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.     

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     

The activity of pleurodorsal muscles during flight and at rest in the moth Manduca sexta (L.)

In the moth Manduca sexta, the paired mesothoracic flight steering muscle II PD2m takes part in the generation of the flight rhythm and is spontaneously active in the non-flying animal. This spontaneous activity is modulated by optomotor stimuli and directionally selective. The directional response characteristics are analyzed. Another spontaneously active steering muscle pair, the III PD2c, is situated in the metathorax. The activities of this pair and of a third muscle pair, the III PD3 are also influenced by visual stimulation.The responses of all 6 muscles to optomotor stimuli which simulate the flight situations yaw, roll, thrust and lift are analyzed. Each situation elicits a unique pattern of activation/deactivation within this set of muscles. The activity pattern in non-flying animals allows the prediction of flight steering mechanisms such as changes of wing area in flight turns and provides a useful basis for the analysis of visuo-motor pathways.     

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.     

Pheromone-modulated optomotor response in male gypsy moths,Lymantria dispar L.: Directionally selective visual interneurons in the ventral nerve cord

In response female pheromone the male gypsy moth flies a zigzagging path upwind to locate the source of odor. He determines wind direction visually. To learn more about the mechanism underlying this behavior, we studied descending interneurons with dye-filled micro-electrodes. We studied the interneuronal responses to combinations of pheromone and visual stimuli.

神经毒素ECMA对家鸽视网膜神经节单元反应特性的影响

从家鸽视差表层总共记录了１０１个视网膜神经节单元,并定量分析研究ＥＣＭＡ损伤对其反应特性的影响,在对照组中,神经节单元都没有自发放电,而需要视觉刺激才能引起反应,对闪光刺激的反应,分别为ＯＮ—ＯＦＦ,ＯＮ,ＯＦＦ三种,其反应均是瞬变的,而且也都对在感受野内运动的小条纹起反应。４２个单元中有１４个是方向选择性单元。其它的则为运动敏感单元。方向选择性单元的无效方向不是均等分布的,其中有８个单元的无效是从前向后的,但没有发现其无效方向是从后向前的单元。与对照组相比,经ＥＣＭＡ损伤后的实验组中只记录到ＯＮ－ＯＦＦ反应和ＯＮ反应单元,未能找到单独的ＯＦＦ反应单元。神经节单元的ＯＮ反应部分为持续成分。所有的单元对运动条纹刺激都失掉了方向选择性,这些现象的机理可能是由于ＥＣＭＡ去除了胆碱能无足细胞所致。     

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.     

On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly

A new class of large-field tangential neurones (Figure Detection (FD-) cells) has been found and analysed in the lobula plate, the posterior part of the third visual ganglion, of the fly by combined extra-and intracellular recording as well as Lucifer Yellow injection. The FD-cells are likely to play a prominent role in figure-ground discrimination. Together with the Horizontal Cells, the output elements of the neuronal network underlying the optomotor course control reaction, they seem to be appropriate to account for the characteristic yaw torque response to relative motion. The FD-cells might thus compensate for the deficits of the Horizontal Cells with respect to figureground discrimination (see Egelhaaf, 1985a).The FD-cells are directionally selective for either front-to-back (FD 1, FD 4) or back-to-front motion (FD 2, FD 3). Their excitatory receptive fields cover part of (FD 1, FD 2, FD 3) or the entire horizontal extent (FD 4) of the visual field of one eye. Their most important common property in the context of figureground discrimination is that they are more sensitive to relatively small objects than to spatially extended patterns. Their response to a small figure is much reduced by simultaneous large-field motion in front of the ipsi-as well as the contralateral eye. This large-field inhibition is either directionally selective or bidirectional, depending on the FD-cell under consideration. The main dendritic arborization of all FD-cells resides in the lobula plate. Their axonal projections lie in either the ipsi-or contralateral posterior optic foci and, thus, in the same area as the terminals of the Horizontal Cells. The FD-cells are, therefore, appropriate candidates for output elements of the optic lobes involved in figure-ground discrimination.     

