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Abstract Animals have evolved mechanisms to travel safely and efficiently within different habitats. On a journey in dense terrains animals avoid collisions and cross narrow passages while controlling an overall course. Multiple hypotheses target how animals solve challenges faced during such travel. Here we show that a single mechanism enables safe and efficient travel. We developed a robot inspired by insects. It has remarkable capabilities to travel in dense terrain, avoiding collisions, crossing gaps and selecting safe passages. These capabilities are accomplished by a neuromorphic network steering the robot toward regions of low apparent motion. Our system leverages knowledge about vision processing and obstacle avoidance in insects. Our results demonstrate how insects might safely travel through diverse habitats. We anticipate our system to be a working hypothesis to study insects’ travels in dense terrains. Furthermore, it illustrates that we can design novel hardware systems by understanding the underlying mechanisms driving behaviour.

IntroductionIn order to successfully move from place to place, our brain often combines sensory inputs from various sources by dynamically weighting spatial cues according to their reliability and relevance for a given task. Two of the most important cues in navigation are the spatial arrangement of landmarks in the environment, and the continuous path integration of travelled distances and changes in direction. Several studies have shown that Bayesian integration of cues provides a good explanation for navigation in environments dominated by small numbers of easily identifiable landmarks. However, it remains largely unclear how cues are combined in more complex environments.MethodsTo investigate how humans process and combine landmarks and path integration in complex environments, we conducted a series of triangle completion experiments in virtual reality, in which we varied the number of landmarks from an open steppe to a dense forest, thus going beyond the spatially simple environments that have been studied in the past. We analysed spatial behaviour at both the population and individual level with linear regression models and developed a computational model, based on maximum likelihood estimation (MLE), to infer the underlying combination of cues.ResultsOverall homing performance was optimal in an environment containing three landmarks arranged around the goal location. With more than three landmarks, individual differences between participants in the use of cues are striking. For some, the addition of landmarks does not worsen their performance, whereas for others it seems to impair their use of landmark information.DiscussionIt appears that navigation success in complex environments depends on the ability to identify the correct clearing around the goal location, suggesting that some participants may not be able to see the forest for the trees.

Social insects such as ants and bees are excellent navigators. To manage their daily routines bumblebees, as an example, must learn multiple locations in their environment, like flower patches and their nest. While navigating from one location to another, they mainly rely on vision. Although the environment in which bumblebees live, be it a meadow or a garden, is visually stable overall, it may be prone to changes such as moving shadows or the displacement of an object in the scenery. Therefore, bees might not solely rely on visual cues, but use additional sources of information, forming a multimodal guidance system to ensure their return home to their nest. Here we show that the home-finding behavior of bumblebees, when confronted with a visually ambiguous scenario, is strongly influenced by natural scent marks they deposit at the inconspicuous nest hole when leaving their nest. Bumblebees search for a longer time and target their search with precision at potential nest locations that are visually familiar, if also marked with their natural scent. This finding sheds light on the crucial role of odor in helping bees find their way back to their inconspicuous nest.

Spatial navigation research in humans increasingly relies on experiments using virtual reality (VR) tools, which allow for the creation of highly flexible, and immersive study environments, that can react to participant interaction in real time. Despite the popularity of VR, tools simplifying the creation and data management of such experiments are rare and often restricted to a specific scope-limiting usability and comparability. To overcome those limitations, we introduce the Virtual Navigation Toolbox (VNT), a collection of interchangeable and independent tools for the development of spatial navigation VR experiments using the popular Unity game engine. The VNT's features are packaged in loosely coupled and reusable modules, facilitating convenient implementation of diverse experimental designs. Here, we depict how the VNT fulfils feature requirements of different VR environments and experiments, guiding through the implementation and execution of a showcase study using the toolbox. The presented showcase study reveals that homing performance in a classic triangle completion task is invariant to translation velocity of the participant's avatar, but highly sensitive to the number of landmarks. The VNT is freely available under a creative commons license, and we invite researchers to contribute, extending and improving tools using the provided repository.

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.

