Visual receptive field properties of feature detecting neurons in the dragonfly

The dragonfly, (Aeshna, Anax) which feeds on small flying insects, requires a visual system capable of signaling the movements of airborne prey. A group of 8 descending feature detectors in the dragonfly are tuned exclusively to moving contrasting objects. These target-selective descending neurons project from the brain to the thoracic ganglia. Their activity drives steering movement of the wings.In this study, we recorded target-selective descending neuron activity intracellularly.To define their receptive fields, we recorded responses to the movement of black square targets projected onto a screen in front of the animal. Each neuron was identified by dye injection.Target-selective descending neurons exhibit several receptive field properties. Our results show that they are strongly directionally selective. Two TSDNs, exclusively tuned to small targets, have receptive fields restricted to visual midline. Others, which are not selective for target size, have asymmetric receptive fields centered laterally.We suggest that the behavioral function of these specialized feature detectors is to steer the dragonfly during prey-tracking so as to fix the position of the prey image on the retina. If the dragonfly maintains a constant visual bearing to its prey over time it will intercept its prey.Abbreviations TSDN target-selective descending neuron - DCMD descending contralateral movement detector - MDT median dorsal tract - DIT dorsal intermediate tract - VNC ventral nerve cord     

Elementary detectors for vertical movement in the visual system of Drosophila

Optomotor thrust responses of the fruitfly Drosophila melanogaster to moving gratings have been analysed in order to determine the arrangement of elementary movement detectors in the hexagonal array of the compound eye. These detectors enable the fly to perceive vertical movement. The results indicate that, under photopic stimulation of a lateral equatorial eye region, the movement specific response originates predominantly from two types of elementary movement detectors which connect neighbouring visual elements in the compound eye. One of the detectors is oriented vertically, the other detector deviates 60° towards the anterior-superior direction (Fig. 5b). The maximum of the thrust differences to antagonistic movement is obtained if the pattern is moving vertically or along a superior/anterior — inferior/posterior direction 30° displaced from the vertical (Fig. 3d,e, Fig. 6). Only one of the detectors coincides with one of the two detectors responsible for horizontal movement detection. This indicates that a third movement specific interaction in the compound eye of Drosophila has to be postulated. — The contrast dependence of the thrust response (Fig. 2) yields the acceptance angle of the receptors mediating the response. The result coincides with the acceptance angle found by analysis of the turning response of Drosophila (Heisenberg and Buchner, 1977). This value corresponds to the acceptance angle expected, on the basis of optical considerations, for the receptor system R 1–6. — The movement-specific neuronal network responsible for thrust control is not homogeneous throughout the visual field of Drosophila. Magnitude and preferred direction of the thrust response in the upper frontal part of the visual field seem to vary considerably in different flies (Fig. 6).     

The angular orientation of the movement detectors acting on the flight lift response in flies

The lift response of houseflies Musca domestica in fixed flight to periodic gratings movins in 12 different orientations has been measured. Two projectors were arranged symmetrically to the flies stimulating successively 18 circular patches of 50° (25°) diameter (9 for each eye) in their visual field. The shapes of the lift responses measured as a function of the orientation of the moving grating varied when different patches in the visual field were stimulated. A qualitative comparison of these response curves leads to the conclusion that the orientation of the movement detecting substrate acting on the flight lift response varies as a function of the stimulated area in the visual field. A straightforward correlation between the geometry of the ommatidial pattern and the orientation of the movement detecting substrate valid for all stimulated areas of the compound eyes does not seem very likely.     

Properties of individual movement detectors as derived from behavioural experiments on the visual system of the fly

The performance of the fly's movement detection system is analysed using the visually induced yaw torque generated during tethered flight as a behavioural indicator. In earlier studies usually large parts of the visual field were exposed to the movement stimuli; the fly's response, therefore, represented the spatially pooled output signals of a large number of local movement detectors. Here we examined the responses of individual movement detectors. The stimulus pattern was presented to the fly via small vertical slits, thus, nearly avoiding spatial integration of local movement information along the horizontal axis of the eye. The stimulus consisted of a vertically oriented sine-wave grating which was moved with a constant velocity either clockwise or counterclockwise. In agreement with the theory of movement detectors of the correlation type, the time-course of the detector signal is modulated with the spatial phase of the stimulus pattern. It can even assume negative values for some time during the response cycle and thus signal the wrong direction of motion. By spatially integrating the response over sufficiently large arrays of movement detectors these response modulations disappear. Finally, one obtains a signal of the movement detection system which is constant while the pattern moves in one direction and only changes its sign when the pattern reverses its direction of motion. Spatial integration thus represents a simple means to obtain a meaningful representations of motion information.     

