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

A predictive focus of gain modulation encodes target trajectories in insect vision

Published: 25 July 2017When a human catches a ball, they estimate future target location based on the current trajectory. How animals, small and large, encode such predictive processes at the single neuron level is unknown. Here we describe small target-selective neurons in predatory dragonflies that exhibit localized enhanced sensitivity for targets displaced to new locations just ahead of the prior path, with suppression elsewhere in the surround. This focused region of gain modulation is driven by predictive mechanisms, with the direction tuning shifting selectively to match the target's prior path. It involves a large local increase in contrast gain which spreads forward after a delay (e.g. an occlusion) and can even transfer between brain hemispheres, predicting trajectories moved towards the visual midline from the other eye. The tractable nature of dragonflies for physiological experiments makes this a useful model for studying the neuronal mechanisms underlying the brain's remarkable ability to anticipate moving stimuli.Steven D Wiederman, Joseph M Fabian, James R Dunbier, David C O'Carrol

Psychological stress modulates synaptic mechanisms for prostaglandin E2-mediated HPA axis activation

Immune-induced activation of the hypothalamic-pituitary-adrenal (HPA) axis elevates glucocorticoids, anti-inflammatory hormones, promoting the effective resolution of inflammation. Psychological stress can modulate this anti-inflammatory mechanism, but the mechanisms underlying this modulation remain largely unknown. The immune-induced HPA axis activation is, in large part, mediated by prostaglandin E2 (PGE2), an inflammatory mediator. In the brain, PGE2 attenuates GABAergic synaptic transmission onto corticotropin-releasing hormone (CRH) neurons in the paraventricular nucleus of the hypothalamus (PVN) that act as the apex of the HPA axis. The removal of GABA-mediated inhibition (i.e. disinhibition) excites CRH neurons and, consequently, activates the HPA axis. Here, we examined the modulatory effects of psychological stress on this PGE2-mediated synaptic mechanism for HPA axis activation. To this end, we used whole-cell patch clamp electrophysiology to record GABAergic synaptic transmission onto PVN-CRH neurons as changes in the amplitude of evoked inhibitory post-synaptic current (eIPSCs). We contrasted findings in acute brain slices from mice that have been stressed by restraint (psychological stress) with those of naïve (non-stressed) mice. We first confirmed that, in slices from naïve mice, PGE2 potently depressed GABAergic synaptic transmission to PVN-CRH neurons. On the other hand, in slices from stressed mice, PGE2 had heterogeneous effects, potentiating some synapses in addition to depressing others. Using receptor subtype-specific agonists and antagonists, we showed that the EP3 subtype of the PGE2 receptor mediated the synaptic depression by inhibiting the release of GABA from the pre-synaptic terminals in naïve slices. On the other hand, the EP2 and EP4 receptors mediated the potentiation of GABA release from the pre-synaptic terminals. Acute stress did not alter these mechanisms for bidirectional synaptic plasticity. By contrast, a blockade of EP1 receptor mimicked the effects of stress, shifting the balance of depression and potentiation toward potentiation. We conclude that EP1 receptor suppresses EP2 and EP4-mediated pre-synaptic potentiation (thus making EP3-mediated depression dominant) and that psychological stress blocks this EP1-mediated mechanism. We propose that psychological stress modulates the interplay between different subtypes of EP receptors to ultimately contribute to altering the immune-induced activation of the HPA axis

Discrimination of features in natural scenes by a dragonfly neuron

Flying insects engage in spectacular high-speed pursuit of targets, requiring visual discrimination of moving objects against cluttered backgrounds. As a first step toward understanding the neural basis for this complex task, we used computational modeling of insect small target motion detector (STMD) neurons to predict responses to features within natural scenes and then compared this with responses recorded from an identified STMD neuron in the dragonfly brain (Hemicordulia tau). A surprising model prediction confirmed by our electrophysiological recordings is that even heavily cluttered scenes contain very few features that excite these neurons, due largely to their exquisite tuning for small features. We also show that very subtle manipulations of the image cause dramatic changes in the response of this neuron, because of the complex inhibitory and facilitatory interactions within the receptive field.Steven D. Wiederman and David C. O'Carrol

Correlation between OFF and ON channels underlies dark target selectivity in an insect visual system

In both vertebrates and invertebrates, evidence supports separation of luminance increments and decrements (ON and OFF channels) in early stages of visual processing (Hartline, 1938; Joesch et al., 2010); however, less is known about how these parallel pathways are recombined to encode form and motion. In Drosophila, genetic knockdown of inputs to putative ON and OFF pathways and direct recording from downstream neurons in the wide-field motion pathway reveal that local elementary motion detectors exist in pairs that separately correlate contrast polarity channels, ON with ON and OFF with OFF (Joesch et al., 2013). However, behavioral responses to reverse-phi motion of discrete features reveal additional correlations of the opposite signs (Clark et al., 2011). We here present intracellular recordings from feature detecting neurons in the dragonfly that provide direct physiological evidence for the correlation of OFF and ON pathways. These neurons show clear polarity selectivity for feature contrast, responding strongly to targets that are darker than the background and only weakly to dark contrasting edges. These dark target responses are much stronger than the linear combination of responses to ON and OFF edges. We compare these data with output from elementary motion detector-based models (Eichner et al., 2011; Clark et al., 2011), with and without stages of strong center-surround antagonism. Our data support an alternative elementary small target motion detector model, which derives dark target selectivity from the correlation of a delayed OFF with an un-delayed ON signal at each individual visual processing unit (Wiederman et al., 2008, 2009).Steven D. Wiederman, Patrick A. Shoemaker and David C. O’Carrol