Bumblebees perform complex flight maneuvers around the barely visible entrance of their nest upon their first departures. During these flights bees learn visual information about the surroundings, possibly including its spatial layout. They rely on this information to return home. Depth information can be derived from the apparent motion of the scenery on the bees' retina. This motion is shaped by the animal's flight and orientation: Bees employ a saccadic flight and gaze strategy, where rapid turns of the head (saccades) alternate with flight segments of apparently constant gaze direction (intersaccades). When during intersaccades the gaze direction is kept relatively constant, the apparent motion contains information about the distance of the animal to environmental objects, and thus, in an egocentric reference frame. Alternatively, when the gaze direction rotates around a fixed point in space, the animal perceives the depth structure relative to this pivot point, i.e., in an allocentric reference frame. If the pivot point is at the nest-hole, the information is nest-centric. Here, we investigate in which reference frames bumblebees perceive depth information during their learning flights. By precisely tracking the head orientation, we found that half of the time, the head appears to pivot actively. However, only few of the corresponding pivot points are close to the nest entrance. Our results indicate that bumblebees perceive visual information in several reference frames when they learn about the surroundings of a behaviorally relevant location.

Returning home is a crucial task accomplished daily by many animals, including humans. Because of their tiny brains, insects, like bees or ants, are good study models for efficient navigation strategies. Bees and ants are known to rely mainly on learned visual information about the nest surroundings to pinpoint their barely visible nest-entrance. During the return, when the actual sight of the insect matches the learned information, the insect is easily guided home. Occasionally, modifications to the visual environment may take place while the insect is on a foraging trip. Here, we addressed the ecologically relevant question of how bumblebees' homing is affected by such a situation. In an artificial setting, we habituated bees to be guided to their nest by two constellations of visual cues. After habituation, these cues were displaced during foraging trips into a conflict situation. We recorded bumblebees' return flights in such circumstances and investigated where they search for their nest entrance following the degree of displacement between the two visually relevant cues. Bumblebees mostly searched at the fictive nest location as indicated by either cue constellation, but never at a compromise location between them. We compared these experimental results to the predictions of different types of homing models. We found that models guiding an agent by a single holistic view of the nest surroundings could not account for the bumblebees' search behaviour in cue-conflict situations. Instead, homing models relying on multiple views were sufficient. We could further show that homing models required fewer views and got more robust to height changes if optic flow-based spatial information was encoded and learned, rather than just brightness information.

Emulating the highly resource-efficient processing of visual motion information in the brain of flying insects, a bio-inspired controller for collision avoidance and navigation was implemented on a novel, integrated System-on-Chip-based hardware module. The hardware module is used to control visually-guided navigation behavior of the stick insect-like hexapod robot HECTOR. By leveraging highly parallelized bio-inspired algorithms to extract nearness information from visual motion in dynamically reconfigurable logic, HECTOR is able to navigate to predefined goal positions without colliding with obstacles. The system drastically outperforms CPU- and graphics card-based implementations in terms of speed and resource efficiency, making it suitable to be also placed on fast moving robots, such as flying drones.

Navigation in cluttered environments is an important challenge for animals and robots alike and has been the subject of many studies trying to explain and mimic animal navigational abilities. However, the question of selecting an appropriate home location has, so far, received only little attention. This is surprising, since the choice of a home location might greatly influence an animal's navigation performance. To address the question of home choice in cluttered environments, a systematic analysis of homing trajectories was performed by computer simulations using a skyline-based local homing method. Our analysis reveals that homing performance strongly depends on the location of the home in the environment. Furthermore, it appears that by assessing homing success in the immediate vicinity of the home, an animal might be able to predict its overall success in returning to it from within a much larger area.

Neuronal representation and extraction of spatial information are essential for behavioral control. For flying insects, a plausible way to gain spatial information is to exploit distance-dependent optic flow that is generated during translational self-motion. Optic flow is computed by arrays of local motion detectors retinotopically arranged in the second neuropile layer of the insect visual system. These motion detectors have adaptive response characteristics, i.e. their responses to motion with a constant or only slowly changing velocity decrease, while their sensitivity to rapid velocity changes is maintained or even increases. We analyzed by a modeling approach how motion adaptation affects signal representation at the output of arrays of motion detectors during simulated flight in artificial and natural 3D environments. We focused on translational flight, because spatial information is only contained in the optic flow induced by translational locomotion. Indeed, flies, bees and other insects segregate their flight into relatively long intersaccadic translational flight sections interspersed with brief and rapid saccadic turns, presumably to maximize periods of translation (80% of the flight). With a novel adaptive model of the insect visual motion pathway we could show that the motion detector responses to background structures of cluttered environments are largely attenuated as a consequence of motion adaptation, while responses to foreground objects stay constant or even increase. This conclusion even holds under the dynamic flight conditions of insects.

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.