Responses of visual interneurons in the fly optic lobe during stimulation by motion in depth

Summary A high-order wide-field neuron in the optic lobe of the fly,Phormia terraenovae (Calliphoridae), has been investigated by stimulation with simple or multiple black stripes on a white background moving sinusoidally towards and away from the head. The variation in spike frequency in correlation with the optical stimulation provides evidence that the unit detects angular velocity as well as more complex features of the stimulus. It responds preferentially to movement towards the head. Spike frequency turned out to be a two-valued function of relative angular velocity across the eye. A simple formula predicts the highly reliable responses to visual stimuli in different parts of the visual field.The author wants to thank Professor G. A. Horridge for his valuable support and clarifying discussions and to Dr. M. Srinivasan for his comments. The project has been supported by grants from the Swedish Council for Natural Science Research.     

Stochastic constancy,variability and adaptation of spike generation: Performance of a giant neuron in the visual system of the fly

The stochastic structure of the spike activity generated by a movement processing wide-field element in the visual system of the fly has been studied over the whole performance area of the neuron. The structure of this discharge is described in terms of an Adaptive Integrate-to-Threshold model for a wide variety of spatio-temporal stimuli as well as steady-state stimuli. In order to reproduce the experimental results it is shown that the source of randomness in the model (e.g. the threshold) behaves like a random variable which is distributed according to a two-state Markov renewal process. In the case of stationary discharges generated by moving sinewave patterns the shape of the interspike interval distribution (which, in the Integrate-to-Threshold model, reflects the shape of the threshold distribution) changes continuously from a two-state distribution at low firing rates to a one-state distribution at high firing rates. In dynamic conditions of the discharge, generated by temporal dynamic stimuli, the experimental results show that the shape of the (demodulated) interval distribution of the discharge is determined by the highest instantaneous firing rate with an adaptation time constant of a few seconds. The physioligical origin of this intriguing behaviour remains — up till now — out of the picture.     

Control of flight by means of lateral visual stimuli in gregarious desert locusts, Schistocerca gregaria

Abstract. Tethered flying locusts were stimulated either by a periodic grating or by a spotted 'swarm-simulating' pattern moving horizontally, parallel to their longitudinal body axis within their lateral visual fields. The direction of movement of the pattern was changed periodically from progressive to regressive and vice versa.
Both kinds of patterns induced a correlated modulation of yaw-torque and thrust. The two measured flight parameters were modulated independently of each other. Each parameter either increased with progressive and decreased with regressive pattern motion or vice versa. The characteristic curves of thrust and yaw-torque responses - i.e. response amplitude versus contrast frequency resp. angular velocity – measured upon stimulation with the periodic grating between 2 and 70 Hz were at a maximum at 10 Hz and decreased at higher and lower contrast frequencies. The shape of the curves was nearly identical. The characteristic curves measured upon stimulation with the 'swarm-simulating' pattern between 60 and 1500^o s^-1 could be simulated using the spatial wavelength content of the pattern and the characteristic curves for periodic gratings.
Therefore, we suggest that the speed and direction of locusts' flight result from the optomotor effectiveness of the pattern image formed by the neighbouring individuals under free flight. The measured responses would thus contribute to the common orientation of groups of locusts within a migrating swarm and thus to swarm cohesion.     

Connections between wide-field monocular and binocular movement detectors in the brain of a hawk moth

Summary Recordings were made in the brain of Sphinx ligustri of pairs of directionally selective movement detectors, and the spike trains analysed with a computer for possible synaptic connections between two classes of movement detector. (1) Neurones with large binocular fields which arise in the medial protocerebrum and project to the medulla or lobula of one optic lobe, or to the ventral nerve cord. (2) Movement detectors which project from the lobula complex of one optic lobe to the opposite medial protocerebrum. The majority of the second group had back-to-front preferred directions over the ipsilateral eye, and of these many were weakly sensitive to stimuli to the opposite eye. The ipsilateral receptive field covered most of the eye.Optic lobe output cells with the appropriate preferred direction provide a powerful excitatory input to the binocular movement detectors centrifugal to the medulla. Each centrifugal movement detector probably receives excitatory inputs from no more than two optic lobe output cells with back-to-front preferred direction. The same set of optic lobe output neurones probably feeds several cells projecting to the medulla and lobula of both optic lobes, and, possibly, to the ventral nerve cord.Evidence was obtained that the optic lobe output cells themselves receive few excitatory inputs, and that therefore the receptive fields of their input cells are large.Two moving stimuli were presented in different areas of the receptive field. Movement through the null direction in one area inhibited the response to movement in the preferred direction in another area. This suppression was stronger in optic lobe output cells with front-to-back preferred direction than in units with back-to-front preferred direction. Thus the optic lobe output cells, or wide-field units feeding them, receive inhibitory inputs from wide-field units with the opposite preferred direction.Similar tests in which moving stimuli were presented to both eyes gave results indicating that the binocular centrifugal movement detectors may receive inhibitory inputs from movement detectors with back-to-front preferred direction. The possible functional significance of these inhibitory inputs is discussed.I am very greatful to F. A. Miles for helpful discussion and criticism. Financial support came from the U. K. Science Research Council.     