Visual afferences to flight steering muscles controlling optomotor responses of the fly

Summary In tethered flying house-flies (Musca domestica) visually induced turning reactions were monitored under open-loop conditions simultaneously with the spike activity of four types of steering muscles (M.b1, M.b2, M.I1, M.III1). Specific behavioral response components are attributed to the activity of particular muscles. Compensatory optomotor turning reactions to large-field image displacements mainly occur when the stimulus pattern oscillates at low frequencies. In contrast, turning responses towards objects are preferentially induced by motion of relatively small stimuli at high oscillation frequencies. The different steering muscles seem to be functionally specialized in that they contribute to the control of these behavioral responses in different ways. The muscles I1, III1 and b2 are preferentially active during small-field motion at high oscillation frequencies. They are much less active during small-field motion at low oscillation frequencies and large-field motion at all oscillation frequencies which were tested. M.b2 is most extreme in this respect. These steering muscles thus mediate mainly turns towards objects. In contrast, M.b1 responds best during large-field motion at low oscillation frequencies and, thus, is appropriate to control compensatory optomotor responses. However, the activity of this muscle is also strongly modulated during small-field motion at high oscillation frequencies and, therefore, may be involved also in the control of turns towards objects. These functional specializations of the different steering muscles in mediating different behavioral response components are related to the properties of two parallel visual pathways that are selectively tuned to large-field and small-field motion, respectively.Abbreviations FD (cell) figure detection (cell) - HS (cell) horizontal (cell)     

The Optomotor Response in Weak-electric Mormyrid Fish: Can they See?

The present study has explored the optomotor response in two species of mormyrid fish, Gnathonemus petersii and Brienomyrus niger. Both species tended to follow a black and white striped stimulus pattern under illumination levels of 6, 12, and 60 lx. The optomotor response ceased to occur under 540 lx. The behavioral data support earlier histological findings implicating the mormyrid retina in dim light vision.     

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.     

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.     

The responses of peripheral and central mechanosensory lateral line units of weakly electric fish to moving objects

Mechanosensory lateral line afferents of weakly electric fish (Eigenmannia) responded to an object which moved parallel to the long axis of the fish with phases of increased spike activity separated by phases of below spontaneous activity. Responses increased with object speed but finally may show saturation. At increasingly greater distances the responses decayed as a power function of distance. For different object velocities the exponents (mean±SD) describing this response falloff were -0.71±0.4 (20 cm/s object velocity) and-1.9±1.25 (10 cm/s). Opposite directions of object movement may cause an inversion of the main features of the response histograms. In terms of peak spike rate or total number of spikes elicited, however, primary lateral line afferents were not directionally sensitive.Central (midbrain) lateral line units of weakly electric fish (Apteronotus) showed a jittery response if an object moved by. In midbrain mechanosensory lateral line, ampullary, and tuberous units the response to a rostral-tocaudal object movement may be different from that elicited by a caudal-to-rostral object motion. Central units of Apteronotus may receive input from two or more sensory modalities. Units may be lateral line-tuberous or lateral line-ampullary. Multimodal lateral line units were OR units, i.e., the units were reliably driven by a unimodal stimulus of either modality. The receptive fields of central units demonstrate a weak somatotopic organization of lateral line input: anterior body areas project to rostral midbrain, posterior body areas project to caudal midbrain.Abbreviation EOD electric organ discharge     

Columnar cells necessary for motion responses of wide-field visual interneurons in <Emphasis Type="Italic">Drosophila</Emphasis>

Wide-field motion-sensitive neurons in the lobula plate (lobula plate tangential cells, LPTCs) of the fly have been studied for decades. However, it has never been conclusively shown which cells constitute their major presynaptic elements. LPTCs are supposed to be rendered directionally selective by integrating excitatory as well as inhibitory input from many local motion detectors. Based on their stratification in the different layers of the lobula plate, the columnar cells T4 and T5 are likely candidates to provide some of this input. To study their role in motion detection, we performed whole-cell recordings from LPTCs in Drosophila with T4 and T5 cells blocked using two different genetically encoded tools. In these flies, motion responses were abolished, while flicker responses largely remained. We thus demonstrate that T4 and T5 cells indeed represent those columnar cells that provide directionally selective motion information to LPTCs. Contrary to previous assumptions, flicker responses seem to be largely mediated by a third, independent pathway. This work thus represents a further step towards elucidating the complete motion detection circuitry of the fly.     

Are the large monopolar cells of the insect lamina on the optomotor pathway?

Evidence is presented here from experiments on the visual system of the fly that questions participation of the large monopolar cells (LMCs) in the optomotor response.

