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79
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Introduction
I am a sensory neurobiologist. I investigate evolution of dynamic cephalopod iridescence and colour vision in flies, how they evolved, how they function and what purpose they serve in the ecology of the animal. In particular, I am interested in understanding how squids generate skin patterns and colour changes though dynamic iridescence and how flies use their colour vision to avoid predation or find mates and food. I am looking for PhD candidates.
Additional affiliations
May 2018 - present
October 2014 - February 2019
April 2014 - October 2014
Education
November 2001 - January 2006
Publications
Publications (79)
Internal predictions about the sensory consequences of self-motion, encoded by corollary discharge, are ubiquitous in the animal kingdom, including for fruit flies, dragonflies, and humans. In contrast, predicting the future location of an independently moving external target requires an internal model. With the use of internal models for predictiv...
The evolutionary history of visual genes in Coleoptera differs from other well-studied insect orders, such as Lepidoptera and Diptera, as beetles have lost the widely conserved short-wavelength (SW) insect opsin gene that typically underpins sensitivity to blue light (∼ 440 nm). Duplications of the ancestral ultraviolet (UV) and long-wavelength (LW...
The ability to visualize small moving objects is vital for the survival of many animals, as these could represent predators or prey. For example, 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 hoverfli...
Octopus’ limb hyper-redundancy complicates traditional motor control system theory due to its extensive sensory inputs, subsequent decision-making, and arm coordination. Octopuses are thought to reduce flexibility control complexity by relying on highly stereotypical motor primitives (e.g., reaching1, 2, 3, 4 and crawling⁵) and multi-level processe...
The ability to visualize small moving objects is vital for the survival of many animals, as these could represent predators or prey. For example, predatory insects, including dragonflies, robber flies and killer flies, perform elegant, high-speed pursuit of both biological and artificial targets. Many non-predatory insects, including male hoverflie...
The miniature robber fly Holcocephala fusca intercepts its targets with behaviour that is approximated by the proportional navigation guidance law. During predatory trials, we challenged the interception of H. fusca performance by placing a large object in its potential flight path. In response, H. fusca deviated from the path predicted by pure pro...
Drosophila melanogaster has long been a popular model insect species, due in large part to the availability of genetic tools and is fast becoming the model for insect colour vision. Key to understanding colour reception in Drosophila is in-depth knowledge of spectral inputs and downstream neural processing. While recent studies have sparked renewed...
Motion vision has been extensively characterised in Drosophila melanogaster, but substantially less is known about how flies process colour, or how spectral information affects other visual modalities. To accurately dissect the components of the early visual system responsible for processing colour, we developed a versatile visual stimulation setup...
Genes for endoplasmic reticulum (ER)-shaping proteins are among the most commonly mutated in hereditary spastic paraplegia (HSP). Mutation of these genes in model organisms can lead to disruption of the ER network. To investigate how the physiological roles of the ER might be affected by such disruption, we developed tools to interrogate its Ca²⁺ s...
Drosophila melanogaster has long been a popular model insect species, due in large part to the availability of genetic tools and is fast becoming the model for insect colour vision. Key to understanding colour reception in Drosophila is in-depth knowledge of spectral inputs and downstream neural processing. While recent studies have sparked renewed...
Motion vision has been extensively characterized in Drosophila melanogaster, but substantially less is known about how flies process colour, or how spectral information affects other visual modalities. To accurately dissect the components of the early visual system responsible for processing colour, we developed a versatile visual stimulation setup...
Why Velcro 3D glasses onto cuttlefish? In Episode 69, Trevor Wardill from the Department of Ecology, Evolution and Behavior at the University of Minnesota discusses his research into the previously unknown ability of the cephalopod to see in stereo vision. His article, “Cuttlefish use stereopsis to strike at prey,“ was published along with multiple...
Genes for ER-shaping proteins are among the most commonly mutated in Hereditary Spastic Paraplegia (HSP). Mutation of these genes in model organisms can lead to disruption of the ER network. To investigate how the physiological roles of the ER might be affected by such disruption, we developed tools to interrogate its Ca2+ signaling function. We ge...
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 track...
The camera-type eyes of vertebrates and cephalopods exhibit remarkable convergence, but it is currently unknown whether the mechanisms for visual information processing in these brains, which exhibit wildly disparate architecture, are also shared. To investigate stereopsis in a cephalopod species, we affixed “anaglyph” glasses to cuttlefish and use...