Identification of optic lobe neurons of locusts by video films

The response characteristic of visual interneurons of the brain was studied in Locusta migratoria and Schistocerca gregaria. Alternating light and dark, moving dots, bars and striped patterns were used for stimulation (Fig. 3). These stimuli were recorded with a video system and replayed on TV-screens during the experiment to allow fast testing of the sensitivity of a neuron to different stimuli during the limited time of intracellular recording. Data were stored and analysed by computer. The neurons were anatomically identified by intracellular injection of Lucifer yellow. Neutral (non-visual) and several classes of spiking interneurons of the medulla and lobula sensitive to visual stimuli could be distinguished by anatomical and physiological characteristics (Figs. 1, 2). The visual cells respond either to light-on, or to light-off, flicker, moving small dots, bars or striped patterns (Figs. 2–6). One class is directionally sensitive to pattern movement either from back to front or into the reverse direction (horizontal cells; Figs. 7, 8) and may therefore be involved in optomotor flight control.Dedicated to Prof. Dr. Dietrich Burkhardt on the occasion of his 60th birthday     

Experimental analysis of the prey catching behavior ofHydromantes italicus Dunn (Amphibia,Plethodontidae)

Summary 1. The Italian bolitoglossine salamanderHydromantes italicus shows a periodic cave life. In spring and in the fall it leaves the caves after which it lives under stones, in leaves and crevices. Inside the limestone caves,H. i. can be found both in the zone of dim light near the entrance and in total darkness. 2. Corresponding to these two environments there are two guidance systems of the prey catching behavior: one visual and one olfactory. 3. The visually guided prey catching behavior is determined by the stimulus parameters: velocity, size, contrast, and ambient illumination. Continuously moving objects are effective within a velocity range of 0.05 to 6 cm/s with an optimum at 1.25 cm/s (Fig. 2). Stimuli moving stepwise elicit fixation of the prey and complete approach more frequently than continuously moving stimuli. The prey size which elicits prey catching ranges from 0.5 to 10 mm² with an optimum size between 2.5–5.0 mm² (Fig. 3). The prey catching behavior is hardly impaired by a decrease in ambient illumination down to 0.03 cd/m². Beyond 0.03 cd/m², the prey catching activity decreases sharply, but there are still responses at an illumination level of 0.003 cd/m² (Fig. 4). 4.H.i. also responds to stationary non-smelling visual stimuli following stimulation by smell or movement.H.i. is able to detect prey by smell only both in total darkness and in the light (Fig. 5 A). In the light, the prey catching behavior with regard to smelling objects is inhibited by the absence of visual contrast (Fig. 5B).I would like to thank Prof. Dr. R. Altevogt, University of Münster (Germany) for his generous help and constant encouragement. Furthermore, I want to express my gratitude to Prof. Dr. D.B. Wake, University of California, Berkeley (USA), Prof. Dr. P. Mancino, University of Pisa (Italy), and Prof. Dr. J.-P. Ewert, University (GH) of Kassel (Germany) for stimulating discussions and helpful comments.     

华虻小叶神经元运动敏感性的研究

用电生理细胞内记录的方法记录了１０个以上小叶神经元对闪光、运动光斑及运动光栅刺激的电生理反应特点,结果表明：（１）小叶神经元对闪光刺激具有特征性反应,细胞对给光和撤光刺激都会表现出不同程度的去极化和超极化,反应的波形不随闪光时间的改变而改变,两次去极化之间的时间间隔与闪光刺激的时间长度成线性关系;（２）小叶神经元对运动光斑的运动速度非常敏感,而对光斑的运动方向的改变却不敏感,尽管有的细胞存在一个能使反应的变化更快的优势方向,但并没有明显的运动方向选择性;（３）小叶神经元对运动光栅的响应频率受光栅的空间频率和运动速度的双重调制,与光栅的运动方向无关。     

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.     