The responses of central octavolateralis cells to moving sources

Mechanosensory lateral line units recorded from the medulla (medial octavolateralis nucleus) and midbrain (torus semicircularis) of the bottom dwelling catfish Ancistrus sp. responded to water movements caused by an object that passed the fish laterally. In terms of peak spike rate or total number of spikes elicited responses increased with object speed and sometimes showed saturation (Figs. 7, 14). At sequentially greater distances the responses of most medullary lateral line units decayed with object distance (Fig. 11). Units tuned to a certain object speed or distance were not found. The signed directionality index of most lateral line units was between –50 and +50, i.e. these units were not or only slightly sensitive to the direction of object motion (Figs. 10, 17). However, some units were highly directionally sensitive in that the main features of the response histograms and/or peak spike rates clearly depended on the direction of object movement (e.g. Fig. 9C, D and Fig. 16). Midbrain lateral line units of Ancistrus may receive input from more than one sensory modality. All bimodal lateral line units were OR units, i.e., the units were reliably driven by a unimodal stimulus of either modality. Units which receive bimodal input may show an extended speed range (e.g. Fig. 18).Abbreviations MON medial octavolateralis nucleus - MSR mean spike rate - PSR peak spike rate - p-p peak-to-peak - SDI signed directionality index     

A search for color encoding in the responses of a class of fly interneurons

Summary Extracellular recordings were obtained from single units in the lobula region of the optic lobe of the blowfly Calliphora phaenicia and housefly Musca domestica. These units responded selectively to the direction of movement of objects in the visual field. Previously it was suggested that these units are part of the neural system that controls flying behavior. The responses of these units were examined with monochromatic light flashes over four log units of intensity. No opponent cells were found. The spectral sensitivity was determined directly and found to be similar for all units studied. Responses patterns were investigated with test flashes of equal physiological brightness. It was concluded that color is not encoded by this class of interneurons. It is suggested that the optomotor response is determined by the activities of retinula cells 1–6.This research was supported by the National Institutes of Health, USPHS Grant NB 03627.     

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.     

The role of retinula cell types in fixation behaviour of walkingDrosophila melanogaster

Summary Fixation behaviour of free walking wild typeDrosophila and various retinal mutants was tested in a circular arena. Optomotor response was also measured as a test of the function of R1-6.ora andsev,ora do not fixate a narrow stripe (10° or 20°, Fig. 1) but are able to orient towards broad stripes (110° or 180°, Fig. 1). The behaviour ofsev is not different from wild type. Fixation behaviour ofw rdgB is similar toora (Figs. 5, 6). The mutantora has a maximum optomotor response at low contrast frequencies (Fig. 2), but the threshold for this response is at least one log unit higher than in wild type orsev (Fig. 8). The light intensity threshold at 550 nm of fixation to a broad stripe (110°) is 1–2 log units higher inora than in wildtype, and 4 log units higher insev,ora and the structural brain mutantVam (Fig. 7).The conclusions are that retinula cells R1-6 mediate fixation to a narrow stripe at high and low ambient light intensities, and to a broad stripe at low ambient light levels. R8, possibly in conjunction with R1-6, contributes to orientation towards broad stripes at high light intensities. This hypothesis is supported by evidence that blue-adapted white-eyed flies are able to orient towards a broad stripe at high blue light intensities (Figs. 9 and 12). Blue adaptation totally eliminates the optomotor response (Figs. 10, 11) and so the optomotor response observed inora at low contrast frequencies (Figs. 2 and 8) is most likely due to the small remnants of the rhabdomeres of R1-6 that remain.Abbreviations PDA prolonged depolarising afterpotential - ERG electroretinogram     

Directional selectivity and frequency tuning of midbrain cells in the oyster toadfish, Opsanus tau

Single-unit recordings were made from areas in the midbrain (torus semicircularis) of the oyster toadfish. We evaluated frequency tuning and directional responses using whole-body oscillation to simulate auditory stimulation by particle motion along axes in the horizontal and mid-sagittal planes. We also tested for bimodality in responses to auditory and hydrodynamic stimuli. One recording location in each animal was marked by a neurobiotin injection to confirm the recording site. Recordings were made in nucleus centralis, nucleus ventrolateralis, and the deep cell layer. Most units were frequency-selective with best frequencies between 50 and 141 Hz. Suppression of activity was apparent in 10% of the cells. Bimodality was common, including inhibition and suppression of background activity by auditory or hydrodynamic stimulation. The majority of the cells were directionally selective with directional response patterns that were sharpened compared with those of primary saccular afferents. The best directional axes were arrayed widely in spherical space, covering most azimuths and elevations. This representation is adequate for the computation of the motional axis of an auditory stimulus for sound source localization.Abbreviations BF best frequency - DCL deep cell layer - DON descending octaval nucleus - DRP directional response pattern - FFT fast Fourier transform - LL lateral lemniscus - NC nucleus centralis - NVL nucleus ventrolateralis - PVC periventricular cells - R coefficient of synchronization - TS torus semicircularis - Z Rayleigh statistic