Target detection in insects: optical, neural and behavioral optimizations.

This is the final version of the article. It first appeared from Elsevier via https://doi.org/10.1016/j.conb.2016.09.001Motion vision provides important cues for many tasks. Flying insects, for example, 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.Air Force Office of Scientific Research (Grant ID: FA9550-15-1-0188

Visual approach computation in feeding hoverflies.

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 are suggested to be the most important pollinators 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 if another insect approaches. We 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 with 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-1 compared with 0.55±0.08 m s-1 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 that, when approached by wasps, 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.This work was funded by the Air Force Office of Scientific Research (FA9550-15-1-0188 to P.T. Gonzalez-Bellido and K. Nordström), the Biotechnology and Biological Sciences Research Council (BB/L024667/1 David Phillips Fellowship to T. Wardill), Australian Research Council (DP170100008), Stiftelsen Olle Engkvist Byggmästare (2016/348) and Stiftelsen Längmanska Kulturfonden (BA17-0812)

Neural control of tuneable skin iridescence in squid

In addition to the Introduction readme document, find also the Materials and Methods readme document that describes the methods used to collect the data for this paper. The final readme, File Descriptions, describes how the files are arranged in various Zip files. The data within these zip files should be considered the gold standard data, although considerably more data exists than is reported in this repository. Please contact the authors directly ([email protected] and [email protected]) for any additional data.Fast dynamic control of skin coloration is rare in the animal kingdom, whether it be pigmentary or structural. Iridescent structural coloration results when nanoscale structures disrupt incident light and selectively reflect specific colours. Unlike animals with fixed iridescent coloration (e.g. butterflies), squid iridophores (i.e. aggregations of iridescent cells in the skin), produce dynamically tuneable structural coloration, as exogenous application of acetylcholine (ACh) changes the colour and brightness output. Previous efforts to stimulate iridophores neurally or to identify the source of endogenous ACh were unsuccessful, leaving researchers to question the activation mechanism. We developed a novel neurophysiological preparation in the squid Doryteuthis pealeii and demonstrated that electrical stimulation of neurons in the skin shifts the spectral peak of the reflected light to shorter wavelengths (>145 nm) and increases the peak reflectance (>245 %) of innervated iridophores. We show ACh is released within the iridophore layer and that extensive nerve branching is seen within the iridophore. The dynamic colour shift is significantly faster (17 s) than the peak reflectance increase (32 s) revealing two distinct mechanisms. Responses from a structurally altered preparation indicate that the reflectin protein condensation mechanism explains peak reflectance change, while an undiscovered mechanism causes the fast colour shift

Expression of squid iridescence depends on environmental luminance and peripheral ganglion control

Author Posting. © The Author(s), 2013. This is the author's version of the work. It is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 217 (2014):850-858, doi:10.1242/​jeb.091884.Squids display impressive changes in body coloration that are afforded by two types of dynamic skin elements: structural iridophores (which produce iridescence) and pigmented chromatophores. Both color elements are neurally controlled, but nothing is known about the iridescence circuit, or the environmental cues, that elicit iridescence expression. To tackle this knowledge gap, we performed denervation, electrical stimulation and behavioral experiments using the long-fin squid, Doryteuthis pealeii. We show that while the pigmentary and iridescence circuits originate in the brain, they are wired differently in the periphery: (i) the iridescence signals are routed through a peripheral center called the stellate ganglion and (ii) the iridescence motorneurons likely originate within this ganglion (as revealed by nerve fluorescence dye fills). Cutting the inputs to the stellate ganglion that descend from the brain shifts highly reflective iridophores into a transparent state. Taken together, these findings suggest that although brain commands are necessary for expression of iridescence, integration with peripheral information in the stellate ganglion could modulate the final output. We also demonstrate that squids change their iridescence brightness in response to environmental luminance; such changes are robust but slow (minutes to hours). The squid's ability to alter its iridescence levels may improve camouflage under different lighting intensities.This research was supported by the ONR Basic Research Challenge grant no. N00014-10-1-0989 and by the AFOSR grant FA9950090346.2015-03-1

The Killer Fly Hunger Games: Target Size and Speed Predict Decision to Pursuit.

