How the two eyes add together: monocular properties of the visually guided orientation behaviour of flies

In this account fixation and the torque response to a transient moving stripe of flying femaleMusca domestica with monocular sight was tested. This was made by either covering one eye of the fly with opaque paint or by placing a screen in front of one side of the fly's visual field. A stripe was moved with constant speed once around the fly clockwise and, after a pause, counterclockwise. The torque response of the fly was measured during the motion of the stripe and shortly beforehand. The results demonstrated that the monocular torque response to progressive (from front to back) motion and regressive (from back to front) motion essentially do not differ from the binocular response, except for the region of bionocular overlap. The beginning of the response of a fly with monocular vision to progressive motion is 11 ° (on average) before the direction of flight (0°), which means that the maximal functional binocular overlap of femaleMusca domestica is stretched at least 15° to each side (3.1). In addition, the shape of the monocular torque response to a progressively moving stripe was determined (see Figs. 5Ia and 5IIb). In other experiments similar to the ones described above, a screen was placed on one side of the fly's visual field or then on the other, (instead of covering one eye) and the torque response to the moving stripe was measured. Using this method, a delay response of 90 ms was measured. We suggest that this is the delay of the direction-sensitive component of the torque response, and therefore an additional argument for the existence of two components for the optomotor torque response. Flies with a covered eye or with a screen placed in front of one side of the visual field were able to fixate a single narrow long black stripe. This, however, was possible only when an additional offset signal was added, in order to give the stripe a constant velocity component. As a result there was a shift of the fixation towards the unobscured eye. The shift was small for the monocular flies, and it was larger (13° on average) when the screen was on one side of the fly. A new type of laser torquethrust transducer was developed and is described.     

蜜蜂视叶和脑中的方向选择水平运动检测

在蜜蜂被刺激眼的同侧视叶内记录方向选择前进和后退水平运动灵敏的细胞反应。水平前进运动灵敏细胞对同侧前进运动的反应为很强的兴奋和去极化,以及去极化伴随有锋电位发放,同侧的后退运动引起抑制和超极化。在仅刺激对侧眼时,发放的频率不依赖于运动。水平后奶退运动灵敏的细胞对同侧水平后退运动反应出很强的兴奋和去极化,其去极化上伴随有锋电位发放,锋电位达不到零电位而且在其终点没有回射,同侧的前进运动几乎没有反应。     

Optomotor responses of the fly Musca domestica to transient stimuli of edges and stripes

The fly's optomotor response to transient stimuli was studied under open loop conditions. The stimuli used were moving edges and stripes. A comparison of the fly's responses to these stimuli bends to the result that progressive moving patterns (from front to back with respect to the fly) elicit stronger responses than regressive moving ones (from back to front). Edges followed by darkness elicit a stronger response than those followed by light. A narrow, bright or dark stripe and a single edge evoke a similar response, whereas a broad stripe elicitis a stronger response than a single edge.     

The interaction between visual edge fixation and skototaxis in the mealworm beetle Tenebrio molitor

Summary (1) It has been shown in earlier experiments that during the visually guided orientation response of the mealworm beetle,Tenebrio molitor, edge fixation and skototaxis interact. Under certain stimulus conditions these two effects act against each other and relative movement between the retina and the surroundings shifts the balance in favour of edge fixation. In this paper, three further parameters are described which change the contribution of the two mechanisms to the turning tendency of the animals. (2) When the centre of a broad black stripe lies on one side and one of the edges on the other side of the animal (Fig. 1B, C) then motion of an edge from front to back (progressive movement) more effectively increases the relative weight of edge fixation than do regressive movements (motion of an edge from back to front). (3) In the same situation temporal modulation of the overall illumination weakens skototaxis, dimming more than brightening (Fig. 2 A). From this it was predicted — and confirmed — that the dependence on the direction of motion will be reversed if both the centre and the edge closest to the midline of a broad black stripe lie on the same side of the animal (Fig. 2 B). (4) Animals with one eye blinded can fixate an edge (Fig. 3). Furthermore, edge fixation is mediated mainly by the ventral part of the eyes and skototaxis by the dorsal (Fig. 5). (5) The possible significance of the results for the animal's natural behaviour and for the underlying neural circuitry is discussed.     

Is there a motion-independent position computation of an object in the visual system of the housefly?