Figure-ground discrimination by relative movement in the visual system of the fly

The visual system of the fly performs various computations on photoreceptor outputs. The detection and measurement of movement is based on simple nonlinear multiplication-like interactions between adjacent pairs and groups of photoreceptors. The position of a small contrasted object against a uniform background is measured, at least in part, by (formally) 1-input nonlinear flicker detectors. A fly can also detect and discriminate a figure that moves relative to a ground texture. This computation of relative movement relies on a more complex algorithm, one which detects discontinuities in the movement field. The experiments described in this paper indicate that the outputs of neighbouring movement detectors interact in a multiplication-like fashion and then in turn inhibit locally the flicker detectors. The following main characteristic properties (partly a direct consequence of the algorithm's structure) have been established experimentally: a) Coherent motion of figure and ground inhibit the position detectors whereas incoherent motion fails to produce inhibition near the edges of the moving figure (provided the textures of figure and ground are similar). b) The movement detectors underlying this particular computation are direction-insensitive at input frequencies (at the photoreceptor level) above 2.3 Hz. They become increasingly direction-sensitive for lower input frequencies. c) At higher input frequencies the fly cannot discriminate an object against a texture oscillating at the same frequency and amplitude at 0° and 180° phase, whereas 90° or 270° phase shift between figure and ground oscillations yields maximum discrimination. d) Under conditions of coherent movement, strong spatial incoherence is detected by the same mechanism. The algorithm underlying the relative movement computation is further discussed as an example of a coherence measuring process, operating on the outputs of an array of movement detectors. Possible neural correlates are also mentioned.     

Influence of adaptation to horizontal body position on pointing errors and visual estimation of a target position in humans

The central program of a targeted movement includes a component intended for to compensate for the weight of the arm; this is why the accuracy of pointing to a memorized position of the visual target in darkness depends on orientation of the moving limb in relation to the vertical axis. Transition from the vertical to the horizontal body position is accompanied by a shift of the final hand position along the body axis towards the head. We studied how pointing errors and visual localization of the target are modified due to adaptation to the horizontal body position; targeted movements to a real target were repeatedly performed during the adaptation period. Three types of experiments were performed: a basic experiment, and two different experiments with adaptation realized under somewhat dissimilar conditions. In the course of the first adaptation experiment, subjects received no visual information on the hand’s position in space, and targeted movements of the arm to a luminous target could be corrected using proprioceptive information only. With such a paradigm, the accuracy of pointing to memorized visual targets showed no adaptation-related changes. In the second adaptation experiment, subjects were allowed to continuously view a marker (a light-emitting diode taped to the fingertip). After such adaptation practice, the accuracy of pointing movements to memorized targets increased: both constant and variational errors, as well as both components of constant error (i.e.,X andY errors) significantly dropped. Testing the accuracy of visual localization of the targets by visual/verbal adjustment, performed after this adaptation experiment, showed that the pattern of errors did not change compared with that in the basic experiment. Therefore, we can conclude that sensorimotor adaptation to the horizontal position develops much more successfully when the subject obtains visual information about the working point position; such adaptation is not related to modifications in the system of visual localization of the target.     

Solid perception mechanism by a shading pattern: Spatial frequency components in a corrugated wave pattern

Primary visual coding can be characterized by the receptive field (RF) properties of single neurons. Subject of this paper is our search for a global,second coding step beyond the RF-concept that links related features in a visual scene. In recent models of visual coding, oscillatory activities have been proposed to constitute such linking signals. We tested the neurophysiological relevance of this hypothesis for the visual system. Single and multiple spikes as well as local field potentials were recorded simultaneously from several locations in the primary visual cortex (A17 and A18) using 7 or 19 individually advanceable fibermicroelectrodes (250 or 330 m apart).Stimulusevoked (SE)-resonances of 35–85 Hz were found in these three types of signals throughout the visual cortex when the primary coding channels were activated by their specific stimuli. Stimulus position, orientation, movement direction and velocity, ocularity and stationary flicker caused specific SE-resonances.Coherent SE-resonances were found at distant cortical positions when at least one of the primary coding properties was similar. Coherence was found1) within a vertical cortex column,2) between neighbouring hypercolumns, and3) between two different cortical areas. We assume that the coherence of SE-resonances is mediated by recurrent excitatory intra- and inter-areal connections via phase locking between assemblies that represent the linking features of the actual visual scene. Visually related activities are, thus, transiently labelled by a temporal code that signalizes their momentary association.     

