Disentangling of Local and Wide-Field Motion Adaptation.

Motion adaptation has been attributed in flying insects a pivotal functional role in spatial vision based on optic flow. Ongoing motion enhances in the visual pathway the representation of spatial discontinuities, which manifest themselves as velocity discontinuities in the retinal optic flow pattern during translational locomotion. There is evidence for different spatial scales of motion adaptation at the different visual processing stages. Motion adaptation is supposed to take place, on the one hand, on a retinotopic basis at the level of local motion detecting neurons and, on the other hand, at the level of wide-field neurons pooling the output of many of these local motion detectors. So far, local and wide-field adaptation could not be analyzed separately, since conventional motion stimuli jointly affect both adaptive processes. Therefore, we designed a novel stimulus paradigm based on two types of motion stimuli that had the same overall strength but differed in that one led to local motion adaptation while the other did not. We recorded intracellularly the activity of a particular wide-field motion-sensitive neuron, the horizontal system equatorial cell (HSE) in blowflies. The experimental data were interpreted based on a computational model of the visual motion pathway, which included the spatially pooling HSE-cell. By comparing the difference between the recorded and modeled HSE-cell responses induced by the two types of motion adaptation, the major characteristics of local and wide-field adaptation could be pinpointed. Wide-field adaptation could be shown to strongly depend on the activation level of the cell and, thus, on the direction of motion. In contrast, the response gain is reduced by local motion adaptation to a similar extent independent of the direction of motion. This direction-independent adaptation differs fundamentally from the well-known adaptive adjustment of response gain according to the prevailing overall stimulus level that is considered essential for an efficient signal representation by neurons with a limited operating range. Direction-independent adaptation is discussed to result from the joint activity of local motion-sensitive neurons of different preferred directions and to lead to a representation of the local motion direction that is independent of the overall direction of global motion.

Taking a goal-centred dynamic snapshot as a possibility for local homing in initially naïve bumblebees.

It is essential for central place foragers, such as bumblebees, to return reliably to their nest. Bumblebees, leaving their inconspicuous nest hole for the first time need to gather and learn sufficient information about their surroundings to allow them to return to their nest at the end of their trip, instead of just flying away to forage. Therefore, we assume an intrinsic learning programme that manifests itself in the flight structure immediately after leaving the nest for the first time. In this study, we recorded and analysed the first outbound flight of individually marked naïve bumblebees in an indoor environment. We found characteristic loop-like features in the flight pattern that appear to be necessary for the bees to acquire environmental information and might be relevant for finding the nest hole after a foraging trip. Despite common features in their spatio-temporal organisation, first departure flights from the nest are characterised by a high level of variability in their loop-like flight structure across animals. Changes in turn direction of body orientation, for example, are distributed evenly across the entire area used for the flights without any systematic relationship to the nest location. By considering the common flight motifs and this variability, we came to the hypothesis that a kind of dynamic snapshot is taken during the early phase of departure flights centred at the nest location. The quality of this snapshot is hypothesised to be 'tested' during the later phases of the departure flights concerning its usefulness for local homing.

Influence of environmental information in natural scenes and the effects of motion adaptation on a fly motion-sensitive neuron during simulated flight.

Gaining information about the spatial layout of natural scenes is a challenging task that flies need to solve, especially when moving at high velocities. A group of motion sensitive cells in the lobula plate of flies is supposed to represent information about self-motion as well as the environment. Relevant environmental features might be the nearness of structures, influencing retinal velocity during translational self-motion, and the brightness contrast. We recorded the responses of the H1 cell, an individually identifiable lobula plate tangential cell, during stimulation with image sequences, simulating translational motion through natural sceneries with a variety of differing depth structures. A correlation was found between the average nearness of environmental structures within large parts of the cell's receptive field and its response across a variety of scenes, but no correlation was found between the brightness contrast of the stimuli and the cell response. As a consequence of motion adaptation resulting from repeated translation through the environment, the time-dependent response modulations induced by the spatial structure of the environment were increased relatively to the background activity of the cell. These results support the hypothesis that some lobula plate tangential cells do not only serve as sensors of self-motion, but also as a part of a neural system that processes information about the spatial layout of natural scenes.

