ORCID Profile
0000-0002-6020-6348
Current Organisations
Flinders University
,
Uppsala Universitet
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Sensory Systems | Animal Behaviour | Neurosciences | Animal Neurobiology | Zoology | Animal Physiology - Cell | Sensory Systems | Sensory systems | Animal behaviour | Computer Vision | Animal neurobiology | Information Systems Theory | Zoology |
Expanding Knowledge in the Biological Sciences | Air Force | Expanding Knowledge in Psychology and Cognitive Sciences | Application Software Packages (excl. Computer Games) | Expanding Knowledge in the Information and Computing Sciences | Biological sciences | Expanding Knowledge in Technology
Publisher: Frontiers Media SA
Date: 2012
Publisher: Elsevier BV
Date: 04-2012
DOI: 10.1016/J.CONB.2011.12.013
Abstract: Despite being equipped with low-resolution eyes and tiny brains, many insects show exquisite abilities to detect and pursue targets even in highly textured surrounds. Target tracking behavior is subserved by neurons that are sharply tuned to the motion of small high-contrast targets. These neurons respond robustly to target motion, even against self-generated optic flow. A recent model, supported by neurophysiology, generates target selectivity by being sharply tuned to the unique spatiotemporal profile associated with target motion. Target neurons are likely connected in a complex network where some provide more direct output to behavior, whereas others serve an inter-regulatory role. These interactions may regulate attention and aid in the robust detection of targets in clutter observed in behavior.
Publisher: Society for Neuroscience
Date: 29-10-2018
DOI: 10.1523/JNEUROSCI.1695-18.2018
Abstract: For many animals, target motion carries high ecological significance as this may be generated by a predator, prey, or potential mate. Indeed, animals whose survival depends on early target detection are often equipped with a sharply tuned visual system, yielding robust performance in challenging conditions. For ex le, many fast-flying insects use visual cues for identifying targets, such as prey (e.g., predatory dragonflies and robberflies) or conspecifics (e.g., nonpredatory hoverflies), and can often do so against self-generated background optic flow. Supporting these behaviors, the optic lobes of insects that pursue targets harbor neurons that respond robustly to the motion of small moving objects, even when displayed against syn-directional background clutter. However, in diptera, the encoding of target information by the descending neurons, which are more directly involved in generating the behavioral output, has received less attention. We characterized target-selective neurons by recording in the ventral nerve cord of male and female predatory Holcocephala fusca robberflies and of male nonpredatory Eristalis tenax hoverflies. We show that both species have dipteran target-selective descending neurons that only respond to target motion if the background is stationary or moving slowly, moves in the opposite direction, or has un-naturalistic spatial characteristics. The response to the target is suppressed when background and target move at similar velocities, which is strikingly different to the response of target neurons in the optic lobes. As the neurons we recorded from are premotor, our findings affect our interpretation of the neurophysiology underlying target-tracking behaviors. SIGNIFICANCE STATEMENT Many animals use sensory cues to detect moving targets that may represent predators, prey, or conspecifics. For ex le, birds of prey show superb sensitivity to the motion of small prey, and intercept these at high speeds. In a similar manner, predatory insects visually track moving prey, often against cluttered backgrounds. Accompanying this behavior, the brains of insects that pursue targets contain neurons that respond exclusively to target motion. We here show that dipteran insects also have target-selective descending neurons in the part of their nervous system that corresponds to the vertebrate spinal cord. Surprisingly, and in contrast to the neurons in the brain, these premotor neurons are inhibited by background patterns moving in the same direction as the target.
Publisher: Springer Science and Business Media LLC
Date: 06-12-2008
Publisher: Public Library of Science (PLoS)
Date: 08-05-2015
Publisher: The Royal Society
Date: 08-02-2006
Abstract: While predators such as dragonflies are dependent on visual detection of moving prey, social interactions make conspecific detection equally important for many non-predatory insects. Specialized ‘acute zones’ associated with target detection have evolved in several insect groups and are a prominent male-specific feature in many dipteran flies. The physiology of target selective neurons associated with these specialized eye regions has previously been described only from male flies. We show here that female hoverflies ( Eristalis tenax) have several classes of neurons within the third optic ganglion (lobula) capable of detecting moving objects smaller than 1°. These neurons have frontal receptive fields covering a large part of the ipsilateral world and are tuned to a broad range of target speeds and sizes. This could make them suitable for detecting targets under a range of natural conditions such as required during predator avoidance or conspecific interactions.
Publisher: Elsevier BV
Date: 10-2021
DOI: 10.1016/J.CUB.2021.09.016
Abstract: Across the animal kingdom, efference copies of neuronal motor commands are used to ensure our senses ignore stimuli generated by our own actions. New work shows that the underlying motivation for an action affects whether visual neurons are responsive to self-generated stimuli.
Publisher: The Royal Society
Date: 08-02-2006
Abstract: While predators such as dragonflies are dependent on visual detection of moving prey, social interactions make conspecific detection equally important for many non-predatory insects. Specialized ‘acute zones’ associated with target detection have evolved in several insect groups and are a prominent male-specific feature in many dipteran flies. The physiology of target selective neurons associated with these specialized eye regions has previously been described only from male flies. We show here that female hoverflies ( Eristalis tenax) have several classes of neurons within the third optic ganglion (lobula) capable of detecting moving objects smaller than 1°. These neurons have frontal receptive fields covering a large part of the ipsilateral world and are tuned to a broad range of target speeds and sizes. This could make them suitable for detecting targets under a range of natural conditions such as required during predator avoidance or conspecific interactions.