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 (Drosophila melanogaster) 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 example of a loosely designed matched filter to Drosophila, but one which will still generate successful pursuits of other suitable prey.This work was funded the Air force Office of Scientific Research (FA9550-10-0472 to Prof. Robert Olberg). An Isaac Newton Trust / Wellcome Trust ISSF / University of Cambridge Joint Research Grant to Gonzalez-Bellido. BBSRC TO TREVOR WARDILL The Swedish Research Council (2012-4740) to Nordström and a Shared Equipment Grant from the School of Biological Sciences (U. of Cambridge).This is the final version of the article. It first appeared from Karger via http://dx.doi.org/10.1159/00043594

The killer fly hunger games : target size and speed predict decision to pursuit

© The Author(s), 2015. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Brain, Behavior and Evolution 86 (2015): 28-27, doi:10.1159/000435944.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 (Drosophila melanogaster) 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 example of a loosely designed matched filter to Drosophila, but one which will still generate successful pursuits of other suitable prey.This work was funded by the Air Force Office of Scientific Research (FA9550-10-0472 to R.M. Olberg and FA9550-15-1-0188 to P.T. Gonzalez-Bellido and K. Nordström), an Isaac Newton Trust/Wellcome Trust ISSF/University of Cambridge Joint Research Grant to Paloma T. Gonzalez-Bellido, a Biotechnology and Biological Sciences Research Council David Phillips Fellowship (BBSRC, BB/L024667/1) to Trevor J. Wardill, the Swedish Research Council (2012-4740) to Karin Nordström and a Shared Equipment Grant from the School of Biological Sciences (University of Cambridge)

Binocular Encoding in the Damselfly Pre-motor Target Tracking System.

Akin to all damselflies, Calopteryx (family Calopterygidae), commonly known as jewel wings or demoiselles, possess dichoptic (separated) eyes with overlapping visual fields of view. In contrast, many dragonfly species possess holoptic (dorsally fused) eyes with limited binocular overlap. We have here compared the neuronal correlates of target tracking between damselfly and dragonfly sister lineages and linked these changes in visual overlap to pre-motor neural adaptations. Although dragonflies attack prey dorsally, we show that demoiselles attack prey frontally. We identify demoiselle target-selective descending neurons (TSDNs) with matching frontal visual receptive fields, anatomically and functionally homologous to the dorsally positioned dragonfly TSDNs. By manipulating visual input using eyepatches and prisms, we show that moving target information at the pre-motor level depends on binocular summation in demoiselles. Consequently, demoiselles encode directional information in a binocularly fused frame of reference such that information of a target moving toward the midline in the left eye is fused with information of the target moving away from the midline in the right eye. This contrasts with dragonfly TSDNs, where receptive fields possess a sharp midline boundary, confining responses to a single visual hemifield in a sagittal frame of reference (i.e., relative to the midline). Our results indicate that, although TSDNs are conserved across Odonata, their neural inputs, and thus the upstream organization of the target tracking system, differ significantly and match divergence in eye design and predatory strategies. VIDEO ABSTRACT

Neural Control of Dynamic 3-Dimensional Skin Papillae for Cuttlefish Camouflage

Summary: The color and pattern changing abilities of octopus, squid, and cuttlefish via chromatophore neuro-muscular organs are unparalleled. Cuttlefish and octopuses also have a unique muscular hydrostat system in their skin. When this system is expressed, dermal bumps called papillae disrupt body shape and imitate the fine texture of surrounding objects, yet the control system is unknown. Here we report for papillae: (1) the motoneurons and the neurotransmitters that control activation and relaxation, (2) a physiologically fast expression and retraction system, and (3) a complex of smooth and striated muscles that enables long-term expression of papillae through sustained tension in the absence of neural input. The neural circuits controlling acute shape-shifting skin papillae in cuttlefish show homology to the iridescence circuits in squids. The sustained tension in papillary muscles for long-term camouflage utilizes muscle heterogeneity and points toward the existence of a “catch-like” mechanism that would reduce the necessary energy expenditure. : Animal Physiology; Neuroanatomy; Evolutionary Biology Subject Areas: Animal Physiology, Neuroanatomy, Evolutionary Biolog

Data from: Visual approach computation in feeding hoverflies

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 ca. 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