Local motion adaptation enhances the representation of spatial structure at EMD arrays.

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.

Head orientation of walking blowflies is controlled by visual and mechanical cues.

During locomotion, animals employ visual and mechanical cues in order to establish the orientation of their head, which reflects the orientation of the visual coordinate system. However, in certain situations, contradictory cues may suggest different orientations relative to the environment. We recorded blowflies walking on a horizontal or tilted surface surrounded by visual cues suggesting a variety of orientations. We found that the different orientations relative to gravity of visual cues and walking surface were integrated, with the orientation of the surface being the major contributor to head orientation, while visual cues and gravity also play an important role. In contrast, visual cues did not affect body orientation much. Cue integration was modeled as the weighted sum of orientations suggested by the different cues. Our model suggests that in the case of lacking visual cues, more weight is given to gravity.

Peripheral Processing Facilitates Optic Flow-Based Depth Perception.

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 (LMCs) 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.

A Bio-inspired Collision Avoidance Model Based on Spatial Information Derived from Motion Detectors Leads to Common Routes.

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.

Depth information in natural environments derived from optic flow by insect motion detection system: a model analysis.

Knowing the depth structure of the environment is crucial for moving animals in many behavioral contexts, such as collision avoidance, targeting objects, or spatial navigation. An important source of depth information is motion parallax. This powerful cue is generated on the eyes during translatory self-motion with the retinal images of nearby objects moving faster than those of distant ones. To investigate how the visual motion pathway represents motion-based depth information we analyzed its responses to image sequences recorded in natural cluttered environments with a wide range of depth structures. The analysis was done on the basis of an experimentally validated model of the visual motion pathway of insects, with its core elements being correlation-type elementary motion detectors (EMDs). It is the key result of our analysis that the absolute EMD responses, i.e., the motion energy profile, represent the contrast-weighted nearness of environmental structures during translatory self-motion at a roughly constant velocity. In other words, the output of the EMD array highlights contours of nearby objects. This conclusion is largely independent of the scale over which EMDs are spatially pooled and was corroborated by scrutinizing the motion energy profile after eliminating the depth structure from the natural image sequences. Hence, the well-established dependence of correlation-type EMDs on both velocity and textural properties of motion stimuli appears to be advantageous for representing behaviorally relevant information about the environment in a computationally parsimonious way.

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.

Texture dependence of motion sensing and free flight behavior in blowflies.

MANY FLYING INSECTS EXHIBIT AN ACTIVE FLIGHT AND GAZE STRATEGY: purely translational flight segments alternate with quick turns called saccades. To generate such a saccadic flight pattern, the animals decide the timing, direction, and amplitude of the next saccade during the previous translatory intersaccadic interval. The information underlying these decisions is assumed to be extracted from the retinal image displacements (optic flow), which scale with the distance to objects during the intersaccadic flight phases. In an earlier study we proposed a saccade-generation mechanism based on the responses of large-field motion-sensitive neurons. In closed-loop simulations we achieved collision avoidance behavior in a limited set of environments but observed collisions in others. Here we show by open-loop simulations that the cause of this observation is the known texture-dependence of elementary motion detection in flies, reflected also in the responses of large-field neurons as used in our model. We verified by electrophysiological experiments that this result is not an artifact of the sensory model. Already subtle changes in the texture may lead to qualitative differences in the responses of both our model cells and their biological counterparts in the fly's brain. Nonetheless, free flight behavior of blowflies is only moderately affected by such texture changes. This divergent texture dependence of motion-sensitive neurons and behavioral performance suggests either mechanisms that compensate for the texture dependence of the visual motion pathway at the level of the circuits generating the saccadic turn decisions or the involvement of a hypothetical parallel pathway in saccadic control that provides the information for collision avoidance independent of the textural properties of the environment.