Motion as a source of environmental information: a fresh view on biological motion computation by insect brains.

Despite their miniature brains insects, such as flies, bees and wasps, are able to navigate by highly erobatic flight maneuvers in cluttered environments. They rely on spatial information that is contained in the retinal motion patterns induced on the eyes while moving around ("optic flow") to accomplish their extraordinary performance. Thereby, they employ an active flight and gaze strategy that separates rapid saccade-like turns from translatory flight phases where the gaze direction is kept largely constant. This behavioral strategy facilitates the processing of environmental information, because information about the distance of the animal to objects in the environment is only contained in the optic flow generated by translatory motion. However, motion detectors as are widespread in biological systems do not represent veridically the velocity of the optic flow vectors, but also reflect textural information about the environment. This characteristic has often been regarded as a limitation of a biological motion detection mechanism. In contrast, we conclude from analyses challenging insect movement detectors with image flow as generated during translatory locomotion through cluttered natural environments that this mechanism represents the contours of nearby objects. Contrast borders are a main carrier of functionally relevant object information in artificial and natural sceneries. The motion detection system thus segregates in a computationally parsimonious way the environment into behaviorally relevant nearby objects and-in many behavioral contexts-less relevant distant structures. Hence, by making use of an active flight and gaze strategy, insects are capable of performing extraordinarily well even with a computationally simple motion detection mechanism.

Texture-defined objects influence responses of blowfly motion-sensitive neurons under natural dynamical conditions.

The responses of visual interneurons of flies involved in the processing of motion information do not only depend on the velocity, but also on other stimulus parameters, such as the contrast and the spatial frequency content of the stimulus pattern. These dependencies have been known for long, but it is still an open question how they affect the neurons' performance in extracting information about the structure of the environment under the specific dynamical conditions of natural flight. Free-flight of blowflies is characterized by sequences of phases of translational movements lasting for just 30-100 ms interspersed with even shorter and extremely rapid saccade-like rotational shifts in flight and gaze direction. Previous studies already analyzed how nearby objects, leading to relative motion on the retina with respect to a more distant background, influenced the response of a class of fly motion sensitive visual interneurons, the horizontal system (HS) cells. In the present study, we focused on objects that differed from their background by discontinuities either in their brightness contrast or in their spatial frequency content. We found strong object-induced effects on the membrane potential even during the short intersaccadic intervals, if the background contrast was small and the object contrast sufficiently high. The object evoked similar response increments provided that it contained higher spatial frequencies than the background, but not under reversed conditions. This asymmetry in the response behavior is partly a consequence of the depolarization level induced by the background. Thus, our results suggest that, under the specific dynamical conditions of natural flight, i.e., on a very short timescale, the responses of HS cells represent object information depending on the polarity of the difference between object and background contrast and spatial frequency content.

Octopaminergic modulation of a fly visual motion-sensitive neuron during stimulation with naturalistic optic flow.

In a variety of species locomotor activity, like walking or flying, has been demonstrated to alter visual information processing. The neuromodulator octopamine was shown to change the response characteristics of optic flow processing neurons in the fly's visual system in a similar way as locomotor activity. This modulation resulted in enhanced neuronal responses, in particular during sustained stimulation with high temporal frequencies, and in shorter latencies of responses to abrupt onsets of pattern motion. These state-dependent changes were interpreted to adjust neuronal tuning to the range of high velocities encountered during locomotion. Here we assess the significance of these changes for the processing of optic flow as experienced during flight. Naturalistic image sequences were reconstructed based on measurements of the head position and gaze direction of Calliphora vicina flying in an arena. We recorded the responses of the V1 neuron during presentation of these image sequences on a panoramic stimulus device ("FliMax"). Consistent with previous accounts, we found that spontaneous as well as stimulus-induced spike rates were increased by an octopamine agonist and decreased by an antagonist. Moreover, a small but consistent decrease in response latency upon octopaminergic activation was present, which might support fast responses to optic flow cues and limit instabilities during closed-loop optomotor regulation. However, apart from these effects the similarities between the dynamic response properties in the different pharmacologically induced states were surprisingly high, indicating that the processing of naturalistic optic flow is not fundamentally altered by octopaminergic modulation.