A single vertical stripe (long or short) was moved clockwise, with constant speed, around a tethered femaleMusca domestica fly. The yaw torque response of the fly was analyzed as a function of the position of the object. After an interval of 8 s the stripe was moved counterclockwise and a similar analysis of the torque was made. This procedure was repeated a few times and averaged to each direction separately and for all the flies tested. The results suggested that: a) There are at least two mechanisms for computing the optomotor response in the lower part of the fly's eye, one performing a position-dependent velocity computation and the other depending on the position but not on the direction of motion of an object. b) These two components are parametrized over the position on the lower part of the eye. The results also show that: c) There is a significant difference in the response between the upper and the lower part of the eye. The position-dependent component cannot be detected in the upper part of the eye. In addition: d) Two different control mechanisms are proposed, one responding to progressive (from front to back) and one to regressive (from back to front) movement of objects.     

Visuomotor Response to Object Expansion in Free-Flying Bumble Bees

The flight control systems of flying insects enable many kinds of sophisticated maneuvers, including avoidance of midair collisions. Visuomotor response to an approaching object, received as image expansion on insects’ retina, is a complex event in a dynamic environment where both animals and objects are moving. There are intensive free flight studies on the landing response in which insects receive image expansion by their own movement. However, few studies have been conducted regarding how freely flying insects respond to approaching objects. Here, using common laboratory insects for behavioral research, the bumblebee Bombus ignitus, we examined their visual response to an approaching object in the free-flying condition. While the insect was slowly flying in a free-flight arena, an expanding stripe was projected laterally from one side of the arena with a high-speed digital mirror device projector. Rather than turning away reported before, the bumble bees performed complex flight maneuvers. We synchronized flight trajectories, orientations and wing stroke frequencies with projection parameters of temporal resolution in 0.5 ms, and analyzed the instantaneous relationship between visual input and behavioral output. In their complex behavioral responses, we identified the following two visuomotor behaviors: increasing stroke frequency when the bumble bees confront the stripe expansion, and turning towards (not away) the stripe expansion when it is located laterally to the bee. Our results suggested that the response to object expansion is not a simple and reflexive escape but includes object fixation, presumably for subsequent behavioral choice.     

Fast and slow flight torque responses in flies and their possible role in visual orientation behaviour

The flight torque responses of tethered flying houseflies to motion and presentation or removal of a vertical dark stripe on a bright background were recorded in real time. Motion with constant speed of 100° s^-1 from front to back elicits a strong fast response following the diraction of the stimulus motion. Motion from back to front elicits a weaker response. Instantaneous presentation and removal of a stationary stripe elicit weak, slow response. Apparent motion from front to back and from back to front elicit weak responses with a fast, directionally selective, transient peak followed by a slow response component oriented towards the stripes position. The fast transient peak response is not elicited if the animals were stimulated before with real movement of the stripe. The results are discussed and an earlier proposed model for free flight tracking and fixation is extended.     

Motion sensitive interneurons in the optomotor system of the fly

The functional properties of the three horizontal cells (north horizontal cell, HSN; equatorial horizontal cell, HSE; south horizontal cell, HSS) in the lobula plate of the blowflyCalliphora erythrocephala were investigated electrophysiologically. 1. The receptive fields of the HSN, HSE, and HSS cover the dorsal, equatorial and ventral part of the ipsilateral visual field, respectively. In all three cells, the sensitivity to visual stimulation is highest in the frontal visual field and decreases laterally. The receptive fields and spatial sensitivity distributions of the horizontal cells are directly determined by the position and extension of their dendritic fields in the lobula plate and the dendritic density distributions within these fields. 2. The horizontal cells respond mainly to progressive (front to back) motion and are inhibited by motion in the reverse direction, the preferred and null direction being antiparallel. The amplitudes of motion induced excitatory and inhibitory responses decline like a cosine function with increasing deviation of the direction of motion from the preferred direction. Stimulation with motion in directions perpendicular to the preferred direction is ineffective. 3. The preferred directions of the horizontal cells show characteristic gradual orientation changes in different parts of the receptive fields: they are horizontally oriented only in the equatorial region and increasingly tilted vertically towards the dorsofrontal and ventrofrontal margins of the visual field. These orientation changes can be correlated with equivalent changes in the local orientation of the lattice of ommatidial axes in the pertinent compound eye. 4. The response amplitudes of the horizontal cells under stimulation with a moving periodic grating depend strongly on the contrast frequency of the stimulus. Maximal responses were found at contrast frequencies of 2–5 Hz. 5. The spatial integration properties of the horizontal cells (studied in the HSE) are highly nonlinear. Under stimulation with extended moving patterns, their response amplitudes are nearly independent of the size of the stimuli. It is demonstrated that this response behaviour does not result from postsynaptic saturation in the dendrites of the cells. The results indicate that the horizontal system is essentially involved in the neural control of optomotor torque responses performed by the fly in order to minimize unvoluntary deviations from a straight flight course.     