Both vertebrates and invertebrates commonly exploit photonic structures adjacent to their photoreceptors for visual benefits. For example, use of a reflecting structure (tapetum) behind the retina increases photon capture, enhancing vision in dim light. Colored filters positioned lateral or distal to a photoreceptive unit may also be used to tune s...
When aiming to capture a fast-moving target, animals can follow it until they catch up, or try to intercept it. In principle, interception is the more complicated strategy, but also more energy efficient. To study whether simple feedback controllers can explain interception behaviours by animals with miniature brains, we have reconstructed and stud...
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 ot...
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,...
The color and pattern changing abilities of octopus, squid, and cuttlefish via chromatophore neuromuscular 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, y...
Holcocephala takes off when the bead is moving forward. Shortly after, the bead stops and reverses in direction. During flight, Holcocephala compensates reactively for such changes, which leads to a successful target interception. Each frame equals one millisecond.
Movie S2. Testing the Object Detection Threshold of Holcocephala, Related to Figure?2
This video shows the second longest distance (59?cm) at which Holcocephala detected and subsequently successfully intercepted the 1.3?mm bead. Each frame equals one millisecond.
The cuticle?s autofluorescence signal is particularly strong, and the ommatidial lattice can be seen with ease. The autofluorescence signal arising from the photoreceptors is weaker, but it is sufficient to locate the photoreceptor tips. The sample was bleached and cleared before being imaged with a two-photon microscope.
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, f...
Stubbs and Stubbs present a novel visual mechanism based on chromatic aberration that might allow animals with only one spectral photoreceptor-type to perceive color (1) (see ref. 1 for details about their mechanism). The authors chose cephalopods to showcase their hypothesis and claim that discrepancies between earlier (2, 3) and recent (4, 5) neg...
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...
Cephalopods are famous for their ability to change color and pattern rapidly for signaling and camouflage. They have keen eyes and remarkable vision, made possible by photoreceptors in their retinas. External to the eyes, photoreceptors also exist in parolfactory vesicles and some light organs, where they function using a rhodopsin protein that is...
Cuttlefish, Sepia officinalis, possess neurally controlled, pigmented chromatophore organs that allow rapid changes in skin patterning and coloration in response to visual cues. This process of adaptive coloration is enabled by the 500% change in chromatophore surface area during actuation. We report two adaptations that help to explain how colour...
Squid 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....
Fluorescent protein-based sensors for detecting neuronal activity have been developed largely based on non-neuronal screening systems. However, the dynamics of neuronal state variables (e.g., voltage, calcium, etc.) are typically very rapid compared to those of non-excitable cells. We developed an electrical stimulation and fluorescence imaging pla...
Catching insects on the wing requires visual speed, acuity and body maneuverability. This situation is exemplified by dragonflies, which exhibit a predatory behavior and sport the largest of all insect eyes. However, miniature killer flies (Coenosia species, 4 mm body length) also catch targets midflight. How do miniature killer flies accommodate t...
Cephalopods create precise skin color and pattern displays for the purpose of signaling and camouflage. In squids, such visual trickery is achieved through the combined action of two color elements: pigmented chromatophores and structural iridophores (which produce iridescence). The neural control of chromatophores was recognized many decades ago b...
Fluorescent calcium sensors are widely used to image neural activity. Using structure-based mutagenesis and neuron-based screening, we developed a family of ultrasensitive protein calcium sensors (GCaMP6) that outperformed other sensors in cultured neurons and in zebrafish, flies and mice in vivo. In layer 2/3 pyramidal neurons of the mouse visual...
Cephalopod skin is soft, flexible, and produces rapid color changes for camouflage and signaling primarily by regulating the shapes of its numerous chromatophore organs. Each chromatophore has 10–30 radial muscle cells, termed fibers, under central nervous system control. Each fiber contains myofilaments that contract in concert to stretch the pigm...
Genetically encoded calcium indicators (GECIs) are powerful tools for systems neuroscience. Here we describe red, single-wavelength GECIs, "RCaMPs," engineered from circular permutation of the thermostable red fluorescent protein mRuby. High-resolution crystal structures of mRuby, the red sensor RCaMP, and the recently published red GECI R-GECO1 gi...
