The three-dimensional optomotor torque system ofDrosophila melanogaster

Summary The well known optomotor yaw torque response in flies is part of a 3-dimensional system. Optomotor responses around the longitudinal and transversal body axes (roll and pitch) with strinkingly similar properties to the optomotor yaw response are described here forDrosophila melanogaster. Stimulated by visual motion from a striped drum rotating around an axis aligned with the measuring axis, a fly responds with torque of the same polarity as that of the rotation of the pattern. In this stimulus situation the optomotor responses for yaw, pitch and roll torque have about the same amplitudes and dynamic properties (Fig. 2). Pronounced negative responses are measured with periodic gratings of low pattern wavelengths due to geometrical interference (Fig. 3). The responses depend upon the contrast frequency rather than the angular velocity of the pattern (Fig. 4). Like the optomotor yaw response, roll and pitch responses can be elicited by small field motion in most parts of the visual field; only for motion below and behind the fly roll and pitch responses have low sensitivity.The mutantoptomotor-blind ^H31 (omb ^H31) in which the giant neurones of the lobula plate are missing or severely reduced, is impaired in all 3 optomotor torque responses (Fig. 5) whereas other visual responses like the optomotor lift/thrust response and the landing response (elicited by horizontal front-to-back motion) are not affected (Heisenberg et al. 1978).We propose that the lobula plate giant neurons mediate optomotor torque responses and that the VS-cells in particular are involved in roll and pitch but not in lift/thrust control. This hypothesis accommodates various electrophysiological and anatomical observations about these neurons in large flies.Abbreviation EMD elementary movement detector     

Object detection in the fly during simulated translatory flight

Translatory movement of an animal in its environment induces optic flow that contains information about the three-dimensional layout of the surroundings: as a rule, images of objects that are closer to the animal move faster across the retina than those of more distant objects. Such relative motion cues are used by flies to detect objects in front of a structured background. We confronted flying flies, tethered to a torque meter, with front-to-back motion of patterns displayed on two CRT screens, thereby simulating translatory motion of the background as experienced by an animal during straight flight. The torque meter measured the instantaneous turning responses of the fly around its vertical body axis. During short time intervals, object motion was superimposed on background pattern motion. The average turning response towards such an object depends on both object and background velocity in a characteristic way: (1) in order to elicit significant responses object motion has to be faster than background motion; (2) background motion within a certain range of velocities improves object detection. These properties can be interpreted as adaptations to situations as they occur in natural free flight. We confirmed that the measured responses were mediated mainly by a control system specialized for the detection of objects rather than by the compensatory optomotor system responsible for course stabilization. Accepted: 20 March 1997     

Spectral sensitivity of the accessory optic system of the pigeon

When an animal is moving relative to its surroundings it can nevertheless stabilize the image on the retina, at least partially, by means of the large-field optomotor response. In the animal species investigated so far, this response has been found to be colour-blind as indicated by grey-matching tests, and to involve only photoreceptors sensitive in the long-wavelength region of the spectrum. Here we show that this rule also applies to pigeons, i.e. birds, a group not previously studied in this regard. Accepted: 4 February 1998     

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     

The pursuit response of the housefly and its interaction with the optomotor response

Summary Pursuit responses that are probably involved in chasing behavior can be evoked and quantitatively measured in male houseflies under conditions of tethered flight (Figs. 2, 3, 5). Pursuit responses of females are significantly different from those of males (Table 1).Characteristics of the pursuit response are compared with those of the optomotor response to show that they are mediated by different neural subsystems that are in parallel. A slow system mediates the optomotor response, while a much faster system mediates the pursuit response (Table 1).The interaction between the pursuit response and the optomotor response is one of switching. The optomotor stimulus, when presented alone, evokes the optomotor response. When the pursuit stimulus is superposed, the fly switches from the optomotor system to the pursuit system, and ignores the optomotor stimulus. When the pursuit stimulus is removed, the animal switches back to the optomotor system (Fig. 8).We wish to thank Dr. M.F. Land for his valuable suggestion for measuring the optomotor response. This work was supported by NEI grants EY 01140 and EY 00785.     