Detection of object motion by a fly neuron during simulated flight

Object detection on the basis of relative motion was investigated in the fly at the neuronal level. A representative of the figure detection cells (FD-cells), the FD1b-cell, was characterized with respect to its responses to optic flow which simulated the presence of an object during translatory flight. The figure detection cells reside in the fly's third visual neuropil and are believed to play a central role in mediating object-directed turning behaviour. The dynamical response properties as well as the mean response amplitudes of the FD1b-cell depend on the temporal frequency of object motion and on the presence or absence of background motion. The responses of the FD1b-cell to object motion during simulated translatory flight were compared to behavioural responses of the fly as obtained with identical stimuli in a previous study. The behavioural responses could only partly be explained on the basis of the FD1b-cell's responses. Further processing between the third visual neuropil and the final motor output has to be assumed which involves (1) facilitation of the object-induced responses during translatory background motion at moderate temporal frequencies, and (2) inhibition of the object-induced turning responses during translatory background motion at high temporal frequencies. Accepted: 9 October 1999     

Processing of figure and background motion in the visual system of the fly

The visual system of the fly is able to extract different types of global retinal motion patterns as may be induced on the eyes during different flight maneuvers and to use this information to control visual orientation. The mechanisms underlying these tasks were analyzed by a combination of quantitative behavioral experiments on tethered flying flies (Musca domestica) and model simulations using different conditions of oscillatory large-field motion and relative motion of different segments of the stimulus pattern. Only torque responses about the vertical axis of the animal were determined. The stimulus patterns consisted of random dot textures (Julesz patterns) which could be moved either horizontally or vertically. Horizontal rotatory large-field motion leads to compensatory optomotor turning responses, which under natural conditions would tend to stabilize the retinal image. The response amplitude depends on the oscillation frequency: It is much larger at low oscillation frequencies than at high ones. When an object and its background move relative to each other, the object may, in principle, be discriminated and then induce turning responses of the fly towards the object. However, whether the object is distinguished by the fly depends not only on the phase relationship between object and background motion but also on the oscillation frequency. At all phase relations tested, the object is detected only at high oscillation frequencies. For the patterns used here, the turning responses are only affected by motion along the horizontal axis of the eye. No influences caused by vertical motion could be detected. The experimental data can be explained best by assuming two parallel control systems with different temporal and spatial integration properties: TheLF-system which is most sensitive to coherent rotatory large-field motion and mediates compensatory optomotor responses mainly at low oscillation frequencies. In contrast, theSF-system is tuned to small-field and relative motion and thus specialized to discriminate a moving object from its background; it mediates turning responses towards objects mainly at high oscillation frequencies. The principal organization of the neural networks underlying these control systems could be derived from the characteristic features of the responses to the different stimulus conditions. The input to the model circuits responsible for the characteristic sensitivity of the SF-system to small-field and relative motion is provided by retinotopic arrays of local movement detectors. The movement detectors are integrated by a large-field element, the output cell of the network. The synapses between the detectors and the output cells have nonlinear transmission characteristics. Another type of large-field elements (pool cells) which respond to motion in front of both eyes and have characteristic direction selectivities are assumed to interact with the local movement detector channels by inhibitory synapses of the shunting type, before the movement detectors are integrated by the output cells. The properties of the LF-system can be accounted for by similar model circuits which, however, differ with respect to the transmission characteristic of the synapses between the movement detectors and the output cell; moreover, their pool cells are only monocular. This type of network, however, is not necessary to account for the functional properties of the LF-system. Instead, intrinsic properties of single neurons may be sufficient. Computer simulations of the postulated mechanisms of the SF-and LF-system reveal that these can account for the specific features of the behavioral responses under quite different conditions of coherent large-field motion and relative motion of different pattern segments.     