Genetically encoded calcium indicators (GECIs) are powerful tools for systems neuroscience. Recent efforts in protein engineering have significantly increased the performance of GECIs. The state-of-the art single-wavelength GECI, GCaMP3, has been deployed in a number of model organisms and can reliably detect three or more action potentials in shor...
Neuroscience researchers have long sought methods to describe the neural connectivity of the circuits responsible for specific behaviors. One major obstacle is scale: Neural spines can be <1 µm in diameter, but axons can range from millimeters to centimeters (or larger) in length, making tissue imaging and neuron reconstruction a challenging task....
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...
Color and Movement
From humans to insects, color and motion information are thought to be channeled through separate neural pathways for efficient visual processing, but it remains unclear if and how these pathways interact in improving perception of moving colored stimuli. By using sophisticated Drosophila genetics, intracellular electrophysiology...
Color and motion information are thought be distributed into separate visual pathways for efficient neural processing, but it remains unclear how these pathways interact to allow discrimination of moving colored objects. Here we report that in the early visual system of Drosophila color information partially feeds into the motion pathway, refining...
The compound eye of insects imposes a tradeoff between resolution and sensitivity, which should exacerbate with diminishing eye size. Tiny lenses are thought to deliver poor acuity because of diffraction; nevertheless, miniature insects have visual systems that allow a myriad of lifestyles. Here, we investigate whether size constraints result in an...
shibire(ts1), a temperature-sensitive mutation of the Drosophila gene encoding a Dynamin orthologue, blocks vesicle endocytosis and thus synaptic transmission, at elevated, or restrictive temperatures. By targeted Gal4 expression, UAS-shibire(ts1) has been used to dissect neuronal circuits. We investigated the effects of UAS-shibire(ts1) overexpres...
Compared to higher organisms, the relatively simple and genetically malleable Drosophila can help us to make sense of motion coding strategies and visually driven behaviour. We wish to study how visual motion-sensitive information is routed to and processed in lobula plate tangential neurons (LPTNs) which express calcium sensitive dyes. For this pu...
The Drosophila visual system copes with the strains imposed by a small body size and successfully guides complex behaviors. To understand a visual system, knowing its acuity is paramount. The acceptance angle Δρ, is the parameter used to describe spatial performance. Stavenga (2003) calculated Δρ=4.2°. However, through in-vivo recordings of intrace...
Retinal networks must adapt constantly to best present the ever changing visual world to the brain. Here we test the hypothesis that adaptation is a result of different mechanisms at several synaptic connections within the network. In a companion paper (Part I), we showed that adaptation in the photoreceptors (R1-R6) and large monopolar cells (LMC)...
Because of the limited processing capacity of eyes, retinal networks must adapt constantly to best present the ever changing visual world to the brain. However, we still know little about how adaptation in retinal networks shapes neural encoding of changing information. To study this question, we recorded voltage responses from photoreceptors (R1-R...
Reducing L2-R-feedback reduces the high-frequency content and hence adaptational “whitening” of LMC output. A. Mean output of WT Canton-S LMCs to middle-intensity naturalistic stimulus (NS) at 19 oC (left) and 30 oC (right), n = 13 and 14 cells, respectively. B. The mean normalized spectra of LMCs (n = 11–14 cells) measured at the 20th s of NS in W...
Photoreceptor and LMC outputs to repeated NS is independent of the observation window and the speed of stimulation. A 10,000-points-long NS pattern was repeatedly presented to a WT Canton-S photoreceptor and LMC at 50 kHz (200 ms observation window; i.e. the duration of each input and output) at 19°C. A. Four first voltage responses of a photorecep...
Leucine aminopeptidase (LAP) belongs to a family of ubiquitous peptidases, with roles in growth and development, stress responses and adaptation to changing environmental conditions. The LAP gene was sequenced from a commercially important marine bivalve: the Pacific oyster Crassostrea gigas, and sequence polymorphisms were identified. This study i...
This manual provides guidelines for the design and reporting of silvicultural field experiments, focusing on hardwoods in plantations. It was compiled using contemporary literature and advice from silvicultural researchers throughout Australia. The manual is available at: http://www.agrifutures.com.au/publications/designing-silvicultural-research-t...