Flying insects, such as flies or bees, rely on consistent information regarding the depth structure of the environment when performing their flight maneuvers in cluttered natural environments. These behaviors include avoiding collisions, approaching targets or spatial navigation. Insects are thought to obtain depth information visually from the retinal image displacements (`optic flow') during translational ego-motion. Optic flow in the insect visual system is processed by a mechanism that can be modeled by correlation-type elementary motion detectors (EMDs). However, it is still an open question how spatial information can be extracted reliably from the responses of the highly contrast- and pattern-dependent EMD responses, especially if the vast range of light intensities encountered in natural environments is taken into account. This question will be addressed here by systematically modeling the peripheral visual system of flies, including various adaptive mechanisms. Different model variants of the peripheral visual system were stimulated with image sequences that mimic the panoramic visual input during translational ego-motion in various natural environments, and the resulting peripheral signals were fed into an array of EMDs. We characterized the influence of each peripheral computational unit on the representation of spatial information in the EMD responses. Our model simulations reveal that information about the overall light level needs to be eliminated from the EMD input as is accomplished under light-adapted conditions in the insect peripheral visual system. The response characteristics of large monopolar cells resemble that of a band-pass filter, which reduces the contrast dependency of EMDs strongly, effectively enhancing the representation of the nearness of objects and, especially, of their contours. We furthermore show that local brightness adaptation of photoreceptors allows for spatial vision under a wide range of dynamic light conditions.

Optic flow, i.e., retinal image movement resulting from ego-motion, is a crucial source of information used for obstacle avoidance and course control in flying insects. Optic flow analysis may prove promising for mobile robotics although it is currently not among the standard techniques. Insects have developed a computationally cheap analysis mechanism for image motion. Detailed computational models, the so-called elementary motion detectors (EMDs), describe motion detection in insects. However, the technical application of EMDs is complicated by the strong effect of local pattern contrast on their motion response. Here we present augmented versions of an EMD, the (s)cc-EMDs, which normalise their responses for contrast and thereby reduce the sensitivity to contrast changes. Thus, velocity changes of moving natural images are reflected more reliably in the detector response. The (s)cc-EMDs can easily be implemented in hardware and software and can be a valuable novel visual motion sensor for mobile robots.

Avoiding collisions is one of the most basic needs of any mobile agent, both biological and technical, when searching around or aiming toward a goal. We propose a model of collision avoidance inspired by behavioral experiments on insects and by properties of optic flow on a spherical eye experienced during translation, and test the interaction of this model with goal-driven behavior. Insects, such as flies and bees, actively separate the rotational and translational optic flow components via behavior, i.e. by employing a saccadic strategy of flight and gaze control. Optic flow experienced during translation, i.e. during intersaccadic phases, contains information on the depth-structure of the environment, but this information is entangled with that on self-motion. Here, we propose a simple model to extract the depth structure from translational optic flow by using local properties of a spherical eye. On this basis, a motion direction of the agent is computed that ensures collision avoidance. Flying insects are thought to measure optic flow by correlation-type elementary motion detectors. Their responses depend, in addition to velocity, on the texture and contrast of objects and, thus, do not measure the velocity of objects veridically. Therefore, we initially used geometrically determined optic flow as input to a collision avoidance algorithm to show that depth information inferred from optic flow is sufficient to account for collision avoidance under closed-loop conditions. Then, the collision avoidance algorithm was tested with bio-inspired correlation-type elementary motion detectors in its input. Even then, the algorithm led successfully to collision avoidance and, in addition, replicated the characteristics of collision avoidance behavior of insects. Finally, the collision avoidance algorithm was combined with a goal direction and tested in cluttered environments. The simulated agent then showed goal-directed behavior reminiscent of components of the navigation behavior of insects.

Changes in flight direction in flying insects are largely due to roll, yaw and pitch rotations of their body. Head orientation is stabilized for most of the time by counter rotation. Here, we use high-speed video to analyse head- and body-movements of the bumblebee Bombus terrestris while approaching and departing from a food source located between three landmarks in an indoor flight-arena. The flight paths consist of almost straight flight segments that are interspersed with rapid turns. These short and fast yaw turns ("saccades") are usually accompanied by even faster head yaw turns that change gaze direction. Since a large part of image rotation is thereby reduced to brief instants of time, this behavioural pattern facilitates depth perception from visual motion parallax during the intersaccadic intervals. The detailed analysis of the fine structure of the bees' head turning movements shows that the time course of single head saccades is very stereotypical. We find a consistent relationship between the duration, peak velocity and amplitude of saccadic head movements, which in its main characteristics resembles the so-called "saccadic main sequence" in humans. The fact that bumblebee head saccades are highly stereotyped as in humans, may hint at a common principle, where fast and precise motor control is used to reliably reduce the time during which the retinal images moves.