Distinct Acute Zones for Visual Stimuli in Different Visual Tasks in Drosophila

The fruit fly Drosophila melanogaster has a sophisticated visual system and exhibits complex visual behaviors. Visual responses, vision processing and higher cognitive processes in Drosophila have been studied extensively. However, little is known about whether the retinal location of visual stimuli can affect fruit fly performance in various visual tasks. We tested the response of wild-type Berlin flies to visual stimuli at several vertical locations. Three paradigms were used in our study: visual operant conditioning, visual object fixation and optomotor response. We observed an acute zone for visual feature memorization in the upper visual field when visual patterns were presented with a black background. However, when a white background was used, the acute zone was in the lower visual field. Similar to visual feature memorization, the best locations for visual object fixation and optomotor response to a single moving stripe were in the lower visual field with a white background and the upper visual field with a black background. The preferred location for the optomotor response to moving gratings was around the equator of the visual field. Our results suggest that different visual processing pathways are involved in different visual tasks and that there is a certain degree of overlap between the pathways for visual feature memorization, visual object fixation and optomotor response.     

The role of background movement in goldfish vision

In experiments described in the literature objects presented to restrained goldfish failed to induce eye movements like fixation and/or tracking. We show here that eye movements can be induced only if the background (visual surround) is not stationary relative to the fish but moving. We investigated the influence of background motion on eye movements in the range of angular velocities of 5–20° s⁻¹. The response to presentation of an object is a transient shift in mean horizontal eye position which lasts for some 10 s. If an object is presented in front of the fish the eyes move in a direction such that it is seen more or less symmetrically by both eyes. If it is presented at ±70° from the fish's long axis the eye on the side of the object moves in the direction that the object falls more centrally on its retina. During these object induced eye responses the typical optokinetic nystagmus of amplitude of some 5° with alternating fast and slow phases is maintained, and the eye velocity during the slow phase is not modified by presentation of the object. Presenting an object in front of stationary or moving backgrounds leads to transient suppression of respiration which shows habituation to repeated object presentations. Accepted: 14 April 2000     

Motion detection in the presence and absence of background motion in anAnolis lizard

Anolis lizards respond to a moving object viewed in the periphery of their visual field by turning their eye to fixate the object with their central fovea. This paper describes the relative effectiveness of different patterns of motion of a small black lure in eliciting these eye movements and the way motion of a backdrop of vegetation affects the response. The stimulus was positioned 45 degrees from the animal's line of gaze and oscillated in the vertical axis at different frequencies between 0.5 and 10 Hz. At each frequency, the amplitude of the oscillation was increased until the lizard flicked its eye towards the stimulus. The minimum amplitude needed for response (0.22 degrees of visual angle) was independent of frequency and waveform. The probability of any response occurring was, however, lower at higher frequencies (7 and 10 Hz) and a 1.5 Hz square wave evoked the greatest proportion of responses. Sinusoidal oscillation of a background of vegetation at 1.6 Hz during or before motion of the stimulus lure reduced the probability of an eye flick but did not raise the minimum amplitude needed for a response. The suppressive effect was greatest when the lure was oscillated at frequencies close to that of the background. It is concluded that Anolis, which rely upon motion to detect objects in the periphery of the visual field, filter out irrelevant motion such as that of windblown vegetation by responding preferentially to particular patterns of motion and short term habituation to commonly present patterns of motion.     

A behavioural test of the sensitivity of a nocturnal mosquito, Anopheles gambiae, to dim white, red and infra-red light

Abstract. A behavioural test was used to determine the light sensitivity of the nocturnal mosquito Anopheles gambiae Giles s.s. to low intensities of 'white' light (tungsten filament), 'red' light (white light filtered by a darkroom safelight filter) and 'infra-red' light) of two types (white light filtered by a λ>700 nm filter, and light-emitting diodes with λ>900 nm). Mosquitoes were placed in a 20 cm diameter flight-tunnel and their 'optomotor' response to a pattern of stripes moving across their visual field (at 14.5 cm s^-1) was recorded with infra-red-sensitive video. In free-flight, with ample light, the mosquitoes controlled their flight speed and direction in relation to the stripe movement, so that the stripes always appeared to move across their visual field from front to back. They did this by flying either with the moving stripes fast enough to overtake them (19.5 ± 0.7 cm s^-1), or against them more slowly (10.3 ± 0.7 cm s^-1)- The net ground speed of the mosquitoes was thus c. 4–5 cm s^-1. This response was significant down to 10^-5 W m^-2 in 'white' light, and 10^-3 W m^-2 in 'red' light. At light intensities below threshold and in infra-red light, however, they appeared to fly at random with respect to the stripe movement. The assumption commonly made, that mosquitoes do not 'see' in red light, may thus have to be revised.     