Encoding of naturalistic optic flow by motion sensitive neurons of nucleus rotundus in the zebra finch (Taeniopygia guttata).

The retinal image changes that occur during locomotion, the optic flow, carry information about self-motion and the three-dimensional structure of the environment. Especially fast moving animals with only little binocular vision depend on these depth cues for maneuvering. They actively control their gaze to facilitate perception of depth based on cues in the optic flow. In the visual system of birds, nucleus rotundus neurons were originally found to respond to object motion but not to background motion. However, when background and object were both moving, responses increased the more the direction and velocity of object and background motion on the retina differed. These properties may play a role in representing depth cues in the optic flow. We therefore investigated, how neurons in nucleus rotundus respond to optic flow that contains depth cues. We presented simplified and naturalistic optic flow on a panoramic LED display while recording from single neurons in nucleus rotundus of anaesthetized zebra finches. Unlike most studies on motion vision in birds, our stimuli included depth information. We found extensive responses of motion selective neurons in nucleus rotundus to optic flow stimuli. Simplified stimuli revealed preferences for optic flow reflecting translational or rotational self-motion. Naturalistic optic flow stimuli elicited complex response modulations, but the presence of objects was signaled by only few neurons. The neurons that did respond to objects in the optic flow, however, show interesting properties.

Spatial vision in insects is facilitated by shaping the dynamics of visual input through behavioral action.

Insects such as flies or bees, with their miniature brains, are able to control highly aerobatic flight maneuvres and to solve spatial vision tasks, such as avoiding collisions with obstacles, landing on objects, or even localizing a previously learnt inconspicuous goal on the basis of environmental cues. With regard to solving such spatial tasks, these insects still outperform man-made autonomous flying systems. To accomplish their extraordinary performance, flies and bees have been shown by their characteristic behavioral actions to actively shape the dynamics of the image flow on their eyes ("optic flow"). The neural processing of information about the spatial layout of the environment is greatly facilitated by segregating the rotational from the translational optic flow component through a saccadic flight and gaze strategy. This active vision strategy thus enables the nervous system to solve apparently complex spatial vision tasks in a particularly efficient and parsimonious way. The key idea of this review is that biological agents, such as flies or bees, acquire at least part of their strength as autonomous systems through active interactions with their environment and not by simply processing passively gained information about the world. These agent-environment interactions lead to adaptive behavior in surroundings of a wide range of complexity. Animals with even tiny brains, such as insects, are capable of performing extraordinarily well in their behavioral contexts by making optimal use of the closed action-perception loop. Model simulations and robotic implementations show that the smart biological mechanisms of motion computation and visually-guided flight control might be helpful to find technical solutions, for example, when designing micro air vehicles carrying a miniaturized, low-weight on-board processor.

Octopaminergic modulation of contrast gain adaptation in fly visual motion-sensitive neurons.

Locomotor activity like walking or flying has recently been shown to alter visual processing in several species. In insects, the neuromodulator octopamine is thought to play an important role in mediating state changes during locomotion of the animal [K.D. Longden & H.G. Krapp (2009) J. Neurophysiol., 102, 3606-3618; (2010) Front. Syst. Neurosci., 4, 153; S.N. Jung et al. (2011)J. Neurosci., 31, 9231-9237]. Here, we used the octopamine agonist chlordimeform (CDM) to mimic effects of behavioural state changes on visual motion processing. We recorded from identified motion-sensitive visual interneurons in the lobula plate of the blowfly Calliphora vicina. In these neurons, which are thought to be involved in visual guidance of locomotion, motion adaptation leads to a prominent attenuation of contrast sensitivity. Following CDM application, the neurons maintained high contrast sensitivity in the adapted state. This modulation of contrast gain adaptation was independent of the activity of the recorded neurons, because it was also present after stimulation with visual motion that did not result in deviations from the neurons' resting activity. We conclude that CDM affects presynaptic inputs of the recorded neurons. Accordingly, the effect of CDM was weak when adapting and test stimuli were presented in different parts of the receptive field, stimulating separate populations of local presynaptic neurons. In the peripheral visual system adaptation depends on the temporal frequency of the stimulus pattern and is therefore related to pattern velocity. Contrast gain adaptation could therefore be the basis for a shift in the velocity tuning that was previously suggested to contribute to state-dependent processing of visual motion information in the lobula plate interneurons.