Publisher: Wiley
Date: 13-10-2017
Publisher: The Company of Biologists
Date: 12-2011
DOI: 10.1242/JEB.057539
Abstract: Neural and sensory systems adapt to prolonged stimulation to allow signaling across broader input ranges than otherwise possible with the limited bandwidth of single neurons and receptors. In the visual system, adaptation takes place at every stage of processing, from the photoreceptors that adapt to prevailing luminance conditions, to higher-order motion-sensitive neurons that adapt to prolonged exposure to motion. Recent experiments using dynamic, fluctuating visual stimuli indicate that adaptation operates on a time scale similar to that of the response itself. Further work from our own laboratory has highlighted the role for rapid motion adaptation in reliable encoding of natural image motion. Physiologically, motion adaptation can be broken down into four separate components. It is not clear from the previous studies which of these motion adaptation components are involved in the fast and dynamic response changes. To investigate the adapted response in more detail, we therefore analyzed the effect of motion adaptation using a test–adapt–test protocol with adapting durations ranging from 20 ms to 20 s. Our results underscore the very rapid rate of motion adaptation, suggesting that under free flight, visual motion-sensitive neurons continuously adapt to the changing scenery. This might help explain recent observations of strong invariance in the response to natural scenes with highly variable contrast and image structure.
Publisher: Elsevier BV
Date: 10-2023
Publisher: Proceedings of the National Academy of Sciences
Date: 14-05-2012
Abstract: In higher-order motion stimuli, the direction of object motion does not follow the direction of luminance change. Such stimuli could be generated by the wing movements of a flying butterfly and further complicated by its motion in and out of shadows. Human subjects readily perceive the direction of higher-order motion, although this stands in stark contrast to prevailing motion vision models. Flies and humans compute motion in similar ways, and because flies behaviorally track bars containing higher-order motion cues, they become an attractive model system for investigating the neurophysiology underlying higher-order motion sensitivity. We here use intracellular electrophysiology of motion-vision–sensitive neurons in the hoverfly lobula plate to quantify responses to stimuli containing higher-order motion. We show that motion sensitivity can be broken down into two separate streams, directionally coding for elementary motion and figure motion, respectively, and that responses to Fourier and theta motion can be predicted from these. The sensitivity is affected both by the stimulus’ time course and by the neuron’s underlying receptive field. Responses to preferred-direction theta motion are sexually dimorphic and particularly robust along the visual midline.
Publisher: Elsevier BV
Date: 05-2004
Publisher: Wiley
Date: 27-02-2019
DOI: 10.1111/JSR.12837
Publisher: Elsevier BV
Date: 04-2007
DOI: 10.1016/J.CUB.2007.02.039
Abstract: Despite having tiny brains and relatively low-resolution compound eyes, many fly species frequently engage in precisely controlled aerobatic pursuits of conspecifics. Recent investigations into high-order processing in the fly visual system have revealed a class of neurons, coined small-target-motion detectors (STMDs), capable of responding robustly to target motion against the motion of background clutter. Despite limited spatial acuity in the insect eye, these neurons display exquisite sensitivity to small targets. We recorded intracellularly from morphologically identified columnar neurons in the lobula complex of the hoverfly Eristalis tenax. We show that these columnar neurons with exquisitely small receptive fields, like their large-field counterparts recently described from both male and female flies, have an extreme selectivity for the motion of small targets. In doing so, we provide the first physiological characterization of small-field neurons in female flies. These retinotopically organized columnar neurons include both direction-selective and nondirection-selective classes covering a large area of visual space. The retinotopic arrangement of lobula columnar neurons sensitive to the motion of small targets makes a strong case for these neurons as important precursors in the local processing of target motion. Furthermore, the continued response of STMDs with such small receptive fields to the motion of small targets in the presence of moving background clutter places further constraints on the potential mechanisms underlying their small-target tuning.
Publisher: Proceedings of the National Academy of Sciences
Date: 16-09-2021
Abstract: Target detection in visual clutter is a difficult computational task that insects, with their poor spatial resolution compound eyes and small brains, do successfully and with extremely short behavioral delays. We here show that the responses of target selective descending neurons are attenuated by background motion in the same direction as target motion but facilitated by background motion in the opposite direction. This finding is important for understanding how target pursuit can occur in tandem with gaze stabilization. Indeed, the neural facilitation would come into effect if the hoverfly is subjected to background motion in one direction but the target it is pursuing moves in the opposite direction and could therefore be used to override gaze stabilizing corrective turns.
Publisher: Society for Neuroscience
Date: 11-11-2009
DOI: 10.1523/JNEUROSCI.2857-09.2009
Abstract: Lateral inhibition is perhaps the most ubiquitous of neuronal mechanisms, having been demonstrated in early stages of processing in many different sensory pathways of both mammals and invertebrates. Recent work challenges the long-standing view that assumes that similar mechanisms operate to tune neuronal responses to higher order properties. Scant evidence for lateral inhibition exists beyond the level of the most peripheral stages of visual processing, leading to suggestions that many features of the tuning of higher order visual neurons can be accounted for by the receptive field and other intrinsic coding properties of visual neurons. Using insect target neurons as a model, we present unequivocal evidence that feature tuning is shaped not by intrinsic properties but by potent spatial lateral inhibition operating well beyond the first stages of visual processing. In addition, we present evidence for a second form of higher-order spatial inhibition—a long-range interocular transfer of information that we argue serves a role in establishing interocular rivalry and thus potentially a neural substrate for directing attention to single targets in the presence of distracters. In so doing, we demonstrate not just one, but two levels of spatial inhibition acting beyond the level of peripheral processing.