Is the landing response of the housefly (Musca) driven by motion of a flow field?

The landing response of tethered flying housefliesMusca domestica elicited by motion of periodic gratings is analysed. The field of view of the compound eyes of a fly can be subdivided into a region of binocular overlap and a monocular region. In the monocular region the landing response is elicited by motion from front to back and suppressed by motion from back to front. The sensitivity to front to back motion in monocular flies (one eye covered with black paint) has a maximum at an angle 60°–80° laterally from the direction of flight in the equatorial plane. The maximum of the landing response to front to back motion as a function of the contrast frequencyw/ is observed at around 8 Hz. In the region of binocular overlap of monocular flies the landing response can be elicited by back to front motion around the equatorial plane if a laterally positioned pattern is simulataneously moved from front to back. 40° above the equatorial plane in the binocular region the landing response in binocular flies is elicited by upward motion, 40° below the equatorial plane in the binocular region it is elicited by downward motion. The results are interpreted as an adaptation of the visual system of the fly to the perception of a flow field having its pole in the direction of flight.     

Visual position stabilization in the hummingbird hawk moth, Macroglossum stellatarum L. I. Behavioural analysis

Optomotor responses of freely flying hawk moths, Macroglossum stellatarum, were characterized while the animals were hovering in front of and feeding on a dummy flower. Compensatory translational and rotational movements of the hawk moth were elicited by vertical grating patterns moving horizontally, mimicking imposed rotational and translational displacements of the animal in the horizontal plane. Oscillatory translational and rotational pattern motion leads to compensatory responses that peak in the frequency range between 2 Hz and 4 Hz. The control systems mediating the translational and rotational components of the optomotor response do not seem to influence each other. The system mediating translational responses is more sensitive in the fronto-lateral part of the visual field than in the lateral part; the opposite is true for the rotational system. The sensitivity of the translational system does not change along the vertical, whereas the rotational system is much more sensitive to motion in the dorsal than in the ventral part of the visual field. These sensitivity gradients may reflect an adaptation to the specific requirements of position stabilization in front of flowers during feeding. Accepted: 13 August 1997     

Integration of auditory and visual information about objects in superior temporal sulcus

Two categories of objects in the environment-animals and man-made manipulable objects (tools)-are easily recognized by either their auditory or visual features. Although these features differ across modalities, the brain integrates them into a coherent percept. In three separate fMRI experiments, posterior superior temporal sulcus and middle temporal gyrus (pSTS/MTG) fulfilled objective criteria for an integration site. pSTS/MTG showed signal increases in response to either auditory or visual stimuli and responded more to auditory or visual objects than to meaningless (but complex) control stimuli. pSTS/MTG showed an enhanced response when auditory and visual object features were presented together, relative to presentation in a single modality. Finally, pSTS/MTG responded more to object identification than to other components of the behavioral task. We suggest that pSTS/MTG is specialized for integrating different types of information both within modalities (e.g., visual form, visual motion) and across modalities (auditory and visual).     

Acoustic facilitation of object movement detection during self-motion

In humans, as well as most animal species, perception of object motion is critical to successful interaction with the surrounding environment. Yet, as the observer also moves, the retinal projections of the various motion components add to each other and extracting accurate object motion becomes computationally challenging. Recent psychophysical studies have demonstrated that observers use a flow-parsing mechanism to estimate and subtract self-motion from the optic flow field. We investigated whether concurrent acoustic cues for motion can facilitate visual flow parsing, thereby enhancing the detection of moving objects during simulated self-motion. Participants identified an object (the target) that moved either forward or backward within a visual scene containing nine identical textured objects simulating forward observer translation. We found that spatially co-localized, directionally congruent, moving auditory stimuli enhanced object motion detection. Interestingly, subjects who performed poorly on the visual-only task benefited more from the addition of moving auditory stimuli. When auditory stimuli were not co-localized to the visual target, improvements in detection rates were weak. Taken together, these results suggest that parsing object motion from self-motion-induced optic flow can operate on multisensory object representations.     

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.