Reafferent control of optomotor yaw torque inDrosophila melanogaster

Summary In the flight simulator the optomotor response ofDrosophila melanogaster does not operate as a simple feedback loop. Reafferent and exafferent motion stimuli are processed differently. Under open-loop conditions responses to motion are weaker than under closed-loop conditions. It takes the fly less than 100 ms to distinguish reafferent from exafferent motion. In closed-loop conditions, flies constantly generate torque fluctuations leading to small-angle oscillations of the panorama. This reafferent motion stimulus facilitates the response to exafferent motion but does not itself elicit optomotor responses. Reafference control appears to be directionally selective: while a displacement of the patternm by as little as 0.1° against the expected direction leads to a fast syndirectional torque response, displacements in the expected direction have no comparable effect. Based on the behavior of the mutantrol sol, which under open-loop conditions is directionally motion-blind but in closed-loop conditions still performs optomotor balance, a model is proposed in which the fly's endogenous torque fluctuations are an essential part of the course control process. It is argued that the model may also account for wild type optomotor balance in the flight simulator.     

Neural correlates of the optomotor response in the fly

Summary Studies of the optomotor response, the tendency to turn in response to a moving pattern, have yielded some understanding of the motion detection capabilities of the fly. We present data from extracellular microelectrode recordings from the optic lobes of the housefly, Musca domestica and the blowflies Eucalliphora lilaea and Calliphora phaenicia. Directionally selective and directionally nonselective motion sensitive units were observed in the region between the medulla and the lobula of all three species. Employing similar stimulus conditions to those used in the optomotor reaction studies, it was found that the response of the directionally selective units exhibited most of the characteristics of the optomotor response torque measurements. It is concluded that these units code the information prerequisite to the optomotor response and hence, that much data processing is achieved in the first few synaptic layers of the insect visual nervous system.     

Flight-phase and visual-field related optomotor yaw responses in gregarious desert locusts during tethered flight

Tethered flying desert locusts, Schistocerca gregaria, generate yaw-torque in response to rotation of a radial grating located beneath them. By screening parts of the pattern, rotation of the unscreened grating turned out to induce a compensatory steering (by pattern motion within transversally oriented 90° wide sectors) as well as an upwind/downwind turning response (by pattern motion within the anterior ventral 90° wide sector). The strength and polarity of responses upon the unscreened grating results from a linear superposition of these two response components. The results are discussed with regard to a functional specialization of eye regions.In a typical experiment, 3 consecutive flight-phases, assumed to mirror start, long-range flight, and landing of a free-flying locust, were distinguished. They may result from a time dependent variation of the polarity and relative strength of upwind/downwind turning and compensatory steering responses. Starting and landing phases were under strong optomotor control and were dominated by the high-gain compensatory steering. In contrast, the phase of long-range flight was under weak optomotor control resulting from a low gain in both of the two response components. The biological significance of this variable strength of optomotor control on free flight orientation of swarming locusts is discussed.     

Desert ants Cataglyphis fortis use self-induced optic flow to measure distances travelled

While foraging, desert ants of the genus Cataglyphis use a vector navigation (route integration) system for homing. Any vector navigation system requires that the animal is able to evaluate the angles steered and the distances travelled. Here we investigate whether the ants acquire the latter information by monitoring self-induced optic flow. To answer this question, the animals were trained and tested within perspex channels in which patterns were presented underneath a transparent walking platform. The patterns could be moved at different velocities (up to > 0.5 the ant's walking speed) in the same or in the opposite direction relative to the direction in which the animal walked. Experimental manipulations of the optic flow influenced the ant's homing distances (Figs. 2 and 4). Distance estimation depends on the speed of self-induced image motion rather than on the contrast frequency, indicating that the motion sensitive mechanism involved is different from mechanisms mediating the optomotor response. Experiments in which the ants walked on a featureless floor, or in which they wore eye covers (Fig. 6), show that they are able also to use additional (probably kinesthetic) cues for assessing their travel distance. Hence, even though optic flow cues are not the only ones used by the ants, the experiments show that ants are obviously able to exploit such cues for estimation of travel distance.     

