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.     

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.     

The effect of strenuous exercise and beta-adrenergic blockade on the visual performance of juvenile rainbow trout,Oncorhynchus mykiss

It is hypothesised that the visual performance of rainbow trout, Oncorhynchus mykiss, will be impaired by strenuous exercise as a result of metabolic stress (blood lactacidosis) that activates the Root effect and limits the oxygen-carrying capacity of blood flowing to the eye. The ability to resolve high contrast objects on a moving background, as a measure of visual performance, was quantified pre- and post-exercise using the optomotor response. Strenuous exercise induced a metabolic acidosis (8.0 mmol l(-1) blood lactate) and a significant red cell swelling response but no change in the optomotor response threshold (120 min of arc) was observed. Beta-adrenergic blockade (propranolol) abolished post-exercise red cell swelling but optomotor response thresholds were still maintained at 120 min of arc despite a significant blood lactate load (7.8 mmol l(-1)). The choroid rete mirabile of the trout is extremely well developed (rete area:eye area = 0.39) and may maintain visual performance by ensuring a relatively direct supply of oxygen to the central regions of the avascular retina. Exercised fish under beta-adrenergic blockade exhibited an enhanced optomotor response at 240-300 min of arc. Assuming that these responses reflect "tunnel vision", adrenergic regulation of red cell function may preserve a high ocular PO(2) gradient that satisfies the oxygen demand of peripheral retinal cells.     

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.     

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.     

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     

The orientation of flies towards visual patterns: On the search for the underlying functional interactions

The average optomotor response of insects to a given visual stimulus (measured in open-loop conditions) can be decomposed into a direction sensitive and a direction insensitive component. This decomposition is conceptual and always possible. The direction sensitive optomotor response represents the “classical” optomotor reflex, already studied in previous investigations; the direction insensitive optomotor response is strictly connected to the orientation and tracking behaviour (see the work of Reichardt and coworkers). Thus a characterization of the direction insensitive response is useful in clarifying the nervous mechanisms underlying the orientation behaviour. For this reason we study in this paper the direction insensitive optomotor (torque) response of fixed flying fliesMusca domestica. Periodic gratings, either moving or flickering, represent our main stimulus, since the dependence of the fly response on the spatial wavelength can unravel the presence and properties of the underlying lateral interactions. In this connection an extension of the Volterra series formalism to multi-input (nervous) networks is first outlined in order to connect our (behavioural) input-output data with the interactive structure of the network. A number of results concerning, for instance, the response of such networks to flickered and moving gratings are derived; they are not restricted to our behavioural results and may be relevant in other fields of neuroscience. These theoretical considerations provide the logical framework of our experimental investigation. The main results are:

1. the direction insensitive optomotor response depends on the spatial frequency of a moving grating, implying the existence of (nonlinear) lateral interactions,
2. its wavelength dependence changes with age, unlike the direction sensitive response,
3. both the direction insensitive response and the (closed loop) orientation behaviour are present only in the lower part of the eye; on the other hand the direction sensitive response is present in every part of the two eyes.

Furthermore the attraction towards a flickered periodic grating shows, as theoretically expected, a wavelength-dependence similar to that of the direction insensitive response, again present only in the lower part of the eye. The interactions which affect the orientation response are selective with respect to the spatiotemporal mapping of the pattern onto the receptor array. It is conjectured that these interactions are the basic mechanisms underlying spontaneous pattern discrimination in flies. Their possible organization is further discussed in terms of our formalism. Moreover our data suggest that two specific nervous circuitries correspond to our conceptual decomposition of the optomotor response.     

Evidence for one-way movement detection in the visual system of Drosophila

Optomotor control of course and altitude in the fruitfly, Drosophila melanogaster, requires dense networks of elementary movement detectors (EMD's) which cover most if not all of the visual field. The predominant types of EMD's in these networks represent interactions between neighbouring visual elements along the three main directions of the hexagonal array in the compound eye. — Course control in the walking fly is achieved mainly by pairs of equivalent EMD's which occupy 2 o'clock and 4 o'clock positions with respect to the right eye (Buchner, 1976). Comparison of the turning response and the torque response in the present account confirms the particular properties of this network, and proves the presumed bidirectional sensitivity of its EMD's for the course control responses of legs and wings in the corresponding modes of locomotion. — Altitude control during flight is achieved by a less homogeneous network of EMD's which modifies lift and thrust simultaneously by the appropriate control of the wing beat amplitudes. The predominant types of EMD's in the lateral eye regions occupy 12 o'clock and 2 o'clock positions with respect to the right eye (Buchner et al., 1978). The present evaluation of the optomotor responses of thrust and wing beat confirms the preferred orientation of these EMD's and discloses a pecularity of their internal structure. The movement detectors of this network lack the bidirectional sensitivity of the EMD's in the course control system. At least the fronto-lateral network of the altitude control system seems to consist mainly of pairs of equivalent unidirectional EMD's. The detectors in 12 o'clock position increase wing beat in response to movement of the visual surroundings from inferior to superior. The opposite effect is produced by the detectors in 2 o'clock position which respond to movement from anterior-superior to posterior-inferior. These properties qualify unidirectional EMD's as the functional units of the optomotor control system in the fruitfly. Pairs of unidirectional antagonists would be sufficient to establish the bidirectional sensitivity found in the movement detectors of the course control system.     