Facilitation of dragonfly target-detecting neurons by slow moving features on continuous paths

Extent: 29p.Dragonflies detect and pursue targets such as other insects for feeding and conspecific interaction. They have a class of neurons highly specialized for this task in their lobula, the “small target motion detecting” (STMD) neurons. One such neuron, CSTMD1, reaches maximum response slowly over hundreds of milliseconds of target motion. Recording the intracellular response from CSTMD1 and a second neuron in this system, BSTMD1, we determined that for the neurons to reach maximum response levels, target motion must produce sequential local activation of elementary motion detecting elements. This facilitation effect is most pronounced when targets move at velocities slower than what was previously thought to be optimal. It is completely disrupted if targets are instantaneously displaced a few degrees from their current location. Additionally, we utilize a simple computational model to discount the parsimonious hypothesis that CSTMD1's slow build-up to maximum response is due to it incorporating a sluggish neural delay filter. Whilst the observed facilitation may be too slow to play a role in prey pursuit flights, which are typically rapidly resolved, we hypothesize that it helps maintain elevated sensitivity during prolonged, aerobatically intricate conspecific pursuits. Since the effect seems to be localized, it most likely enhances the relative salience of the most recently “seen” locations during such pursuit flights.James R. Dunbier, Steven D. Wiederman, Patrick A. Shoemaker and David C. O’Carrol

Dragonfly Neurons Selectively Attend to Targets Within Natural Scenes

Aerial predators, such as the dragonfly, determine the position and movement of their prey even when both are moving through complex, natural scenes. This task is likely supported by a group of neurons in the optic lobe which respond to moving targets that subtend less than a few degrees. These Small Target Motion Detector (STMD) neurons are tuned to both target size and velocity, whilst also exhibiting facilitated responses to targets traveling along continuous trajectories. When presented with a pair of targets, some STMDs generate spiking activity that represent a competitive selection of one target, as if the alternative does not exist (i.e., selective attention). Here, we describe intracellular responses of CSTMD1 (an identified STMD) to the visual presentation of targets embedded within cluttered, natural scenes. We examine CSTMD1 response changes to target contrast, as well as a range of target and background velocities. We find that background motion affects CSTMD1 responses via the competitive selection between features within the natural scene. Here, robust discrimination of our artificially embedded “target” is limited to scenarios when its velocity is matched to, or greater than, the background velocity. Additionally, the background’s direction of motion affects discriminability, though not in the manner observed in STMDs of other flying insects. Our results highlight that CSTMD1’s competitive responses are to those features best matched to the neuron’s underlying spatiotemporal tuning, whether from the embedded target or other features in the background clutter. In many scenarios, CSTMD1 responds robustly to targets moving through cluttered scenes. However, whether this neuronal system could underlie the task of competitively selecting slow moving prey against fast-moving backgrounds remains an open question.Bernard John Essex Evans, David Charles O, Carroll, Joseph Mahandas Fabian, and Steven D. Wiederma

A Feedback Neural Network for Small Target Motion Detection in Cluttered Backgrounds

Small target motion detection is critical for insects to search for and track mates or prey which always appear as small dim speckles in the visual field. A class of specific neurons, called small target motion detectors (STMDs), has been characterized by exquisite sensitivity for small target motion. Understanding and analyzing visual pathway of STMD neurons are beneficial to design artificial visual systems for small target motion detection. Feedback loops have been widely identified in visual neural circuits and play an important role in target detection. However, if there exists a feedback loop in the STMD visual pathway or if a feedback loop could significantly improve the detection performance of STMD neurons, is unclear. In this paper, we propose a feedback neural network for small target motion detection against naturally cluttered backgrounds. In order to form a feedback loop, model output is temporally delayed and relayed to previous neural layer as feedback signal. Extensive experiments showed that the significant improvement of the proposed feedback neural network over the existing STMD-based models for small target motion detection

A target-detecting visual neuron in the dragonfly locks-on to selectively attended targets

The visual world projects a complex and rapidly changing image onto the retina of many animal species. This presents computational challenges for those animals reliant on visual processing to provide an accurate representation of the world. One such challenge is parsing a visual scene for the most salient targets, such as the selection of prey amidst a swarm. The ability to selectively prioritize processing of some stimuli over others is known as 'selective attention'. We recently identified a dragonfly visual neuron called 'Centrifugal Small Target Motion Detector 1' (CSTMD1) that exhibits selective attention when presented with multiple, equally salient targets. Here we conducted in vivo, electrophysiological recordings from CSTMD1 in wild-caught male dragonflies (Hemicordulia tau), whilst presenting visual stimuli on an LCD monitor. To identify the target selected in any given trial, we uniquely modulated the intensity of the moving targets (frequency-tagging). We found that the frequency information of the selected target is preserved in the neuronal response, whilst the distracter is completely ignored. We also show that the competitive system that underlies selection in this neuron can be biased by the presentation of a preceding target on the same trajectory, even when it is of lower contrast than an abrupt, novel distracter. With this improved method for identifying and biasing target selection in CSTMD1, the dragonfly provides an ideal animal model system to probe the neuronal mechanisms underlying selective attention.Benjamin H. Lancer, Bernard J.E. Evans, Joseph M. Fabian, David C. O’Carroll, and Steven D. Wiederma