Gonzalez-Bellido Paloma T.

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Gonzalez-Bellido
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Paloma T.
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  • Preprint
    Expression of squid iridescence depends on environmental luminance and peripheral ganglion control
    ( 2013-10) Gonzalez-Bellido, Paloma T. ; Wardill, Trevor J. ; Buresch, Kendra C. ; Ulmer, Kevin M. ; Hanlon, Roger T.
    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.
  • Dataset
    Neural control of tuneable skin iridescence in squid
    ( 2012-07-25) Wardill, Trevor J. ; Gonzalez-Bellido, Paloma T. ; Crook, Robyn J. ; Hanlon, Roger T.
    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.
  • Article
    Virtual finger boosts three-dimensional imaging and microsurgery as well as terabyte volume image visualization and analysis
    (Nature Publishing Group, 2014-07-11) Peng, Hanchuan ; Tang, Jianyong ; Xiao, Hang ; Bria, Alessandro ; Zhou, Jianlong ; Butler, Victoria ; Zhou, Zhi ; Gonzalez-Bellido, Paloma T. ; Oh, Seung W. ; Chen, Jichao ; Mitra, Ananya ; Tsien, Richard W. ; Zeng, Hongkui ; Ascoli, Giorgio A. ; Iannello, Giulio ; Hawrylycz, Michael ; Myers, Eugene ; Long, Fuhui
    Three-dimensional (3D) bioimaging, visualization and data analysis are in strong need of powerful 3D exploration techniques. We develop virtual finger (VF) to generate 3D curves, points and regions-of-interest in the 3D space of a volumetric image with a single finger operation, such as a computer mouse stroke, or click or zoom from the 2D-projection plane of an image as visualized with a computer. VF provides efficient methods for acquisition, visualization and analysis of 3D images for roundworm, fruitfly, dragonfly, mouse, rat and human. Specifically, VF enables instant 3D optical zoom-in imaging, 3D free-form optical microsurgery, and 3D visualization and annotation of terabytes of whole-brain image volumes. VF also leads to orders of magnitude better efficiency of automated 3D reconstruction of neurons and similar biostructures over our previous systems. We use VF to generate from images of 1,107 Drosophila GAL4 lines a projectome of a Drosophila brain.
  • Article
    Neural control of dynamic 3-dimensional skin papillae for cuttlefish camouflage
    (Cell Press, 2018-04-04) Gonzalez-Bellido, Paloma T. ; Scaros, Alexia T. ; Hanlon, Roger T. ; Wardill, Trevor J.
    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.
  • Article
    Target detection in insects : optical, neural and behavioral optimizations
    (Elsevier, 2016-09-20) Gonzalez-Bellido, Paloma T. ; Fabian, Samuel T. ; Nordstrom, Karin
    Motion 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.
  • Article
    The killer fly hunger games : target size and speed predict decision to pursuit
    (S. Karger AG, Basel, 2015-09-24) Wardill, Trevor J. ; Knowles, K. ; Barlow, L. ; Tapia, G. ; Nordstrom, Karin ; Olberg, R. M. ; Gonzalez-Bellido, Paloma T.
    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.
  • Article
    A novel interception strategy in a miniature robber fly with extreme visual acuity
    (Cell Press, 2017-03-09) Wardill, Trevor J. ; Fabian, Samuel T. ; Pettigrew, Ann C. ; Stavenga, Doekele ; Nordström, Karin ; Gonzalez-Bellido, Paloma T.
    Our visual system allows us to rapidly identify and intercept a moving object. When this object is far away, we base the trajectory on the target’s location relative to an external frame of reference [1]. This process forms the basis for the constant bearing angle (CBA) model, a reactive strategy that ensures interception since the bearing angle, formed between the line joining pursuer and target (called the range vector) and an external reference line, is held constant [2; 3 ; 4]. The CBA model may be a fundamental and widespread strategy, as it is also known to explain the interception trajectories of bats and fish [5 ; 6]. Here, we show that the aerial attack of the tiny robber fly Holcocephala fusca is consistent with the CBA model. In addition, Holcocephala fusca displays a novel proactive strategy, termed “lock-on” phase, embedded with the later part of the flight. We found the object detection threshold for this species to be 0.13°, enabled by an extremely specialized, forward pointing fovea (∼5 ommatidia wide, interommatidial angle Δφ = 0.28°, photoreceptor acceptance angle Δρ = 0.27°). This study furthers our understanding of the accurate performance that a miniature brain can achieve in highly demanding sensorimotor tasks and suggests the presence of equivalent mechanisms for target interception across a wide range of taxa.