Publisher: Elsevier BV
Date: 2023
Publisher: The Royal Society
Date: 25-02-2009
Abstract: Motion adaptation is a widespread phenomenon analogous to peripheral sensory adaptation, presumed to play a role in matching responses to prevailing current stimulus parameters and thus to maximize efficiency of motion coding. While several components of motion adaptation (contrast gain reduction, output range reduction and motion after-effect) have been described, previous work is inconclusive as to whether these are separable phenomena and whether they are locally generated. We used intracellular recordings from single horizontal system neurons in the fly to test the effect of local adaptation on the full contrast-response function for stimuli at an unadapted location. We show that contrast gain and output range reductions are primarily local phenomena and are probably associated with spatially distinct synaptic changes, while the antagonistic after-potential operates globally by transferring to previously unadapted locations. Using noise analysis and signal processing techniques to remove ‘spikelets’, we also characterize a previously undescribed alternating current component of adaptation that can explain several phenomena observed in earlier studies.
Publisher: Wiley
Date: 10-2023
DOI: 10.1002/ECE3.10516
Publisher: Cold Spring Harbor Laboratory
Date: 29-07-2022
DOI: 10.1101/2022.07.27.501787
Abstract: The ability to visualize small moving objects is vital for the survival of many animals, as these could represent predators or prey. For ex le, predatory insects, including dragonflies, robber flies and killer flies, perform elegant, high-speed pursuits of both biological and artificial targets. Many non-predatory insects, including male hoverflies and blowflies, also pursue targets during territorial or courtship interactions. To date, most hoverfly pursuits were studied outdoors. To investigate naturalistic hoverfly ( Eristalis tenax ) pursuits under more controlled settings, we constructed an indoor arena that was large enough to encourage naturalistic behavior. We presented artificial beads of different sizes, moving at different speeds, and filmed pursuits with two cameras, allowing subsequent 3D reconstruction of the hoverfly and bead position as a function of time. We show that male E. tenax hoverflies are unlikely to use strict heuristic rules based on angular size or speed to determine when to start pursuit, at least in our indoor setting. We found that hoverflies pursued faster beads when the trajectory involved flying downwards towards the bead. Furthermore, we show that target pursuit behavior can be broken down into two stages. In the first stage the hoverfly attempts to rapidly decreases the distance to the target by intercepting it at high speed. During the second stage the hoverfly’s forward speed is correlated with the speed of the bead, so that the hoverfly remains close, but without catching it. This may be similar to dragonfly shadowing behavior, previously coined ‘motion camouflage’.
Publisher: S. Karger AG
Date: 2015
DOI: 10.1159/000435944
Abstract: Predatory animals have evolved to optimally detect their prey using exquisite sensory systems such as vision, olfaction and hearing. It may not be so surprising that vertebrates, with large central nervous systems, excel at predatory behaviors. More striking is the fact that many tiny insects, with their miniscule brains and scaled down nerve cords, are also ferocious, highly successful predators. For predation, it is important to determine whether a prey is suitable before initiating pursuit. This is paramount since pursuing a prey that is too large to capture, subdue or dispatch will generate a substantial metabolic cost (in the form of muscle output) without any chance of metabolic gain (in the form of food). In addition, during all pursuits, the predator breaks its potential camouflage and thus runs the risk of becoming prey itself. Many insects use their eyes to initially detect and subsequently pursue prey. Dragonflies, which are extremely efficient predators, therefore have huge eyes with relatively high spatial resolution that allow efficient prey size estimation before initiating pursuit. However, much smaller insects, such as killer flies, also visualize and successfully pursue prey. This is an impressive behavior since the small size of the killer fly naturally limits the neural capacity and also the spatial resolution provided by the compound eye. Despite this, we here show that killer flies efficiently pursue natural i (Drosophila melanogaster) /i and artificial (beads) prey. The natural pursuits are initiated at a distance of 7.9 ± 2.9 cm, which we show is too far away to allow for distance estimation using binocular disparities. Moreover, we show that rather than estimating absolute prey size prior to launching the attack, as dragonflies do, killer flies attack with high probability when the ratio of the prey's subtended retinal velocity and retinal size is 0.37. We also show that killer flies will respond to a stimulus of an angular size that is smaller than that of the photoreceptor acceptance angle, and that the predatory response is strongly modulated by the metabolic state. Our data thus provide an exciting ex le of a loosely designed matched filter to i Drosophila /i , but one which will still generate successful pursuits of other suitable prey.