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.     

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.     

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.     

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.     

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.     

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     

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.     

Correlates of choroid rete development with the metabolic potential of various tropical reef fish and the effect of strenuous exercise on visual performance

It is hypothesised that the transport of oxygen to the retinal cells of fish with Root effect haemoglobins (Hb) is impaired by strenuous exercise due to a proton load that drastically reduces arterial haemoglobin-oxygen affinity. Routinely active reef fishes have enhanced oxygen transport and anaerobic (i.e. blood lactate loading) potentials relative to inactive species. Surprisingly, the development of the choroid rete mirabile (employed as an oxygen concentrating apparatus in the eye) is directly correlated with post-exercise lactate loads rather than with the magnitude of the Root effect and suggests that an increased development is adaptive for fish with high anaerobic potentials. The hypothesis that visual performance is reduced by strenuous exercise was tested in Lutjanus carponotatus using the optomotor response. Moderate blood lactate loads (2 mmol l⁻¹ blood lactate) and red cell swelling responses were induced by exercise, but the optomotor response threshold (180 min of arc) was maintained. A moderate metabolic disturbance does not therefore appear to be a liability for the visual performance of a tropical fish in possession of Root effect haemoglobins.     

On the organization of memory in the optomotor system of the crab pachygrapsus crassipes

Memory responses of the optomotor system to rotations of various stripe patterns were studied. The separate elements of the visual background are individually remembered in terms of the parts of the eye on which their images fell. A visual illusion resulting from this property is described. All parts of the retina have an equal capacity to contribute to memory. The memory response results from the summation of contributions from individual elements rather than the maintenance of a fixation upon any particular feature of the situation. Both the separation between background elements for angles from 6° up to 60° and the number of elements present affect the size of the memory evoked response.     

On the organization of memeory in the optomotor system of the crab Pachygrapsus crassipes.

Memory responses of the optomotor system to rotations of various stripe patterns were studied. The separate elements of the visual background are individually remembered in terms of the parts of the eye on which their images fell. A visual illusion resulting from this property is described. All parts of the retina have an equal capacity to contribute to memory. The memory response results from the summation of contributions from individual elements rather than the maintenance of a fixation upon any particular feature of the situation. Both the separation between background elements for angles from 6 degrees up to 60 degrees and the number of elements present affect the size of the memory evoked response.     

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.     

Forward genetic analysis of visual behavior in zebrafish

The visual system converts the distribution and wavelengths of photons entering the eye into patterns of neuronal activity, which then drive motor and endocrine behavioral responses. The gene products important for visual processing by a living and behaving vertebrate animal have not been identified in an unbiased fashion. Likewise, the genes that affect development of the nervous system to shape visual function later in life are largely unknown. Here we have set out to close this gap in our understanding by using a forward genetic approach in zebrafish. Moving stimuli evoke two innate reflexes in zebrafish larvae, the optomotor and the optokinetic response, providing two rapid and quantitative tests to assess visual function in wild-type (WT) and mutant animals. These behavioral assays were used in a high-throughput screen, encompassing over half a million fish. In almost 2,000 F2 families mutagenized with ethylnitrosourea, we discovered 53 recessive mutations in 41 genes. These new mutations have generated a broad spectrum of phenotypes, which vary in specificity and severity, but can be placed into only a handful of classes. Developmental phenotypes include complete absence or abnormal morphogenesis of photoreceptors, and deficits in ganglion cell differentiation or axon targeting. Other mutations evidently leave neuronal circuits intact, but disrupt phototransduction, light adaptation, or behavior-specific responses. Almost all of the mutants are morphologically indistinguishable from WT, and many survive to adulthood. Genetic linkage mapping and initial molecular analyses show that our approach was effective in identifying genes with functions specific to the visual system. This collection of zebrafish behavioral mutants provides a novel resource for the study of normal vision and its genetic disorders.