The control of self-motion is a basic, but complex task for both technical and biological systems. Various algorithms have been proposed that allow the estimation of self-motion from the optic flow on the eyes. We show that two apparently very different approaches to solve this task, one technically and one biologically inspired, can be transformed into each other under certain conditions. One estimator of self-motion is based on a matched filter approach; it has been developed to describe the function of motion sensitive cells in the fly brain. The other estimator, the Koenderink and van Doorn (KvD) algorithm, was derived analytically with a technical background. If the distances to the objects in the environment can be assumed to be known, the two estimators are linear and equivalent, but are expressed in different mathematical forms. However, for most situations it is unrealistic to assume that the distances are known. Therefore, the depth structure of the environment needs to be determined in parallel to the self-motion parameters and leads to a non-linear problem. It is shown that the standard least mean square approach that is used by the KvD algorithm leads to a biased estimator. We derive a modification of this algorithm in order to remove the bias and demonstrate its improved performance by means of numerical simulations. For self-motion estimation it is beneficial to have a spherical visual field, similar to many flying insects. We show that in this case the representation of the depth structure of the environment derived from the optic flow can be simplified. Based on this result, we develop an adaptive matched filter approach for systems with a nearly spherical visual field. Then only eight parameters about the environment have to be memorized and updated during self-motion.

Many flying insects, such as flies, wasps and bees, pursue a saccadic flight and gaze strategy. This behavioral strategy is thought to separate the translational and rotational components of self-motion and, thereby, to reduce the computational efforts to extract information about the environment from the retinal image flow. Because of the distinguishing dynamic features of this active flight and gaze strategy of insects, the present study analyzes systematically the spatiotemporal statistics of image sequences generated during saccades and intersaccadic intervals in cluttered natural environments. We show that, in general, rotational movements with saccade-like dynamics elicit fluctuations and overall changes in brightness, contrast and spatial frequency of up to two orders of magnitude larger than translational movements at velocities that are characteristic of insects. Distinct changes in image parameters during translations are only caused by nearby objects. Image analysis based on larger patches in the visual field reveals smaller fluctuations in brightness and spatial frequency composition compared to small patches. The temporal structure and extent of these changes in image parameters define the temporal constraints imposed on signal processing performed by the insect visual system under behavioral conditions in natural environments.

Even if a stimulus pattern moves at a constant velocity across the receptive field of motion-sensitive neurons, such as lobula plate tangential cells (LPTCs) of flies, the response amplitude modulates over time. The amplitude of these response modulations is related to local pattern properties of the moving retinal image. On the one hand, pattern-dependent response modulations have previously been interpreted as 'pattern-noise', because they deteriorate the neuron's ability to provide unambiguous velocity information. On the other hand, these modulations might also provide the system with valuable information about the textural properties of the environment. We analyzed the influence of the size and shape of receptive fields by simulations of four versions of LPTC models consisting of arrays of elementary motion detectors of the correlation type (EMDs). These models have previously been suggested to account for many aspects of LPTC response properties. Pattern-dependent response modulations decrease with an increasing number of EMDs included in the receptive field of the LPTC models, since spatial changes within the visual field are smoothed out by the summation of spatially displaced EMD responses. This effect depends on the shape of the receptive field, being the more pronounced--for a given total size--the more elongated the receptive field is along the direction of motion. Large elongated receptive fields improve the quality of velocity signals. However, if motion signals need to be localized the velocity coding is only poor but the signal provides--potentially useful--local pattern information. These modelling results suggest that motion vision by correlation type movement detectors is subject to uncertainty: you cannot obtain both an unambiguous and a localized velocity signal from the output of a single cell. Hence, the size and shape of receptive fields of motion sensitive neurons should be matched to their potential computational task.

The chasing behaviour of male blowflies after small targets belongs to the most rapid and virtuosic visually guided behaviours 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 analyse potential interactions between the control systems underlying chasing behaviour and optomotor following, respectively, we performed behavioural 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.

Quantitative analysis of animal behaviour is a requirement to understand the task solving strategies of animals and the underlying control mechanisms. The identification of repeatedly occurring behavioural components is thereby a key element of a structured quantitative description. However, the complexity of most behaviours makes the identification of such behavioural components a challenging problem. We propose an automatic and objective approach for determining and evaluating prototypical behavioural components. Behavioural prototypes are identified using clustering algorithms and finally evaluated with respect to their ability to represent the whole behavioural data set. The prototypes allow for a meaningful segmentation of behavioural sequences. We applied our clustering approach to identify prototypical movements of the head of blowflies during cruising flight. The results confirm the previously established saccadic gaze strategy by the set of prototypes being divided into either predominantly translational or rotational movements, respectively. The prototypes reveal additional details about the saccadic and intersaccadic flight sections that could not be unravelled so far. Successful application of the proposed approach to behavioural data shows its ability to automatically identify prototypical behavioural components within a large and noisy database and to evaluate these with respect to their quality and stability. Hence, this approach might be applied to a broad range of behavioural and neural data obtained from different animals and in different contexts.