Publisher: MyJove Corporation
Date: 19-05-2018
DOI: 10.3791/57711
Publisher: Frontiers Media SA
Date: 2012
Publisher: Cold Spring Harbor Laboratory
Date: 29-06-2020
DOI: 10.1101/2020.06.28.172536
Abstract: For the human observer, it can be difficult to follow the motion of small objects, especially when they move against background clutter. In contrast, insects efficiently do this, as evidenced by their ability to capture prey, pursue conspecifics, or defend territories, even in highly textured surrounds. We here recorded from target selective descending neurons (TSDNs) which likely subserve these impressive behaviors. To simulate the type of background optic flow that would be generated by the pursuer’s own movements through the world, we used the coherent motion of a perspective distorted sparse dot field. We show that hoverfly TSDN responses to target motion are suppressed when such background optic flow moves in the same direction as the target. Indeed, the neural responses are strongly attenuated against both translational sideslip as well as rotational yaw. More strikingly, we show that TSDNs are facilitated by background optic flow in the opposite direction to the target, if the target moves horizontally. Furthermore, we show that a small, frontal spatial window of background optic flow is enough to fully facilitate or attenuate TSDN responses to target motion. We argue that the TSDN response facilitation could be beneficial in modulating corrective turns during target pursuit. Target detection in visual clutter is a difficult computational task that insects, with their poor resolution compound eyes and small brains, do successfully and with extremely short behavioral delays. We here show that the responses of target selective descending neurons are attenuated by background motion in the same direction as target motion, but facilitated by opposite direction background motion. This finding is important for understanding conspecific pursuit behavior, since these descending neurons likely control behavioral output. The facilitation that we describe would come into effect if the hoverfly is subjected to background motion in one direction, but the target it is pursuing moves in the opposite direction, and could therefore be used to modulate gaze stabilizing corrective turns.
Publisher: The Royal Society
Date: 12-10-2009
Abstract: Vertebrate cones and rods in several cases use separate but related components for their signal transduction (opsins, G-proteins, ion channels, etc.). Some of these proteins are also used differentially in other cell types in the retina. Because cones, rods and other retinal cell types originated in early vertebrate evolution, it is of interest to see if their specific genes arose in the extensive gene duplications that took place in the ancestor of the jawed vertebrates (gnathostomes) by two tetraploidizations (genome doublings). The ancestor of teleost fishes subsequently underwent a third tetraploidization. Our previously reported analyses showed that several gene families in the vertebrate visual phototransduction cascade received new members in the basal tetraploidizations. We here expand these data with studies of additional gene families and vertebrate species. We conclude that no less than 10 of the 13 studied phototransduction gene families received additional members in the two basal vertebrate tetraploidizations. Also the remaining three families seem to have undergone duplications during the same time period but it is unclear if this happened as a result of the tetraploidizations. The implications of the many early vertebrate gene duplications for functional specialization of specific retinal cell types, particularly cones and rods, are discussed.
Publisher: Elsevier BV
Date: 12-2017
DOI: 10.1016/J.COIS.2017.08.002
Abstract: Natural scenes may appear random, but are not only constrained in space and time, but also show strong spatial and temporal correlations. Spatial constraints and correlations can be described by quantifying image statistics, which include intuitive measures such as contrast, color and luminance, but also parameters that need some type of transformation of the image. In this review we will discuss some common tools used to quantify spatial and temporal parameters of naturalistic visual input, and how these tools have been used to inform us about visual processing in insects. In particular, we will review findings that would not have been possible using conventional, experimenter defined stimuli.
Publisher: Elsevier BV
Date: 05-2008
DOI: 10.1016/J.CUB.2008.03.061
Abstract: Many insects perform high-speed aerial maneuvers in which they navigate through visually complex surrounds. Among insects, hoverflies stand out, with males switching from stationary hovering to high-speed pursuit at extreme angular velocities [1]. In dipterans, 50-60 large interneurons -- the lobula-plate tangential cells (LPTCs) -- detect changes in optic flow experienced during flight [2-5]. It has been predicted that large LPTC receptive fields are a requirement of accurate "matched filters" of optic flow [6]. Whereas many fly taxa have three horizontal system (HS) LPTC neurons in each hemisphere, hoverflies have four [7], possibly reflecting the more sophisticated flight behavior. We here show that the most dorsal hoverfly neuron (HS north [HSN]) is sexually dimorphic, with the male receptive field substantially smaller than in females or in either sex of blowflies. The (hoverfly-specific) HSN equatorial (HSNE) is, however, sexually isomorphic. Using complex optic flow, we show that HSN, despite its smaller receptive field, codes yaw velocity as well as HSNE. Responses to a target moving against a plain or textured background suggest that the male HSN could potentially play a role in target pursuit under some conditions.
Publisher: Elsevier BV
Date: 08-2013
DOI: 10.1016/J.CUB.2013.06.009
Abstract: Visual systems adapt rapidly to objects moving repeatedly within the visual field, because such objects are likely irrelevant. In the crab, the neural switch for such adaptation has been found to take place at a surprisingly early stage of the visual processing pathway.
Publisher: Elsevier BV
Date: 12-2016
DOI: 10.1016/J.CONB.2016.09.001
Abstract: Motion vision provides important cues for many tasks. Flying insects, for ex le, may pursue small, fast moving targets for mating or feeding purposes, even when these are detected against self-generated optic flow. Since insects are small, with size-constrained eyes and brains, they have evolved to optimize their optical, neural and behavioral target visualization solutions. Indeed, even if evolutionarily distant insects display different pursuit strategies, target neuron physiology is strikingly similar. Furthermore, the coarse spatial resolution of the insect compound eye might actually be beneficial when it comes to detection of moving targets. In conclusion, tiny insects show higher than expected performance in target visualization tasks.
Publisher: Elsevier BV
Date: 2013
Publisher: The Royal Society
Date: 26-01-2011
Abstract: Many animals visualize and track small moving targets at long distances—be they prey, approaching predators or conspecifics. Insects are an excellent model system for investigating the neural mechanisms that have evolved for this challenging task. Specialized small target motion detector (STMD) neurons in the optic lobes of the insect brain respond strongly even when the target size is below the resolution limit of the eye. Many STMDs also respond robustly to small targets against complex stationary or moving backgrounds. We hypothesized that this requires a complex mechanism to avoid breakthrough responses by background features, and yet to adequately lify the weak signal of tiny targets. We compared responses of dragonfly STMD neurons to small targets that begin moving within the receptive field with responses to targets that approach the same location along longer trajectories. We find that responses along longer trajectories are strongly facilitated by a mechanism that builds up slowly over several hundred milliseconds. This allows the neurons to give sustained responses to continuous target motion, thus providing a possible explanation for their extraordinary sensitivity.