Blowfly flight characteristics are shaped by environmental features and controlled by optic flow information.

Blowfly flight consists of two main components, saccadic turns and intervals of mostly straight gaze direction, although, as a consequence of inertia, flight trajectories usually change direction smoothly. We investigated how flight behavior changes depending on the surroundings and how saccadic turns and intersaccadic translational movements might be controlled in arenas of different width with and without obstacles. Blowflies do not fly in straight trajectories, even when traversing straight flight arenas; rather, they fly in meandering trajectories. Flight speed and the amplitude of meanders increase with arena width. Although saccade duration is largely constant, peak angular velocity and succession into either direction are variable and depend on the visual surroundings. Saccade rate and amplitude also vary with arena layout and are correlated with the 'time-to-contact' to the arena wall. We provide evidence that both saccade and velocity control rely to a large extent on the intersaccadic optic flow generated in eye regions looking well in front of the fly, rather than in the lateral visual field, where the optic flow at least during forward flight tends to be strongest.

Species-Specific Flight Styles of Flies are Reflected in the Response Dynamics of a Homolog Motion-Sensitive Neuron.

Hoverflies and blowflies have distinctly different flight styles. Yet, both species have been shown to structure their flight behavior in a way that facilitates extraction of 3D information from the image flow on the retina (optic flow). Neuronal candidates to analyze the optic flow are the tangential cells in the third optical ganglion - the lobula complex. These neurons are directionally selective and integrate the optic flow over large parts of the visual field. Homolog tangential cells in hoverflies and blowflies have a similar morphology. Because blowflies and hoverflies have similar neuronal layout but distinctly different flight behaviors, they are an ideal substrate to pinpoint potential neuronal adaptations to the different flight styles. In this article we describe the relationship between locomotion behavior and motion vision on three different levels: (1) We compare the different flight styles based on the categorization of flight behavior into prototypical movements. (2) We measure the species-specific dynamics of the optic flow under naturalistic flight conditions. We found the translational optic flow of both species to be very different. (3) We describe possible adaptations of a homolog motion-sensitive neuron. We stimulate this cell in blowflies (Calliphora) and hoverflies (Eristalis) with naturalistic optic flow generated by both species during free flight. The characterized hoverfly tangential cell responds faster to transient changes in the optic flow than its blowfly homolog. It is discussed whether and how the different dynamical response properties aid optic flow analysis.

Object representation and distance encoding in three-dimensional environments by a neural circuit in the visual system of the blowfly.

Three motion-sensitive key elements of a neural circuit, presumably involved in processing object and distance information, were analyzed with optic flow sequences as experienced by blowflies in a three-dimensional environment. This optic flow is largely shaped by the blowfly's saccadic flight and gaze strategy, which separates translational flight segments from fast saccadic rotations. By modifying this naturalistic optic flow, all three analyzed neurons could be shown to respond during the intersaccadic intervals not only to nearby objects but also to changes in the distance to background structures. In the presence of strong background motion, the three types of neuron differ in their sensitivity for object motion. Object-induced response increments are largest in FD1, a neuron long known to respond better to moving objects than to spatially extended motion patterns, but weakest in VCH, a neuron that integrates wide-field motion from both eyes and, by inhibiting the FD1 cell, is responsible for its object preference. Small but significant object-induced response increments are present in HS cells, which serve both as a major input neuron of VCH and as output neurons of the visual system. In both HS and FD1, intersaccadic background responses decrease with increasing distance to the animal, although much more prominently in FD1. This strong dependence of FD1 on background distance is concluded to be the consequence of the activity of VCH that dramatically increases its activity and, thus, its inhibitory strength with increasing distance.

Synaptic transmission of graded membrane potential changes and spikes between identified visual interneurons.