Sensitivity of the Goldfish Motion Detection System Revealed by Incoherent Random Dot Stimuli: Comparison of Behavioural and Neuronal Data

Background

Global motion detection is one of the most important abilities in the animal kingdom to navigate through a 3-dimensional environment. In the visual system of teleost fish direction-selective neurons in the pretectal area (APT) are most important for global motion detection. As in all other vertebrates these neurons are involved in the control of slow phase eye movements during gaze stabilization. In contrast to mammals cortical pathways that might influence motion detection abilities of the optokinetic system are missing in teleost fish.

Results

To test global motion detection in goldfish we first measured the coherence threshold of random dot patterns to elicit horizontal slow phase eye movements. In addition, the coherence threshold of the optomotor response was determined by the same random dot patterns. In a second approach the coherence threshold to elicit a direction selective response in neurons of the APT was assessed from a neurometric function. Behavioural thresholds and neuronal thresholds to elicit slow phase eye movements were very similar, and ranged between 10% and 20% coherence. In contrast to these low thresholds for the optokinetic reaction and APT neurons the optomotor response could only be elicited by random dot patterns with coherences above 40%.

Conclusion

Our findings suggest a high sensitivity for global motion in the goldfish optokinetic system. Comparison of neuronal and behavioural thresholds implies a nearly one-to-one transformation of visual neuron performance to the visuo-motor output. In addition, we assume that the optomotor response is not mediated by the optokinetic system, but instead by other motion detection systems with higher coherence thresholds.     

Neuronal representation of optic flow experienced by unilaterally blinded flies on their mean walking trajectories

Asymmetries in the optic flow on both eyes may indicate an unintended turn of an animal and evoke compensatory optomotor responses. On a straight path in an evenly structured environment, the optic flow on both eyes is balanced corresponding to a state of optomotor equilibrium. When one eye is occluded an optomotor equilibrium is expected to be reached on a curved path provided that the translatory optic flow component is cancelled by a superimposed rotation. This hypothesis is tested by analysing how the HSE cell, a constituent element of the fly's optomotor system, represents optic flow in behavioural situations. The optic flow as seen on the average trajectory of freely walking monocular flies is reconstructed. This optic flow is used as stimulus of the HSE cell in electrophysiological experiments and as input of a model of the fly's optomotor system. The responses of the HSE cell and of the model fluctuate around the resting potential. On average, they are much smaller than the responses evoked by optic flow experienced on a straight path. These results corroborate the hypothesis that the mean trajectory of monocular flies corresponds to a path of optomotor equilibrium. Accepted: 29 February 2000     

Direction-sensitive partitioning of the honeybee optomotor system

ABSTRACT. The horizontal motion-detecting system controlling optomotor head-turning behaviour in honeybees, Apis mellifera , was found to be partitioned into two separate subsystems. Each subsystem is direction-specific such that visual stimulation in the preferred direction elicited a high level of responses that correcly followed the movement, whereas stimulation in the non-preferred direction resulted in response levels comparable to or lower than those for blinded controls. The results indicate that medial eye regions are specialized for the detection of posterior-to-anterior movements and lateral regions are specialized for detecting anterior-to-posterior motion. A model suggesting possible neural correlates for this functional subdivision of the optomotor response is proposed.     

Integration of binocular optic flow in cervical neck motor neurons of the fly

Global visual motion elicits an optomotor response of the eye that stabilizes the visual input on the retina. Here, we analyzed the neck motor system of the blowfly to understand binocular integration of visual motion information underlying a head optomotor response. We identified and characterized two cervical nerve motor neurons (called CNMN6 and CNMN7) tuned precisely to an optic flow corresponding to pitch movements of the head. By means of double recordings and dye coupling, we determined that these neurons are connected ipsilaterally to two vertical system cells (VS2 and VS3), and contralaterally to one horizontal system cell (HSS). In addition, CNMN7 turned out to be connected to the ipsilateral CNMN6 and to its contralateral counterpart. To analyze a potential function of this circuit, we performed behavioral experiments and found that the optomotor pitch response of the fly head was only observable when both eyes were intact. Thus, this neural circuit performs two visuomotor transformations: first, by integrating binocular visual information it enhances the tuning to the optic flow resulting from pitch movements of the head, and second it could assure an even head declination by coordinating the activity of the CNMN7 neurons on both sides.     