Publisher: Elsevier BV
Date: 07-2009
DOI: 10.1016/J.TINS.2009.03.004
Abstract: Discerning a target amongst visual 'clutter' is a complicated task that has been elegantly solved by flying insects, as evidenced by their mid-air interactions with conspecifics and prey. The neurophysiology of small-target motion detectors (STMDs) underlying these complex behaviors has recently been described and suggests that insects use mechanisms similar to those of hypercomplex cells of the mammalian visual cortex to achieve target-specific tuning. Cortical hypercomplex cells are end-stopped, which means that they respond optimally to small moving targets, with responses to extended bars attenuated. We review not only the underlying mechanisms involved in this tuning but also how recently proposed models provide a possible explanation for another remarkable property of these neurons - their ability to respond robustly to the motion of targets even against moving backgrounds.
Publisher: IEEE
Date: 10-2014
Publisher: The Company of Biologists
Date: 12-2021
DOI: 10.1242/JEB.242833
Abstract: When animals move through the world, their own movements generate widefield optic flow across their eyes. In insects, such widefield motion is encoded by optic lobe neurons. These lobula plate tangential cells (LPTCs) synapse with optic flow-sensitive descending neurons, which in turn project to areas that control neck, wing and leg movements. As the descending neurons play a role in sensorimotor transformation, it is important to understand their spatio-temporal response properties. Recent work shows that a relatively fast and efficient way to quantify such response properties is to use m-sequences or other white noise techniques. Therefore, here we used m-sequences to quantify the impulse responses of optic flow-sensitive descending neurons in male Eristalis tenax hoverflies. We focused on roll impulse responses as hoverflies perform exquisite head roll stabilizing reflexes, and the descending neurons respond particularly well to roll. We found that the roll impulse responses were fast, peaking after 16.5–18.0 ms. This is similar to the impulse response time to peak (18.3 ms) to widefield horizontal motion recorded in hoverfly LPTCs. We found that the roll impulse response litude scaled with the size of the stimulus impulse, and that its shape could be affected by the addition of constant velocity roll or lift. For ex le, the roll impulse response became faster and stronger with the addition of excitatory stimuli, and vice versa. We also found that the roll impulse response had a long return to baseline, which was significantly and substantially reduced by the addition of either roll or lift.
Publisher: Proceedings of the National Academy of Sciences
Date: 24-12-2013
Publisher: Springer Science and Business Media LLC
Date: 28-01-2020
DOI: 10.1007/S00359-020-01402-0
Abstract: Many animals use motion vision information to control dynamic behaviors. For ex le, flying insects must decide whether to pursue a prey or not, to avoid a predator, to maintain their current flight trajectory, or to land. The neural mechanisms underlying the computation of visual motion have been particularly well investigated in the fly optic lobes. However, the descending neurons, which connect the optic lobes with the motor command centers of the ventral nerve cord, remain less studied. To address this deficiency, we describe motion vision sensitive descending neurons in the hoverfly Eristalis tenax . We describe how the neurons can be identified based on their receptive field properties, and how they respond to moving targets, looming stimuli and to widefield optic flow. We discuss their similarities with previously published visual neurons, in the optic lobes and ventral nerve cord, and suggest that they can be classified as target-selective, looming sensitive and optic flow sensitive, based on these similarities. Our results highlight the importance of using several visual stimuli as the neurons can rarely be identified based on only one response characteristic. In addition, they provide an understanding of the neurophysiology of visual neurons that are likely to affect behavior.
Publisher: Elsevier BV
Date: 07-2020
Publisher: Proceedings of the National Academy of Sciences
Date: 27-11-2017
Abstract: The coeveolution of flowers and pollinators is well known, but how generalist pollinators identify suitable flowers across environments and flower species is not well understood. Hoverflies, which are found across the globe, are one of the most important alternative pollinators after bees and bumblebees. Here we measured, predicted, and finally recreated multimodal cues from in idual flowers visited by hoverflies in three different environments (hemiboreal, alpine, and tropical). We found that although “flower signatures” were unique for each environment, some cues were ubiquitously attractive, despite not resembling cue combinations from real flowers. Our results provide unique insights into how a cosmopolitan pollinator identifies flower objects across environments, which has important implications for our understanding of pollination as a global ecological service.
Publisher: The Company of Biologists
Date: 15-02-2023
DOI: 10.1242/JEB.244895
Abstract: The ability to visualize small moving objects is vital for the survival of many animals, as these could represent predators or prey. For ex le, predatory insects, including dragonflies, robber flies and killer flies, perform elegant, high-speed pursuits of both biological and artificial targets. Many non-predatory insects, including male hoverflies and blowflies, also pursue targets during territorial or courtship interactions. To date, most hoverfly pursuits have been studied outdoors. To investigate hoverfly (Eristalis tenax) pursuits under more controlled settings, we constructed an indoor arena that was large enough to encourage naturalistic behavior. We presented artificial beads of different sizes, moving at different speeds, and filmed pursuits with two cameras, allowing subsequent 3D reconstruction of the hoverfly and bead position as a function of time. We show that male E. tenax hoverflies are unlikely to use strict heuristic rules based on angular size or speed to determine when to start pursuit, at least in our indoor setting. We found that hoverflies pursued faster beads when the trajectory involved flying downwards towards the bead. Furthermore, we show that target pursuit behavior can be broken down into two stages. In the first stage, the hoverfly attempts to rapidly decreases the distance to the target by intercepting it at high speed. During the second stage, the hoverfly's forward speed is correlated with the speed of the bead, so that the hoverfly remains close, but without catching it. This may be similar to dragonfly shadowing behavior, previously coined ‘motion camouflage’.
