Contrast sensitivity of insect motion detectors to natural images

How do animals regulate self-movement despite large variation in the luminance contrast of the environment? Insects are capable of regulating flight speed based on the velocity of image motion, but the mechanisms for this are unclear. The Hassenstein–Reichardt correlator model and elaborations can accurately predict responses of motion detecting neurons under many conditions but fail to explain the apparent lack of spatial pattern and contrast dependence observed in freely flying bees and flies. To investigate this apparent discrepancy, we recorded intracellularly from horizontal-sensitive (HS) motion detecting neurons in the hoverfly while displaying moving images of natural environments. Contrary to results obtained with grating patterns, we show these neurons encode the velocity of natural images largely independently of the particular image used despite a threefold range of contrast. This invariance in response to natural images is observed in both strongly and minimally motion-adapted neurons but is sensitive to artificial manipulations in contrast. Current models of these cells account for some, but not all, of the observed insensitivity to image contrast. We conclude that fly visual processing may be matched to commonalities between natural scenes, enabling accurate estimates of velocity largely independent of the particular scene

A `bright zone' in male hoverfly (Eristalis tenax) eyes and associated faster motion detection and increased contrast sensitivity

Eyes of the hoverfly Eristalis tenax are sexually dimorphic such that males have a fronto-dorsal region of large facets. In contrast to other large flies in which large facets are associated with a decreased interommatidial angle to form a dorsal `acute zone' of increased spatial resolution, we show that a dorsal region of large facets in males appears to form a `bright zone' of increased light capture without substantially increased spatial resolution. Theoretically, more light allows for increased performance in tasks such as motion detection. To determine the effect of the bright zone on motion detection, local properties of wide field motion detecting neurons were investigated using localized sinusoidal gratings. The pattern of local preferred directions of one class of these cells, the HS cells, in Eristalis is similar to that reported for the blowfly Calliphora. The bright zone seems to contribute to local contrast sensitivity; high contrast sensitivity exists in portions of the receptive field served by large diameter facet lenses of males and is not observed in females. Finally, temporal frequency tuning is also significantly faster in this frontal portion of the world, particularly in males, where it overcompensates for the higher spatial-frequency tuning and shifts the predicted local velocity optimum to higher speeds. These results indicate that increased retinal illuminance due to the bright zone of males is used to enhance contrast sensitivity and speed motion detector responses. Additionally, local neural properties vary across the visual world in a way not expected if HS cells serve purely as matched filters to measure yaw-induced visual motion

Pattern-Dependent Response Modulations in Motion-Sensitive Visual Interneurons—A Model Study

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

A Model for the Detection of Moving Targets in Visual Clutter Inspired by Insect Physiology

We present a computational model for target discrimination based on intracellular recordings from neurons in the fly visual system. Determining how insects detect and track small moving features, often against cluttered moving backgrounds, is an intriguing challenge, both from a physiological and a computational perspective. Previous research has characterized higher-order neurons within the fly brain, known as ‘small target motion detectors’ (STMD), that respond robustly to moving features, even when the velocity of the target is matched to the background (i.e. with no relative motion cues). We recorded from intermediate-order neurons in the fly visual system that are well suited as a component along the target detection pathway. This full-wave rectifying, transient cell (RTC) reveals independent adaptation to luminance changes of opposite signs (suggesting separate ON and OFF channels) and fast adaptive temporal mechanisms, similar to other cell types previously described. From this physiological data we have created a numerical model for target discrimination. This model includes nonlinear filtering based on the fly optics, the photoreceptors, the 1st order interneurons (Large Monopolar Cells), and the newly derived parameters for the RTC. We show that our RTC-based target detection model is well matched to properties described for the STMDs, such as contrast sensitivity, height tuning and velocity tuning. The model output shows that the spatiotemporal profile of small targets is sufficiently rare within natural scene imagery to allow our highly nonlinear ‘matched filter’ to successfully detect most targets from the background. Importantly, this model can explain this type of feature discrimination without the need for relative motion cues

Optic Flow Based Visual Guidance: From Flying Insects to Miniature Aerial Vehicles

International audienc

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

Velocity constancy and models for wide-field visual motion detection in insects

The tangential neurons in the lobula plate region of the flies are known to respond to visual motion across broad receptive fields in visual space. When intracellular recordings are made from tangential neurons while the intact animal is stimulated visually with moving natural imagery, we find that neural response depends upon speed of motion but is nearly invariant with respect to variations in natural scenery. We refer to this invariance as velocity constancy. It is remarkable because natural scenes, in spite of similarities in spatial structure, vary considerably in contrast, and contrast dependence is a feature of neurons in the early visual pathway as well as of most models for the elementary operations of visual motion detection. Thus, we expect that operations must be present in the processing pathway that reduce contrast dependence in order to approximate velocity constancy. We consider models for such operations, including spatial filtering, motion adaptation, saturating nonlinearities, and nonlinear spatial integration by the tangential neurons themselves, and evaluate their effects in simulations of a tangential neuron and precursor processing in response to animated natural imagery. We conclude that all such features reduce interscene variance in response, but that the model system does not approach velocity constancy as closely as the biological tangential cell

A neurobiological and computational analysis of target discrimination in visual clutter by the insect visual system.