BACKGROUND: Detecting objects is an important task when moving through a natural environment. Flies, for example, may land on salient objects or may avoid collisions with them. The neuronal ensemble of Figure Detection cells (FD-cells) in the visual system of the fly is likely to be involved in controlling these behaviours, as these cells are more sensitive to objects than to extended background structures. Until now the computations in the presynaptic neuronal network of FD-cells and, in particular, the functional significance of the experimentally established distributed dendritic processing of excitatory and inhibitory inputs is not understood. METHODOLOGY/PRINCIPAL FINDINGS: We use model simulations to analyse the neuronal computations responsible for the preference of FD-cells for small objects. We employed a new modelling approach which allowed us to account for the spatial spread of electrical signals in the dendrites while avoiding detailed compartmental modelling. The models are based on available physiological and anatomical data. Three models were tested each implementing an inhibitory neural circuit, but differing by the spatial arrangement of the inhibitory interaction. Parameter optimisation with an evolutionary algorithm revealed that only distributed dendritic processing satisfies the constraints arising from electrophysiological experiments. In contrast to a direct dendro-dendritic inhibition of the FD-cell (Direct Distributed Inhibition model), an inhibition of its presynaptic retinotopic elements (Indirect Distributed Inhibition model) requires smaller changes in input resistance in the inhibited neurons during visual stimulation. CONCLUSIONS/SIGNIFICANCE: Distributed dendritic inhibition of retinotopic elements as implemented in our Indirect Distributed Inhibition model is the most plausible wiring scheme for the neuronal circuit of FD-cells. This microcircuit is computationally similar to lateral inhibition between the retinotopic elements. Hence, distributed inhibition might be an alternative explanation of perceptual phenomena currently explained by lateral inhibition networks.

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.

Response variability is a fundamental issue in neural coding because it limits all information processing. The reliability of neuronal coding is quantified by various approaches in different studies. In most cases it is largely unclear to what extent the conclusions depend on the applied reliability measure, making a comparison across studies almost impossible. We demonstrate that different reliability measures can lead to very different conclusions even if applied to the same set of data: in particular, we applied information theoretical measures (Shannon information capacity and Kullback-Leibler divergence) as well as a discrimination measure derived from signal-detection theory to the responses of blowfly photoreceptors which represent a well established model system for sensory information processing. We stimulated the photoreceptors with white noise modulated light intensity fluctuations of different contrasts. Surprisingly, the signal-detection approach leads to a safe discrimination of the photoreceptor response even when the response signal-to-noise ratio (SNR) is well below unity whereas Shannon information capacity and also Kullback-Leibler divergence indicate a very low performance. Applying different measures, can, therefore, lead to very different interpretations concerning the system's coding performance. As a consequence of the lower sensitivity compared to the signal-detection approach, the information theoretical measures overestimate internal noise sources and underestimate the importance of photon shot noise. We stress that none of the used measures and, most likely no other measure alone, allows for an unbiased estimation of a neuron's coding properties. Therefore the applied measure needs to be selected with respect to the scientific question and the analyzed neuron's functional context.

Sensing is often implicitly assumed to be the passive acquisition of information. However, part of the sensory information is generated actively when animals move. For instance, humans shift their gaze actively in a sequence of saccades towards interesting locations in a scene. Likewise, many insects shift their gaze by saccadic turns of body and head, keeping their gaze fixed between saccades. Here we employ a novel panoramic virtual reality stimulator and show that motion computation in a blowfly visual interneuron is tuned to make efficient use of the characteristic dynamics of retinal image flow. The neuron is able to extract information about the spatial layout of the environment by utilizing intervals of stable vision resulting from the saccadic viewing strategy. The extraction is possible because the retinal image flow evoked by translation, containing information about object distances, is confined to low frequencies. This flow component can be derived from the total optic flow between saccades because the residual intersaccadic head rotations are small and encoded at higher frequencies. Information about the spatial layout of the environment can thus be extracted by the neuron in a computationally parsimonious way. These results on neuronal function based on naturalistic, behaviourally generated optic flow are in stark contrast to conclusions based on conventional visual stimuli that the neuron primarily represents a detector for yaw rotations of the animal.