Publisher: IEEE
Date: 12-2014
Publisher: Frontiers Media SA
Date: 2013
Publisher: Frontiers Media SA
Date: 2012
Publisher: Elsevier BV
Date: 06-2010
DOI: 10.1016/J.CUB.2010.03.072
Abstract: Estimating relative velocity in the natural environment is challenging because natural scenes vary greatly in contrast and spatial structure. Widely accepted correlation-based models for elementary motion detectors (EMDs) are sensitive to contrast and spatial structure and consequently generate ambiguous estimates of velocity. Identified neurons in the third optic lobe of the hoverfly can reliably encode the velocity of natural images largely independent of contrast, despite receiving inputs directly from arrays of such EMDs. This contrast invariance suggests an important role for additional neural processes in robust encoding of image motion. However, it remains unclear which neural processes are contributing to contrast invariance. By recording from horizontal system neurons in the hoverfly lobula, we show two activity-dependent adaptation mechanisms acting as near-ideal normalizers for images of different contrasts that would otherwise produce highly variable response magnitudes. Responses to images that are initially weak neural drivers are boosted over several hundred milliseconds. Responses to images that are initially strong neural drivers are reduced over longer time scales. These adaptation mechanisms appear to be matched to higher-order natural image statistics reconciling the neurons' accurate encoding of image velocity with the inherent ambiguity of correlation-based motion detectors.
Publisher: The Company of Biologists
Date: 15-09-2007
DOI: 10.1242/JEB.008425
Abstract: Visual identification of targets is an important task for many animals searching for prey or conspecifics. Dragonflies utilize specialized optics in the dorsal acute zone, accompanied by higher-order visual neurons in the lobula complex, and descending neural pathways tuned to the motion of small targets. While recent studies describe the physiology of insect small target motion detector (STMD) neurons, little is known about the mechanisms that underlie their exquisite sensitivity to target motion. Lobula plate tangential cells (LPTCs), a group of neurons in dipteran flies selective for wide-field motion, have been shown to take input from local motion detectors consistent with the classic correlation model developed by Hassenstein and Reichardt in the 1950s. We have tested the hypothesis that similar mechanisms underlie the response of dragonfly STMDs. We show that an anatomically characterized centrifugal STMD neuron (CSTMD1) gives responses that depend strongly on target contrast, a clear prediction of the correlation model. Target stimuli are more complex in spatiotemporal terms than the sinusoidal grating patterns used to study LPTCs, so we used a correlation-based computer model to predict response tuning to velocity and width of moving targets. We show that increasing target width in the direction of travel causes a shift in response tuning to higher velocities, consistent with our model. Finally, we show how the morphology of CSTMD1 allows for impressive spatial interactions when more than one target is present in the visual field.
Publisher: Springer International Publishing
Date: 13-10-2015
DOI: 10.1007/978-3-319-10984-8_5
Abstract: The classical Hassenstein-Reichardt mathematical elementary motion detector (EMD) model is treated analytically. The EMD is stimulated with drifting sinusoidal gratings, which are often used in motion vision research, thus enabling direct comparison with neural responses from motion-sensitive neurones in the fly brain. When sinusoidal gratings are displayed on a cathode ray tube monitor, they are modulated by the refresh rate of the monitor. This generates a pulsatile signature of the visual stimulus, which is also seen in the neural response. Such pulsatile signals make a Laguerre domain identification method for estimating the parameters of a single EMD suitable, allowing estimation of both finite and infinite-dimensional dynamics. To model the response of motion-sensitive neurones with large receptive fields, a pool of spatially distributed EMDs is considered, with the weights of the contributing EMDs fitted to the neural data by a sparse estimation method. Such an EMD-array is more reliably estimated by stimulating with multiple sinusoidal gratings, since these provide higher spatial excitation than a single sinusoidal grating. Consequently, a way of designing the visual stimuli for a certain order of spatial resolution is suggested.
Publisher: Society for Neuroscience
Date: 22-05-2013
DOI: 10.1523/JNEUROSCI.5713-12.2013
Abstract: Many animals use visual motion cues for navigating within their surroundings. Both flies and vertebrates compute local motion by temporal correlation of neighboring photoreceptors, via so-called elementary motion detectors (EMDs). In the fly lobula plate and the vertebrate visual cortex the output from many EMDs is pooled in neurons sensitive to wide-field optic flow. Although the EMD has been the preferred model for more than 50 years, recent work has highlighted its limitations in describing some visual behaviors, such as responses to higher-order motion stimuli. Non-EMD motion processing may therefore serve an important function in vision. Here, we describe a novel neuron class in the fly lobula plate that clearly does not derive its input from classic EMDs. The centrifugal stationary inhibited flicker excited (cSIFE) neuron is strongly excited by flicker, up to very high temporal frequencies. The non-EMD driven flicker sensitivity leads to strong, nondirectional responses to high-speed, wide-field motion. Furthermore, cSIFE is strongly inhibited by stationary patterns, within a narrow wavelength band. cSIFE's outputs overlap with the inputs of well described optic flow-sensitive lobula plate tangential cells (LPTCs). Driving cSIFE affects the active dendrites of LPTCs, and cSIFE may therefore play a large role in motion vision.
