Award details

Seeing the world in a different light - discovering how vertebrates see polarized light

Reference	BB/H01635X/1
Principal Investigator / Supervisor	Professor Nicholas Roberts
Co-Investigators / Co-Supervisors	Professor Julian Partridge
Institution	University of Bristol
Department	Biological Sciences
Funding type	Research
Value (£)	325,121
Status	Completed
Type	Research Grant
Start date	01/01/2011
End date	31/12/2013
Duration	36 months

Abstract

We will determine the basis of vertebrate polarization vision (PV) and its behaviour: 1. By using a novel 2-D imaging microspectrophotometer to measure axial spectral (320-800nm) absorbance and dichroic ratios of rods and single, double and twin cones cones of fish. Retinal cryo-sections, with photoreceptors in natural retinal mosaics and geometries, will be measured from fish with different mosaics. Further key outcomes will be the determination of whether UV or VS cones, and opponent processing between different spectral channels in double cones, are independent prerequisites for polarization detection. 2-D axial MSP data will be validated by independent 'side-on' MSP. 2. By quantifying the spatial order of photoreceptor outer segment membranes to test the hypothesis that in-plane order and the alignment of visual pigment molecules underpins cellular dichroism. We will use electron microscopy (TEM) and associated analyses of TEM images to quantify crystalline domains and measure the extent and orientation of phase separations in cone outer segments (COS). Associated micro-polarimetric measurements will reveal the fundamental optical properties of COS. 3. By behavioural tests (operant conditioning) of fish PV using a novel apparatus in which two UV transmissive nematic liquid crystal cells control and modulate polarization stimuli. This new approach is free of potentially confounding variables due to the elimination of moving parts or stimulus intensity changes. Tests will be conducted on a range of species having square and/or row cone mosaics, and/or UVS/VS cones. UV blocking (longwave pass) filters in the stimulus light path will enable us to determine whether UV is a prerequisite for fish PV. UV pass (longwave cut-off) filters will also allow us to determine whether cone beta-band absorption is sufficient for PV. Finally, changing the frequency of liquid crystal modulation will open an entirely new field of study - the temporal dynamics of vertebrate PV.

Summary

Most animals see the world in a very different way from us and differ in their ability to see detail, movement and colour. This study will investigate an aspect of vision beyond these familiar visual properties, and one that is totally alien to us: the ability to see polarized light. Polarization describes the direction in which a wave of light oscillates and, although humans are unaware of this, light around us is polarized. Polarization vision is often considered a characteristic of invertebrates such as insects, but many vertebrates can also detect and decode the polarization of light. This gives them extra visual information for tasks such as object recognition, communication and camouflage detection. It also adds an extra dimension to other sensory abilities, such as smell or magnetoreception for use in navigation and has potential to enhance contrasts in environments where light is scattered, particularly underwater. In this proposed research, we will investigate polarization vision in vertebrates, using fish as model organisms. Several species of fish have been shown relay information about the polarization of light from the eye to the brain. However, very little is known about either the way the eye detects the polarization of light, or how fish use it in their behaviour. Our experiments build on the work of the PI who recently, and for the first time, showed that when particular types of light sensitive cells in vertebrate retina (called cones) were illuminated end on, as they are in the eye, they absorb differently-orientated linear polarized light to different degrees. Our measurements will be made by microspectrophotometry and microspectropolarimetry - techniques that measure how polarized light is absorbed and transmitted through microscopic-sized samples. We will use two techniques for microspectrophotometry: (i) using a conventional instrument in which single cells are measured in a side-on orientation to validate data from (ii) an innovative and specifically constructed 2-dimensional imaging instrument that will allow the simultaneous measurement of many cells in a retina. Along with novel microspectropolarimetric measurements, made by adapting the 2-D microspectrophotometer, we will determine how species known to have different retinal anatomies (e.g. square or linear arrangements of cones in their retinas) and different complements of cone photoreceptor types (e.g. those with and without UV-sensitive cones) absorb polarized light. We will ally these spectral measurements with electron microscopy studies to quantify the organization of proteins and lipids in cone cell outer segments which we suggest may well be the mechanism that enables individual photoreceptors to be sensitive to differently polarized light. The part of cones that absorb light have already been shown to have unexplained organizational sub-structure, but the significance of such structures for photoreceptor function has yet to be demonstrated. Finally, we will use behavioural tests to screen various species of fish for behavioural demonstration of polarization vision, this being the important end point of any sensory capability. Fish readily learn visual tasks that result in a reward such as food and we will use this attribute to test for polarization sensitivity. By using a novel method based on apparatus incorporating nematic liquid crystal cells to control the polarization of the stimulus that the fish see in the experiments, we will investigate their ability to discriminate horizontal from vertical polarization; the importance of ultraviolet light in polarization vision; and the frequency, or speed, with which changes in polarization can be seen. Ultimately this research will answer one of the most significant unanswered questions in vision biology: How do vertebrates see polarized light?