用红外方法对蝇翅视动行为的探索

本文报告了利用红外装置对蝇翅视动行为实验研究的初步结果及其分析:1.在红外探测器探测到的信号中找到了一个能反映蝇翅拍动幅度的参数.2.双侧、单侧刺激域的宽度及刺激域的高度对视动反应发生几率在一定范围内正相关,当超过一阈值(即饱和阈值)后,即出现稳定的视动反应,它们的饱和阈值分别为60°,30°,40°刺激条纹的亮度生有类似情况.刺激条纹的运动速度在一定范围内对视动反应无影响.3.当刺激没有达到饱和时,蝇翅出现断续的典型的视动反应,即“0-1波动反应”.4.单侧条纹由前向后运动时,蝇翅出现典型反应,而条纹从后向前运动时,不出现典型的视动反应或反应很弱.双侧刺激时,条纹向前运动几乎不诱发反应;条纹向后运动诱发明显的蝇翅视动反应,且蝇翅平面的方向在拍动过程中发生变化.     

Response properties of visual interneurons to motion stimuli in the praying mantis,Tenodera aridifolia

Intracellular responses of motion-sensitive visual interneurons were recorded from the lobula complex of the mantis, Tenodera aridifolia. The interneurons were divided into four classes according to the response polarity, spatial tuning, and directional selectivity. Neurons of the first class had small, medium, or large receptive fields and showed a strong excitation in response to a small-field motion such as a small square moving in any direction (SF neurons). The second class neurons showed non-directionally selective responses: an excitation to a large-field motion of gratings in any direction (ND neurons). Most ND neurons had small or medium-size receptive fields. Neurons of the third class had large receptive fields and exhibited directionally selective responses: an excitation to a large-field motion of gratings in preferred direction and an inhibition to a motion in opposite, null direction (DS neurons). The last class neurons had small receptive fields and showed inhibitory responses to a moving square and gratings (I neurons). The functional roles of these neurons in prey recognition and optomotor response were discussed.     

OMR-Arena: Automated Measurement and Stimulation System to Determine Mouse Visual Thresholds Based on Optomotor Responses

Measurement of the optomotor response is a common way to determine thresholds of the visual system in animals. Particularly in mice, it is frequently used to characterize the visual performance of different genetically modified strains or to test the effect of various drugs on visual performance. Several methods have been developed to facilitate the presentation of stimuli using computer screens or projectors. Common methods are either based on the measurement of eye movement during optokinetic reflex behavior or rely on the measurement of head and/or body-movements during optomotor responses. Eye-movements can easily and objectively be quantified, but their measurement requires invasive fixation of the animals. Head movements can be observed in freely moving animals, but until now depended on the judgment of a human observer who reported the counted tracking movements of the animal during an experiment. In this study we present a novel measurement and stimulation system based on open source building plans and software. This system presents appropriate 360 stimuli while simultaneously video-tracking the animal''s head-movements without fixation. The on-line determined head gaze is used to adjust the stimulus to the head position, as well as to automatically calculate visual acuity. Exemplary, we show that automatically measured visual response curves of mice match the results obtained by a human observer very well. The spatial acuity thresholds yielded by the automatic analysis are also consistent with the human observer approach and with published results. Hence, OMR-arena provides an affordable, convenient and objective way to measure mouse visual performance.     

Spectral and Polarization Sensitivity of the Dipteran Visual System

Spectral and polarization sensitivity measurements were made at several levels (retina, first and third optic ganglion, cervical connective, behavior) of the dipteran visual nervous system. At all levels, it was possible to reveal contributions from the retinular cell subsystem cells 1 to 6 or the retinular cell subsystem cells 7 and 8 or both. Only retinular cells 1 to 6 were directly studied, and all possessed the same spectral sensitivity characterized by two approximately equal sensitivity peaks at 350 and 480 nm. All units of both the sustaining and on-off variety in the first optic ganglion exhibited the same spectral sensitivity as that of retinular cells 1 to 6. It was possible to demonstrate for motion detection and optomotor responses two different spectral sensitivities depending upon the spatial wavelength of the stimulus. For long spatial wavelengths, the spectral sensitivity agreed with retinular cells 1 to 6; however, the spectral sensitivity at short spatial wavelengths was characterized by a single peak at 465 nm reflecting contributions from the (7, 8) subsystem. Although the two subsystems exhibited different spectral sensitivities, the difference was small and no indication of color discrimination mechanisms was observed. Although all retinular cells 1 to 6 exhibited a preferred polarization plane, sustaining and on-off units did not. Likewise, motion detection and optomotor responses were insensitive to the polarization plane for long spatial wavelength stimuli; however, sensitivity to select polarization planes was observed for short spatial wavelengths.     