Publisher: Journal of Integrative Bioinformatics
Date: 2007
Publisher: IEEE
Date: 12-2011
Publisher: Springer Science and Business Media LLC
Date: 06-10-2015
DOI: 10.1038/NCOMMS9522
Abstract: Animal sensory systems are optimally adapted to those features typically encountered in natural surrounds, thus allowing neurons with limited bandwidth to encode challengingly large input ranges. Natural scenes are not random, and peripheral visual systems in vertebrates and insects have evolved to respond efficiently to their typical spatial statistics. The mammalian visual cortex is also tuned to natural spatial statistics, but less is known about coding in higher order neurons in insects. To redress this we here record intracellularly from a higher order visual neuron in the hoverfly. We show that the cSIFE neuron, which is inhibited by stationary images, is maximally inhibited when the slope constant of the litude spectrum is close to the mean in natural scenes. The behavioural optomotor response is also strongest to images with naturalistic image statistics. Our results thus reveal a close coupling between the inherent statistics of natural scenes and higher order visual processing in insects.
Publisher: Springer Science and Business Media LLC
Date: 04-2019
Publisher: Springer Science and Business Media LLC
Date: 26-11-2016
Publisher: Elsevier BV
Date: 03-2017
Publisher: Association for Research in Vision and Ophthalmology (ARVO)
Date: 27-12-2011
DOI: 10.1167/11.14.20
Abstract: As a consequence of the non-linear correlation mechanism underlying motion detection, the variability in local pattern structure and contrast inherent within natural scenes profoundly influences local motion responses. To accurately interpret optic flow induced by self-motion, neurons in many dipteran flies smooth this "pattern noise" by wide-field spatial integration. We investigated the role that size and shape of the receptive field plays in smoothing out pattern noise in two unusual hoverfly optic flow neurons: one (HSN) with an exceptionally small receptive field and one (HSNE) with a larger receptive field. We compared the local and global responses to a sequence of panoramic natural images in these two neurons with a parsimonious model for elementary motion detection weighted for their spatial receptive fields. Combined with manipulation of size and contrast of the stimulus images, this allowed us to separate spatial integration properties arising from the receptive field, from other local and global non-linearities, such as motion adaptation and dendritic gain control. We show that receptive field properties alone are poor predictors of the response to natural scenes. If anything, additional non-linearity enhances the pattern dependence of HSN's response, particularly to vertically elongated features, suggesting that it may serve a role in forward fixation during hovering.
Publisher: The Company of Biologists
Date: 2018
DOI: 10.1242/JEB.177162
Abstract: On warm sunny days female hoverflies are often observed feeding from a wide range of wild and cultivated flowers. In doing so, hoverflies serve a vital role as alternative pollinators, and suggested to be the most important after bees and bumblebees. Unless the flower hoverflies are feeding from is large, they do not readily share the space with other insects, but instead opt to leave. We have used high-speed videography followed by 3D reconstruction of flight trajectories to quantify how female Eristalis hoverflies respond to approaching bees, wasps and two different hoverfly species. We found that in 94% of the interactions the occupant female left the flower when approached by another insect. We found that compared to spontaneous take-offs, the occupant hoverfly's escape response was performed at ∼3 times higher speed (spontaneous take-off at 0.2±0.05 m/s compared with 0.55±0.08 m/s when approached by another Eristalis). The hoverflies tended to take off upward and forward, while taking the incomer's approach angle into account. Intriguingly, we found when approached by wasps that the occupant Eristalis took off at a higher speed and when the wasp was further away. This suggests that feeding hoverflies may be able to distinguish these predators, demanding impressive visual capabilities. Our results, including quantification of the visual information available before occupant take-off, provide important insight into how freely behaving hoverflies perform escape responses from competitors and predators (e.g. wasps) in the wild.
Publisher: Public Library of Science (PLoS)
Date: 07-02-2006
Publisher: Cold Spring Harbor Laboratory
Date: 21-10-2022
DOI: 10.1101/2022.10.19.512946
Abstract: Responding rapidly to visual stimuli is fundamental for many animals. For ex le, predatory birds and insects alike have amazing target detection abilities, with incredibly short neural and behavioral delays, enabling efficient prey capture. Similarly, looming objects need to be rapidly avoided to ensure immediate survival, as these could represent approaching predators. Male Eristalis tenax hoverflies are non-predatory, highly territorial insects, that perform high-speed pursuits of conspecifics and other territorial intruders. During the initial stages of the pursuit the retinal projection of the target is very small, but grows to a larger object before physical interaction. Supporting such behaviors, E. tenax and other insects have both target-tuned and loom-sensitive neurons in the optic lobes and the descending pathways. We here show that these visual stimuli are not necessarily encoded in parallel. Indeed, we describe a class of descending neurons that respond to small targets, to looming and to widefield stimuli. We show that these neurons have two distinct receptive fields where the dorsal receptive field is sensitive to the motion of small targets and the ventral receptive field responds to larger objects or widefield stimuli. Our data suggest that the two receptive fields have different pre-synaptic input, where the inputs are not linearly summed. This novel and unique arrangement could support different behaviors, including obstacle avoidance, flower landing, target pursuit or capture. If you are playing baseball, when the ball is far away, it appears as a very small object on your retina. However, as the ball gets closer, its image becomes a rapidly expanding object. Here, we show that within the hoverfly visual system, a single neuron could respond to both of these images. Indeed, we found a class of descending neurons with dual sensitivity, separated into two distinct parts of the visual field. The neurons have a more dorsal receptive field that is sensitive to small targets and a more ventral receptive field that is sensitive to larger objects.