Impact Summary

Who will benefit from this research? The immediate beneficiaries of this research will be the employed PDRA who will gain expertise in state-of-the-art techniques and novel experimental methods. The PI and Co-I will benefit by the further development of their research skills and the project will establish a new research strength within the School of Biological Sciences' Ecology of Vision group. The research outputs will directly benefit and complement existing worldwide research into polarization vision. However, in a wider context, significant new methods, specifically 2-D imaging MSP and the novel behavioural paradigm for testing polarization vision will assist corresponding directions of bio-photonics and bio-imaging, and behavioural ecology respectively. Our work on membrane domains in photoreceptor cell outer segments will have more general relevance to other sub-cellular research into membrane biochemistry and soft matter physics. Beyond academia, we have identified several potential stakeholders as diverse as the general public (via our planned PES and media activities), applied forensic science, natural history and science documentary filmmakers, and companies involved in fish husbandry and the design and construction of fish accommodation. Beneficiaries related to the latter will include policy-makers with responsibility for animal welfare: to date, the sensory environment requirements of animals, particularly fish, has been poorly understood and, to our knowledge, the polarization properties of an animal's environment have never been considered, despite the fact that this is a feature of the natural environment (especially underwater) and will therefore be relevant to animals with polarization vision. How will they benefit from this research? This project has relevance for the maintenance of the UK's pre-eminence in sensory biological science which will be augmented by developing world leading novel methods which will be used to investigate a very poorly understood sensory modality (namely polarization vision in vertebrates). The ability to demonstrate that fish see the world in very different ways from us, specifically by developing a novel way of behaviourally testing for polarization vision, will be of significance to anyone interested in animals. Simply put, it further underlies the fact that an anthropocentric perspective of an animal sensory experience is misplaced and inappropriate. The latter point will be of interest to the general public, TV and filmmaking companies but is particularly relevant when animal welfare considerations are made. This will have direct relevance to the proper design of fish housing in research, public and domestic aquaria, and in some forms of aquaculture, where best husbandry practice is fundamental to maximizing animal welfare. In terms of technology, this project will develop new equipment which will have potential value in applied science and commerce: we have, for instance, already identified the potential value of 2-D imaging MSP in forensic science. Before we can translate our fundamental research into such applications we need to establish and validate several new methods and generate data. We therefore expect that more applied benefits will only become possible towards the end of the project, with PES activities realized earlier on. What will be done to ensure that they have the opportunity to benefit from this research? As explained in the attached Impact Plan, we have well developed plans for the effective communication of our research, both in academic and non-academic contexts. In PES, we have a particular high profile track record. We also have grant applications in preparation for other aspects of work on polarization vision, and links with TV companies regarding possible programs on animal vision, and are initiating discussions with companies constructing fish accommodation systems regarding the design of such equipment.

Committee	Research Committee A (Animal disease, health and welfare)
Research Topics	Neuroscience and Behaviour
Research Priority	X – Research Priority information not available
Research Initiative	X - not in an Initiative
Funding Scheme	X – not Funded via a specific Funding Scheme

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