eye movements and visual motion. When a monkey tracks a moving target with its eyes, these neurons respond to visual motion as well as to smooth pursuit eye movements. Furthermore, the responses of some MSTd neurons to the motion of objects in the world are very similar during pursuit and during fixation, even though the visual information on the retina is altered by the pursuit eye movement. We call these neurons compensatory pursuit neurons. In this study we develop a computational model of MSTd compensatory pursuit neurons based on physiological data from single unit studies. Our model MSTd neurons can simulate the velocity tuning of monkey MSTd neurons. The model MSTd neurons also show the pursuit compensation property. We find that pursuit compensation can be achieved by divisive interaction between signals coding eye movements and signals coding visual motion. The model generates two implications that can be tested in future experiments: (1) compensatory pursuit neurons in MSTd should have the same direction preference for pursuit and retinal visual motion; (2) there should be non-compensatory pursuit neurons that show opposite preferred directions of pursuit and retinal visual motion.     

Influence of prior and visual information on eye movements in amblyopic children

This study analyzed the characteristics of pursuit and assessed the influence of prior and visual information on eye velocity and saccades in amblyopic and control children, in comparison to adults. Eye movements of 41 children (21 amblyopes and 20 controls) were compared to eye movements of 55 adults (18 amblyopes and 37 controls). Participants were asked to pursue a target moving at a constant velocity. The target was either a ‘standard’ target, with a uniform color intensity, or a ‘noisy’ target, with blurry edges, to mimic the blurriness of an amblyopic eye. Analysis of pursuit patterns showed that the onset was delayed, and the gain was decreased in control children with a noisy target in comparison to amblyopic or control children with a standard target. Furthermore, a significant effect of prior and visual information on pursuit velocity and saccades was found across all participants. Moreover, the modulation of the effect of visual information on the pursuit velocity by group, that is amblyopes or controls with a standard target, and controls with a noisy target, was more limited in children. In other words, the effect of visual information was higher in control adults with a standard target compared to control children with the same target. However, in the case of a blurry target, either in control participants with a noisy target or in amblyopic participants with a standard target, the effect of visual information was larger in children.

     

Figure tracking by flies is supported by parallel visual streams

Visual figures may be distinguished based on elementary motion or higher-order non-Fourier features, and flies track both. The canonical elementary motion detector, a compact computation for Fourier motion direction and amplitude, can also encode higher-order signals provided elaborate preprocessing. However, the way in which a fly tracks a moving figure containing both elementary and higher-order signals has not been investigated. Using a novel white noise approach, we demonstrate that (1) the composite response to an object containing both elementary motion (EM) and uncorrelated higher-order figure motion (FM) reflects the linear superposition of each component; (2) the EM-driven component is velocity-dependent, whereas the FM component is driven by retinal position; (3) retinotopic variation in EM and FM responses are different from one another; (4) the FM subsystem superimposes saccadic turns upon smooth pursuit; and (5) the two systems in combination are necessary and sufficient to predict the full range of figure tracking behaviors, including those that generate no EM cues at all. This analysis requires an extension of the model that fly motion vision is based on simple elementary motion detectors and provides a novel method to characterize the subsystems responsible for the pursuit of visual figures.     

Three‐dimensional flight tracking shows how a visual target alters tsetse fly responses to human breath in a wind tunnel

Tsetse flies Glossina spp. (Diptera; Glossinidae) are blood‐feeding vectors of disease that are attracted to vertebrate hosts by odours and visual cues. Studies on how tsetse flies approach visual devices are of fundamental interest because they can help in the development of more efficient control tools. The responses of a forest tsetse fly species Glossina brevipalpis (Newstead) to human breath are tested in a wind tunnel in the presence or absence of a blue sphere as a visual target. The flight responses are video recorded with two motion‐sensitive cameras and characterized in three dimensions. Although flies make meandering upwind flights predominantly in the horizontal plane in the plume of breath alone, upwind flights are highly directed at the visual target presented in the plume of breath. Flies responding to the visual target fly from take‐off within stricter flight limits at lower ground speeds and with a significantly lower variance in flight trajectories in the horizontal plane. Once at the target, flies fly in loops principally in the horizontal plane within 40 cm of the blue sphere before descending in spirals beneath it. Successful field traps designed for G. brevipalpis take into account the strong horizontal component in local search behaviour by this species at objects. The results suggest that trapping devices should also take into account the propensity of G. brevipalpis to descend to the lower parts of visual targets.     

Visual edge orientation shapes free-flight behavior in Drosophila

Insects rely on visual cues to estimate and control their distance to approaching objects and their flight speed. Here we show that in free-flight, the motion cues generated by high-contrast vertical edges are crucial for these estimates. Within a visual environment dominated by high-contrast horizontal edges, flies fly unusually fast and barely avoid colliding with the walls of the enclosure. The disruption of flight behavior by horizontal edges provides insight into the structure of visually-mediated control algorithms.     

Estimating the speed of Drosophila locomotion using an automated behavior detection and analysis system

A fundamental phenotypic trait in Drosophila melanogaster is the speed of movement. Its quantification in response to environmental and experimental factors is highly useful for behavioral and neurological studies. Quantifying this behavioral characteristic in freely moving flies is difficult, and many current systems are limited to evaluating the speed of movement of one fly at a time or rely on expensive, time-consuming methods. Here, we present a novel signal processing method of quantifying the speed of multiple flies using a system with automatic behavior detection and analysis that we previously developed to quantify general activity. By evaluating the shape of the signal wave from recordings of a live and simulated single fly, a metric for speed of movement was found. The feasibility of using this metric to estimate the speed of movement in a population of flies was then confirmed by evaluating recordings taken from populations of flies maintained at two different temperatures. The results were consistent with those reported in the literature. This method provides an automated way of measuring speed of locomotion in a fly population, which will further quantify fly behavioral responses to the environment.     