Several physiological mechanisms allow sensory information to be propagated in neuronal networks. According to the conventional view of signal processing, graded changes of membrane potential at the dendrite are converted into a sequence of spikes. However, in many sensory receptors and several types of mostly invertebrate neurons, graded potential changes have a direct impact on the cells' output signals. The visual system of the blowfly Calliphora vicina is a good model system to study synaptic transmission in vivo during sensory stimulation. We recorded extracellularly from an identified motion-sensitive neuron while simultaneously measuring and controlling the membrane potential of individual elements of its presynaptic input ensemble. The membrane potential in the terminals of the presynaptic neuron is composed of two components, graded membrane potential changes and action potentials. To dissociate the roles of action potentials and graded potential changes in synaptic transmission we used voltage-clamp-controlled current-clamp techniques to suppress the graded membrane potential changes without affecting action potentials. Our results indicate that both the graded potential and the action potentials of the presynaptic neuron have an impact on the spiking characteristics of the postsynaptic neuron. Although a tight temporal coupling between pre- and postsynaptic spikes exists, the timing between these spikes is also affected by graded potential changes. We propose that the control of synaptic transfer of a dynamically complex signal by graded changes in membrane potential and spikes is useful to enable a temporally precise coupling of spikes in response to sudden transitions in stimulus intensity.

Binocular integration of visual information: a model study on naturalistic optic flow processing.

The computation of visual information from both visual hemispheres is often of functional relevance when solving orientation and navigation tasks. The vCH-cell is a motion-sensitive wide-field neuron in the visual system of the blowfly Calliphora, a model system in the field of optic flow processing. The vCH-cell receives input from various other identified wide-field cells, the receptive fields of which are located in both the ipsilateral and the contralateral visual field. The relevance of this connectivity to the processing of naturalistic image sequences, with their peculiar dynamical characteristics, is still unresolved. To disentangle the contributions of the different input components to the cell's overall response, we used electrophysiologically determined responses of the vCH-cell and its various input elements to tune a model of the vCH-circuit. Their impact on the vCH-cell response could be distinguished by stimulating not only extended parts of the visual field of the fly, but also selected regions in the ipsi- and contralateral visual field with behaviorally generated optic flow. We show that a computational model of the vCH-circuit is able to account for the neuronal activities of the counterparts in the blowfly's visual system. Furthermore, we offer an insight into the dendritic integration of binocular visual input.

Impact of visual motion adaptation on neural responses to objects and its dependence on the temporal characteristics of optic flow.

It is still unclear how sensory systems efficiently encode signals with statistics as experienced by animals in the real world and what role adaptation plays during normal behavior. Therefore, we studied the performance of visual motion-sensitive neurons of blowflies, the horizontal system neurons, with optic flow that was reconstructed from the head trajectories of semi-free-flying flies. To test how motion adaptation is affected by optic flow dynamics, we manipulated the seminatural optic flow by targeted modifications of the flight trajectories and assessed to what extent neuronal responses to an object located close to the flight trajectory depend on adaptation dynamics. For all types of adapting optic flow object-induced response increments were stronger in the adapted compared with the nonadapted state. Adaptation with optic flow characterized by the typical alternation between translational and rotational segments produced this effect but also adaptation with optic flow that lacked these distinguishing features and even pure rotation at a constant angular velocity. The enhancement of object-induced response increments had a direction-selective component because preferred-direction rotation and natural optic flow were more efficient adaptors than null-direction rotation. These results indicate that natural dynamics of optic flow is not a basic requirement to adapt neurons in a specific, presumably functionally beneficial way. Our findings are discussed in the light of adaptation mechanisms proposed on the basis of experiments previously done with conventional experimenter-defined stimuli.

Chasing behavior and optomotor following in free-flying male blowflies: flight performance and interactions of the underlying control systems.

The chasing behavior of male blowflies after small targets belongs to the most rapid and virtuosic visually guided behaviors found in nature. Since in a structured environment any turn towards a target inevitably leads to a displacement of the entire retinal image in the opposite direction, it might evoke optomotor following responses counteracting the turn. To analyze potential interactions between the control systems underlying chasing behavior and optomotor following, respectively, we performed behavioral experiments on male blowflies and examined the characteristics of the two flight control systems in isolation and in combination. Three findings are particularly striking. (i) The characteristic saccadic flight and gaze style - a distinctive feature of blowfly cruising flights - is largely abandoned when the entire visual surroundings move around the fly; in this case flies tend to follow the moving pattern in a relatively continuous and smooth way. (ii) When male flies engage in following a small target, they also employ a smooth pursuit strategy. (iii) Although blowflies are reluctant to fly at high background velocities, the performance and dynamical characteristics of the chasing system are not much affected when the background moves in either the same or in the opposite direction as the target. Hence, the optomotor following response is largely suppressed by the chasing system and does not much impair chasing performance.