Polarization contrast and motion detection

Form and motion perception rely upon the visual system’s capacity to segment the visual scene based upon local differences in luminance or wavelength. It is not clear if polarization contrast is a sufficient basis for motion detection. Here we show that crayfish optomotor responses elicited by the motion of images derived from spatiotemporal variations in e-vector angles are comparable to contrast-elicited responses. Response magnitude increases with the difference in e-vector angles in adjacent segments of the scene and with the degree of polarization but the response is relatively insensitive to the absolute values of e-vector angles that compose the stimulus. The results indicate that polarization contrast can support visual motion detection.     

Zum Bewegungssehen des Mehlkäfers Tenebrio molitor

Summary The locomotory turns of the beetle Tenebrio molitor were recorded from free walking animals which were held in stationary position and orientation by means of a tread compensator. Striped patterns revolved around an animal elicit optomotor responses which undergo an inversion at smaller stripe widths. The position of the inversion point characterizes the resolving power of the motion detectors, and corresponds to a 6.5° average angle between the optical axes of interacting elements in the motion detecting device. This indirectly determined value is consistent with the anatomically measured 7° average angle between the axes of neighbouring ommatidia in the Tenebrio compound eye.     

Comparison between the movement detection systems underlying the optomotor and the landing response in the housefly

Flies evaluate movement within their visual field in order to control the course of flight and to elicit landing manoeuvres. Although the motor output of the two types of responses is quite different, both systems can be compared with respect to the underlying movement detection systems. For a quantitative comparison, both responses were measured during tethered flight under identical conditions. The stimulus was a sinusoidal periodic pattern of vertical stripes presented bilaterally in the fronto-lateral eye region of the fly. To release the landing response, the pattern was moved on either side from front to back. The latency of the response depends on the stimulus conditions and was measured by means of an infrared light-beam that was interrupted whenever the fly lifted its forelegs to assume a preprogrammed landing posture (Borst and Bahde 1986). As an optomotor stimulus the pattern moved on one side from front to back and on the other side in the opposite direction. The induced turning tendency was measured by a torque meter (Götz 1964). The response values which will be compared are the inverse latencies of the landing response and the amplitude of the yaw torque.

1. Optomotor course-control is more sensitive to pattern movement at small spatial wavelengths (10° and 20°) than the landing response (Fig. 1a and b). This suggests that elementary movement detectors (EMDs, Buchner 1976) with large detection base (the distance between interacting visual elements) contribute more strongly to the landing than to the optomotor system.
2. The optimum contrast frequencies of the different responses obtained at a comparatively high pattern contrast of about 0.6 was found to be between 1 and 10 Hz for the optomotor response, and around 20 Hz for the landing response (Fig. 2a and b). This discrepancy can be explained by the fact that the optomotor response was tested under stationary conditions (several seconds of stimulation) while for the landing response transient response characteristics of the movement detectors have to be taken into account (landing occurs under these conditions within less than 100 ms after onset of the movement stimulus). To test the landing system under more stationary conditions, the pattern contrast had to be reduced to low values. This led to latencies of several seconds. Then the optimum of the landing response is around 4 Hz. This is in the optimum range of the optomotor course-control response. The result suggests the same filter time constants for the movement detectors of both systems.
3. The dependence of both responses on the position and the size of the pattern was examined. The landing response has its optimum sensitivity more ventrally than the optomotor response (Fig. 3a and b). Both response amplitudes increase with the size of the pattern in a similar progression (Fig. 3c and d).

In first approximation, the present results are compatible with the assumption of a common set of movement detectors for both the optomotor course-control and the landing system. Movement detectors with different sampling bases and at different positions in the visual field seem to contribute with different gain to both responses. Accordingly, the control systems underlying both behaviors are likely to be independent already at the level of spatial integration of the detector output.