Complex predictive eye pursuit in monkey: a model system for cerebellar studies of skilled movement

Smooth pursuit eye movements provide a good model system for cerebellar studies of complex motor control in monkeys. First, the pursuit system exhibits predictive control along complex trajectories and this control improves with training. Second, the flocculus/paraflocculus region of the cerebellum appears to generate this control. Lesions impair pursuit and neural activity patterns are closely related to eye motion during complex pursuit. Importantly, neural responses lead eye motion during predictive pursuit and lag eye motion during non-predictable target motions that require visual control. The idea that flocculus/paraflocculus predictive control is non-visual is also supported by a lack of correlation between neural activity and retinal image motion during pursuit. Third, biologically accurate neural network models of the flocculus/paraflocculus allow the exploration and testing of pursuit mechanisms. Our current model can generate predictive control without visual input in a manner that is compatible with the extensive experimental data available for this cerebellar system. Similar types of non-visual cerebellar control are likely to facilitate the wide range of other skilled movements that are observed.     

Walking deficits and centrophobism in an α‐synuclein fly model of Parkinson's disease

Parkinson's disease (PD) is a movement neurodegenerative disorder, characterized by bradykinesia, rigidity and tremor, constituting difficulties in walking and abnormal gait. Previous research shows that Drosophila expressing human α‐synuclein A30P (A30P) develop deficits in geotaxis climbing; however, geotaxis climbing is a different movement modality from walking. Whether A30P flies would exhibit abnormal walking in a horizontal plane, a measure more relevant to PD, is not known. In this study, we characterized A30P fly walking using a high‐speed camera and an automatic behavior tracking system. We found that old but not young A30P flies exhibited walking abnormalities, specifically decreased total moving distance, distance per movement, velocity, angular velocity and others, compared with old control flies. Those features match the definition of bradykinesia. Multivariate analysis further suggested a synergistic effect of aging and A30P, resulting in a distinct pattern of walking deficits, as seen in aged A30P flies. Psychiatric problems are common in PD patients with anxiety affecting 40–69% of patients. Central avoidance is one assessment of anxiety in various animal models. We found old but not young A30P flies exhibited increased centrophobism, suggesting possible elevated anxiety. Here, we report the first quantitative measures of walking qualities in a PD fly model and propose an alternative behavior paradigm for evaluating motor functions apart from climbing assay.     

Head-centred motion perception in the ageing visual system

Stationary objects appear to move in the opposite direction to a pursuit eye movement (Filehne illusion) and moving objects appear slower when pursued (Aubert-Fleischl phenomenon). Both illusions imply that extra-retinal, eye-velocity signals lead to lower estimates of speed than corresponding retinal motion signals. Intriguingly, the velocity (i.e. speed and direction) of the Filehne illusion depends on the age of the observer, especially for brief display durations (Wertheim and Bekkering, 1992). This suggests relative signal size changes as the visual system matures. To test the signal-size hypothesis, we compared the Filehne illusion and Aubert-Fleischl phenomenon in young and old observers using short and long display durations. The trends in the Filehne data were similar to those reported by Wertheim and Bekkering. However, we found no evidence for an effect of age or duration in the Aubert-Fleischl phenomenon. The differences between the two illusions could not be reconciled on the basis of actual eye movements made. The findings suggest a more complicated explanation of the combined influence of age and duration on head-centred motion perception than that described by the signal-size hypothesis.     

Two distinct visual motion mechanisms for smooth pursuit: evidence from individual differences

Smooth-pursuit eye velocity to a moving target is more accurate after an initial catch-up saccade than before, an enhancement that is poorly understood. We present an individual-differences-based method for identifying mechanisms underlying a physiological response and use it to test whether visual motion signals driving pursuit differ pre- and postsaccade. Correlating moment-to-moment measurements of pursuit over time with two psychophysical measures of speed estimation during fixation, we find two independent associations across individuals. Presaccadic pursuit acceleration is predicted by the precision of low-level (motion-energy-based) speed estimation, and postsaccadic pursuit precision is predicted by the precision of high-level (position-tracking) speed estimation. These results provide evidence that a low-level motion signal influences presaccadic acceleration and an independent high-level motion signal influences postsaccadic precision, thus presenting a plausible mechanism for postsaccadic enhancement of pursuit.     

Attention-like processes underlying optomotor performance in a Drosophila choice maze

The authors present a novel paradigm for studying visual responses in Drosophila. An eight-level choice maze was found to reliably segregate fly populations according to their responses to moving stripes displayed on a computer screen. Visual responsiveness was robust in wild-type flies, and performance depended on salience effects such as stimulus color and speed. Analysis of individual fly choices in the maze revealed that stereotypy, or choice persistence, contributed significantly to a strain's performance. On the basis of these observations, the authors bred wild-type flies for divergent visual phenotypes by selecting individual flies displaying extreme stereotypy. Selected flies alternated less often in the sequential choice maze than unselected flies, showing that stereotypy could evolve across generations. The authors found that selection for increased stereotypy impaired flies' responsiveness to competing stimuli in tests for attention-like behavior in the maze. Visual selective attention was further investigated by electrophysiology, and it was found that increased stereotypy also impaired responsiveness to competing stimuli at the level of brain activity. Combined results present a comprehensive approach to studying visual responses in Drosophila, and show that behavioral performance involves attention-like processes that are variable among individuals and thus sensitive to artificial selection.