Deoxyglucose mapping of nervous activity induced inDrosophila brain by visual movement

Summary Autoradiographs of the brains of the visual mutantsouter rhabdomeres absent ^JK84 (ora),small optic lobes ^KS58 (KS58) andno object fixation E ^B12 (B12) have been obtained by the deoxyglucose method. The patterns of metabolic activity in the optic lobes of the visually stimulated mutants is compared with that of similarly stimulated wildtype (WT) flies which was described in Part I of this work (Buchner et al. 1984b).In the mutantKS58 the optomotor following response to movement is nearly normal despite a 40–45% reduction of volume in the visual neuropils, medulla and lobula complex. InB12 flies the volume of these neuropils and the optomotor response are reduced. In autoradiographs of both mutants the pattern of neuronal activity induced by stimulation with moving gratings does not differ substantially from that in the WT. It suggests that only neurons irrelevant to movement detection are affected by the mutation. However, in the lobula plate of someKS58 flies and in the second chiasma of allB12 flies, the pattern of metabolic activity differs from that observed in WT flies. Up to now no causal relation has been found between the modifications described in behaviour or anatomy and those observed in the labelling of these mutants.In the ommatidia ofora flies the outer rhabdomeres are lacking while the central photoreceptors appear to be normal. Stimulus-specific labelling is absent in the visual neuropil of these mutants stimulated with movement or flicker. This result underlines the importance of the outer rhabdomeres for visual tasks, especially for movement detection.Abbreviations DG deoxyglucose - KS58 small optic lobes^KS58 - B12 no object fixation E^B12 - JK84 ora outer rhabdomeres absent ^JK84 - WT wildtype     

Orientation sensitivity of the visual movement detection system activating the landing response of the blowflies,Calliphora, and Phaenicia: A behavioural investigation

The orientation sensitivity of the visual movement detection system relative to the axes of the eye was investigated for the landing response by changing the direction of movement of a periodic striped pattern (unidirectional movement) and a two-stripe pattern consiting of two stripes moving apart (bidirectional movement). In the momocular, equatorial regions of the eye progressive motion proves to be most effective, whereas in the frontal (equational), binocular region descendive motion is most effective in eliciting the landing response, probably caused by binocular interactions. A strong enhancement of the response is induced by stimulation in the binocular region of the two eyes. The orientation of elementary movement detectors relative to the axes of the ommatidial array is discussed. The findings are summarized in a functional model of the landing response.     

Dynamic response properties of movement detectors: Theoretical analysis and electrophysiological investigation in the visual system of the fly

Dynamic aspects of the computation of visual motion information are analysed both theoretically and experimentally. The theoretical analysis is based on the type of movement detector which has been proposed to be realized in the visual system of insects (e.g. Hassenstein and Reichardt 1956; Reichardt 1957, 1961; Buchner 1984), but also of man (e.g. van Doorn and Koenderink 1982a, b; van Santen and Sperling 1984; Wilson 1985). The output of both a single movement detector and a one-dimensional array of detectors is formulated mathematically as a function of time. The resulting movement detector theory can be applied to a much wider range of moving stimuli than has been possible on the basis of previous formulations of the detector output. These stimuli comprise one-dimensional smooth detector input functions, i.e. functions which can be expanded into a time-dependent convergent Taylor series for any value of the spatial coordinate.The movement detector response can be represented by a power series. Each term of this series consists of one exclusively time-dependent component and of another component that depends, in addition, on the properties of the pattern. Even the exclusively time-dependent components of the movement detector output are not solely determined by the stimulus velocity. They rather depend in a non-linear way on the weighted sum of the instantaneous velocity and all its higher order time derivatives. The latter point represents another reason — not discussed so far in the literature — that movement detectors of the type analysed here do not represent pure velocity sensors.The significance of this movement detector theory is established for the visual system of the fly. This is done by comparing the spatially integrated movement detector response with the functional properties of the directionally-selective motion-sensitive. Horizontal Cells of the third visual ganglion of the fly's brain.These integrate local motion information over large parts of the visual field. The time course of the spatially integrated movement detector response is about proportional to the velocity of the stimulus pattern only as long as the pattern velocity and its time derivatives are sufficiently small. For large velocities and velocity changes of the stimulus pattern characteristic deviations of the response profiles from being proportional to pattern velocity are predicted on the basis of the detector theory developed here. These deviations are clearly reflected in the response of the wide-field Horizontal Cells, thus, providing very specific evidence that the movement detector theory developed here can be applied to motion detection in the fly. The characteristic dynamic features of the theoretically predicted and the experimentally determined cellular responses are exploited to estimate the time constant of the movement detector filter.