Publisher: Cold Spring Harbor Laboratory
Date: 05-05-2023
DOI: 10.1101/2023.05.03.539331
Abstract: Many animals use motion vision information to control dynamic behaviors. Predatory animals, for ex le, show an exquisite ability to detect rapidly moving prey followed by pursuit and capture. Such target detection is not only used by predators but can also play an important role in conspecific interactions. Male hoverflies ( Eristalis tenax ), for ex le, vigorously defend their territories against conspecific intruders. Visual target detection is believed to be subserved by specialized target tuned neurons that are found in a range of species, including cats, zebrafish, and insects. However, how these target-tuned neurons respond to actual pursuit trajectories is currently not well understood. To redress his, we recorded extracellularly from target selective descending neurons (TSDNs) in male Eristalis tenax hoverflies. We show that the neurons have dorso-frontal receptive fields, with a preferred direction up and away from the visual midline. We next reconstructed visual flow-fields as experienced during pursuits of artificial targets (black beads). We recorded TSDN responses to six reconstructed pursuits and found that each neuron responded consistently at remarkably specific time points, but that these time points differed between neurons. We compared the observed spike probability with the spike probability predicted from each neuron’s receptive field and size tuning, and found a correlation coefficient of 0.35. Interestingly, however, the overall response rate was low, with in idual neurons responding to only a small part of each reconstructed pursuit. In contrast, the TSDN population responded to a substantially larger proportion of the pursuits (up to a median of 23%). This large variation between neurons could be useful if different neurons control different parts of the behavioral output. Descending neurons constitute less than 1% of the nervous system, yet have to convey all requisite information from the brain to the body. They are therefore a crucial bottleneck in sensorimotor transformation. Descending target tuned neurons in male hoverflies ( Eristalis tenax) , for ex le, are believed to play a key role in territory defense and pursuit of conspecifics. However, this has not been tested using visual stimuli resembling reconstructed target pursuits. We here found that the observed neural responses to reconstructed pursuits are stronger than those predicted from responses to simpler stimuli. In addition, while the responses to simple stimuli suggested a homogenous population of neurons, the reconstructed pursuits showed important differences between in idual neurons. Our data thus highlight the need for using more naturalistic stimuli when deciphering neural function.
Publisher: Elsevier BV
Date: 11-2003
DOI: 10.1016/S0378-1119(03)00812-6
Abstract: Pax transcription factors are found in animals, from simple sponges to insects and vertebrates. The defining feature of Pax proteins is the DNA-binding paired domain (PD), which consists of two helix-turn-helix subdomains, joined with a linker region. Despite high specificity in vivo, the paired domains of different Pax proteins bind similar consensus DNA sequences in vitro. Using bandshift techniques, we show here that the paired domain of the Acropora millepora PaxD protein, which unambiguously belongs to the Pax3/7 group, does not bind to three defined paired domain-binding sites. Domain swapping experiments and site-directed mutagenesis identified two amino acid residues in the linker region of the paired domain as critical to DNA binding G70 and S71 are highly conserved in Pax proteins, but differ in PaxD (L70 and N71). The PaxD data thus highlight the importance of the linker region, and particularly G70 and S71, in DNA binding by Pax proteins.
Start Date: 2019
End Date: 2020
Funder: United States Air Force
View Funded ActivityStart Date: 2022
End Date: 2024
Funder: Swedish Research Council for Environment Agricultural Sciences and Spatial Planning
View Funded ActivityStart Date: 2008
End Date: 2010
Funder: Australian Research Council
View Funded ActivityStart Date: 2021
End Date: 2023
Funder: Australian Research Council
View Funded ActivityStart Date: 2019
End Date: 2023
Funder: Australian Research Council
View Funded ActivityStart Date: 2008
End Date: 2010
Funder: Australian Research Council
View Funded ActivityStart Date: 2009
End Date: 2011
Funder: Australian Research Council
View Funded ActivityStart Date: 2018
End Date: 2020
Funder: Australian Research Council
View Funded ActivityStart Date: 2017
End Date: 2019
Funder: Australian Research Council
View Funded ActivityStart Date: 2014
End Date: 2016
Funder: Stiftelsen Olle Engkvist Byggmästare
View Funded ActivityStart Date: 2015
End Date: 2018
Funder: Air Force Office of Scientific Research
View Funded ActivityStart Date: 2016
End Date: 2018
Funder: Stiftelsen Olle Engkvist Byggmästare
View Funded ActivityStart Date: 2008
End Date: 12-2010
Amount: $238,648.00
Funder: Australian Research Council
View Funded ActivityStart Date: 05-2021
End Date: 05-2024
Amount: $532,789.00
Funder: Australian Research Council
View Funded ActivityStart Date: 05-2023
End Date: 06-2026
Amount: $591,950.00
Funder: Australian Research Council
View Funded ActivityStart Date: 06-2019
End Date: 06-2023
Amount: $978,125.00
Funder: Australian Research Council
View Funded ActivityStart Date: 02-2017
End Date: 06-2019
Amount: $325,000.00
Funder: Australian Research Council
View Funded ActivityStart Date: 2018
End Date: 02-2021
Amount: $475,383.00
Funder: Australian Research Council
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