A syntax of hoverfly flight prototypes.

Hoverflies such as Eristalis tenax Linnaeus are known for their distinctive flight style. They can hover on the same spot for several seconds and then burst into movement in apparently any possible direction. In order to determine a quantitative and structured description of complex flight manoeuvres, we searched for a set of repeatedly occurring prototypical movements (PMs) and a set of rules for their ordering. PMs were identified by applying clustering algorithms to the translational and rotational velocities of the body of Eristalis during free-flight sequences. This approach led to nine stable and reliable PMs, and thus provided a tremendous reduction in the complexity of behavioural description. This set of PMs together with the probabilities of transition between them constitute a syntactical description of flight behaviour. The PMs themselves can be roughly segregated into fast rotational turns (saccades) and a variety of distinct translational movements (intersaccadic intervals). We interpret this segregation as reflecting an active sensing strategy which facilitates the extraction of spatial information from retinal image displacements. Detailed analysis of saccades shows that they are performed around all rotational axes individually and in all possible combinations. We found the probability of occurrence of a given saccade type to depend on parameters such as the angle between the long body axis and the direction of flight.

Adaptation accentuates responses of fly motion-sensitive visual neurons to sudden stimulus changes.

Adaptation in sensory and neuronal systems usually leads to reduced responses to persistent or frequently presented stimuli. In contrast to simple fatigue, adapted neurons often retain their ability to encode changes in stimulus intensity and to respond when novel stimuli appear. We investigated how the level of adaptation of a fly visual motion-sensitive neuron affects its responses to discontinuities in the stimulus, i.e. sudden brief changes in one of the stimulus parameters (velocity, contrast, grating orientation and spatial frequency). Although the neuron's overall response decreased gradually during ongoing motion stimulation, the response transients elicited by stimulus discontinuities were preserved or even enhanced with adaptation. Moreover, the enhanced sensitivity to velocity changes by adaptation was not restricted to a certain velocity range, but was present regardless of whether the neuron was adapted to a baseline velocity below or above its steady-state velocity optimum. Our results suggest that motion adaptation helps motion-sensitive neurons to preserve their sensitivity to novel stimuli even in the presence of strong tonic stimulation, for example during self-motion.

Gaze strategy in the free flying zebra finch (Taeniopygia guttata).

Fast moving animals depend on cues derived from the optic flow on their retina. Optic flow from translational locomotion includes information about the three-dimensional composition of the environment, while optic flow experienced during a rotational self motion does not. Thus, a saccadic gaze strategy that segregates rotations from translational movements during locomotion will facilitate extraction of spatial information from the visual input. We analysed whether birds use such a strategy by highspeed video recording zebra finches from two directions during an obstacle avoidance task. Each frame of the recording was examined to derive position and orientation of the beak in three-dimensional space. The data show that in all flights the head orientation was shifted in a saccadic fashion and was kept straight between saccades. Therefore, birds use a gaze strategy that actively stabilizes their gaze during translation to simplify optic flow based navigation. This is the first evidence of birds actively optimizing optic flow during flight.

Motion adaptation enhances object-induced neural activity in three-dimensional virtual environment.

Many response characteristics of neurons sensitive to visual motion depend on stimulus history and change during prolonged stimulation. Although the changes are usually regarded as adaptive, their functional significance is still not fully understood. With experimenter-defined stimuli, previous research on motion adaptation has mainly focused on enhancing the detection of changes in the stimulus domain, on preventing output saturation and on energy efficient coding. Here we will analyze in the blowfly visual system the functional significance of motion adaptation under the complex stimulus conditions encountered in the three-dimensional world. Identified motion sensitive neurons are confronted with seminatural optic flow as is seen by semi-free-flying animals as well as targeted modifications of it. Motion adaptation is shown to enhance object-induced neural responses in a three-dimensional environment although the overall neuronal response amplitude decreases during prolonged motion stimulation.