Some insects have the capability to detect and track small moving objects, often against cluttered moving backgrounds. Determining how this task is performed is an intriguing challenge, both from a physiological and computational perspective. Previous research has characterized higher-order neurons within the fly brain known as 'small target motion detectors‘ (STMD) that respond selectively to targets, even within complex moving surrounds. Interestingly, these cells still respond robustly when the velocity of the target is matched to the velocity of the background (i.e. with no relative motion cues). We performed intracellular recordings from intermediate-order neurons in the fly visual system (the medulla). These full-wave rectifying, transient cells (RTC) reveal independent adaptation to luminance changes of opposite signs (suggesting separate 'on‘ and 'off‘ channels) and fast adaptive temporal mechanisms (as seen in some previously described cell types). We show, via electrophysiological experiments, that the RTC is temporally responsive to rapidly changing stimuli and is well suited to serving an important function in a proposed target-detecting pathway. To model this target discrimination, we use high dynamic range (HDR) natural images to represent 'real-world‘ luminance values that serve as inputs to a biomimetic representation of photoreceptor processing. Adaptive spatiotemporal high-pass filtering (1st-order interneurons) shapes the transient 'edge-like‘ responses, useful for feature discrimination. Following this, a model for the RTC implements a nonlinear facilitation between the rapidly adapting, and independent polarity contrast channels, each with centre-surround antagonism. The recombination of the channels results in increased discrimination of small targets, of approximately the size of a single pixel, without the need for relative motion cues. This method of feature discrimination contrasts with traditional target and background motion-field computations. We show that our RTC-based target detection model is well matched to properties described for the higher-order STMD neurons, such as contrast sensitivity, height tuning and velocity tuning. The model output shows that the spatiotemporal profile of small targets is sufficiently rare within natural scene imagery to allow our highly nonlinear 'matched filter‘ to successfully detect many targets from the background. The model produces robust target discrimination across a biologically plausible range of target sizes and a range of velocities. We show that the model for small target motion detection is highly correlated to the velocity of the stimulus but not other background statistics, such as local brightness or local contrast, which normally influence target detection tasks. From an engineering perspective, we examine model elaborations for improved target discrimination via inhibitory interactions from correlation-type motion detectors, using a form of antagonism between our feature correlator and the more typical motion correlator. We also observe that a changing optimal threshold is highly correlated to the value of observer ego-motion. We present an elaborated target detection model that allows for implementation of a static optimal threshold, by scaling the target discrimination mechanism with a model-derived velocity estimation of ego-motion. Finally, we investigate the physiological relevance of this target discrimination model. We show that via very subtle image manipulation of the visual stimulus, our model accurately predicts dramatic changes in observed electrophysiological responses from STMD neurons.Thesis (Ph.D.) - University of Adelaide, School of Molecular and Biomedical Science, 200

Neuronal encoding of natural imagery in dragonfly motion pathways

Vision is the primary sense of humans and most other animals. While the act of seeing seems easy, the neuronal architectures that underlie this ability are some of the most complex of the brain. Insects represent an excellent model for investigating how vision operates as they often lead rich visual lives while possessing relatively simple brains. Among insects, aerial predators such as the dragonfly face additional survival tasks. Not only must aerial predators successfully navigate three-dimensional visual environments, they must also be able to identify and track their prey. This task is made even more difficult due to the complexity of visual scenes that contain detail on all scales of magnification, making the job of the predator particularly challenging. Here I investigate the physiology of neurons accessible through tracts in the third neuropil of the optic lobe of the dragonfly. It is at this stage of processing that the first evidence of both wide-field motion and object detection emerges. My research extends the current understanding of two main pathways in the dragonfly visual system, the wide-field motion pathway and target-tracking pathway. While wide-field motion pathways have been studied in numerous insects, until now the dragonfly wide-field motion pathway remains unstudied. Investigation of this pathway has revealed properties, novel among insects, specifically the purely optical adaptation to motion at both high and low velocities through motion adaptation. Here I characterise these newly described neurons and investigate their adaptation properties. The dragonfly target-tracking pathway has been studied extensively, but most research has focussed on classical stimuli such as gratings and small black objects moving on white monitors. Here I extend previous research, which characterised the behaviour of target tracking neurons in cluttered environments, developing a paradigm to allow numerous properties of targets to be changed while still measuring tracking performance. I show that dragonfly neurons interact with clutter through the previously discovered selective attention system, treating cluttered scenes as collections of target-like features. I further show that this system uses the direction and speed of the target and background as one of the key parameters for tracking success. I also elucidate some additional properties of selective attention including the capacity to select for inhibitory targets or weakly salient features in preference to strongly excitatory ones. In collaboration with colleagues, I have also performed some limited modelling to demonstrate that a selective attention model, which includes switching best explains experimental data. Finally, I explore a mathematical model called divisive normalisation which may partially explain how neurons with large receptive fields can be used to re-establish target position information (lost in a position invariant system) through relatively simple integrations of multiple large receptive field neurons. In summary, my thesis provides a broad investigation into several questions about how dragonflies can function in natural environments. More broadly, my thesis addresses general questions about vision and how complicated visual tasks can be solved via clever strategies employed in neuronal systems and their modelled equivalents.Thesis (Ph.D.) -- University of Adelaide, Adelaide Medical School, 201