XB-ART-55087J Exp Biol January 1, 2017; 220 (Pt 11): 1997-2004.
Optical influence of oil droplets on cone photoreceptor sensitivity.
Oil droplets are spherical organelles found in the cone photoreceptors of vertebrates. They are generally assumed to focus incident light into the outer segment, and thereby improve light catch because of the droplets'' spherical lens-like shape. However, using full-wave optical simulations of physiologically realistic cone photoreceptors from birds, frogs and turtles, we find that pigmented oil droplets actually drastically reduce the transmission of light into the outer segment integrated across the full visible wavelength range of each species. Only transparent oil droplets improve light catch into the outer segments, and any enhancement is critically dependent on the refractive index, diameter of the oil droplet, and diameter and length of the outer segment. Furthermore, oil droplets are not the only optical elements found in cone inner segments. The ellipsoid, a dense aggregation of mitochondria situated immediately prior to the oil droplet, mitigates the loss of light at the oil droplet surface. We describe a framework for integrating these optical phenomena into simple models of receptor sensitivity, and the relevance of these observations to evolutionary appearance and loss of oil droplets is discussed.
PubMed ID: 28314749
Article link: J Exp Biol
Genes referenced: atn1 pin1
GO keywords: sensory perception of light stimulus
Article Images: [+] show captions
|Fig. 1. Summary tree of the pigmentation properties and presence/absence of oil droplets in extant vertebrates. Blue circles indicate that there are no pigmented oil droplets in any cone of a taxon; red circles show taxa that have at least some pigmented droplets and some transparent, most regularly in the violet-sensitive (VS) and ultraviolet-sensitive (UVS) cones. Asterisks indicate the possible first appearance of pigmented or transparent oil droplets. Question marks indicate uncertainties. Source references for oil droplet traits and more detailed notes are provided in the supplementary information (Table S1). Tree informed by Meyer and Zardoya (2003). Figure courtesy of Olle Lind, Lund University.|
|Fig. 3. Simulated enhancement factors for increasing outer segment length, lOS. dOS=1.5 μm and nOD=1.5. Grey regions indicate oil droplets resulting in loss of light. (A) dOD=1.5 μm. (B) dOD=3 μm. Thick light blue line indicates DG of 1 in A and 4 in B, falling outside the axis limits. Enhancement is greater for shorter lOS for both values of dOD.|
|Fig. 4. Simulated enhancement factors for increasing sizes of oil droplet. lOS=30 μm and nOD=1.5. Grey regions indicate oil droplets resulting in loss of light. Larger oil droplets result in greater enhancement factors. Wider outer segments and larger oil droplets give larger enhancement factors.|
|Fig. 5. Refractive index of Xenopus laevis oil droplets measured by digital holographic microscopy. Grey open circles show individual measurements. Black filled circles show mean values at each wavelength with error bars showing single standard deviations. Line shows the Cauchy equation fit to the data points. Xenopus silhouette modified from photograph by Brian Gratwicke available on flickr under Creative Commons attribution license.|
|Fig. 6. Influence of pigmented and unpigmented oil droplets on sensitivity of cones in Xenopus laevis, Gallus gallus domesticus and Trachemys scripta elegans in the absence of the ellipsoid. (A) Relative cone photoreceptor dimensions used in calculations. (B,C) Absorption coefficients of the long-, medium- and short-wavelength-sensitive (LWS, MWS and SWS, respectively) cone oil droplets in the chicken and turtle, respectively. Pale lines show measured spectra, dark lines show modelled spectra. (D–F) Oil droplet enhancement factors for the cone photoreceptors of the three species. (G–I) Relative cone sensitivities using the calculated enhancement factors. Dotted lines show the visual pigment absorbance templates. Solid lines show the result of multiplying the normalised visual pigment absorbance by the enhancement factor. (D,G) Xenopus laevis. (B,E,H) Gallus gallus domesticus. (C,F,I) Trachemys scripta elegans. The chicken silhouette was designed by freepik. Xenopus and turtle silhouettes were modified from photographs by Brian Gratwicke and Jim Capaldi made available on Flickr under Creative Commons attribution licenses.|
|Fig. 7. Impact of the ellipsoid on enhancement factor and relative sensitivity for chicken cone photoreceptors. (A) Enhancement factors with and without the ellipsoid. Dashed lines show enhancement factors without the ellipsoid; solid lines show enhancement factors including both ellipsoid and oil droplet. Greatest increase is seen for the violet-sensitive (VS) cone, which with the addition of an ellipsoid has an enhancement factor much larger than 1. In the SWS and MWS receptors, a small increase is seen. In the LWS receptor, a very slight decrease in enhancement is seen for the visible spectrum. (B) Relative sensitivity of chicken cones with and without the ellipsoid. Ocular media transmittance is included as measured by Lind and Kelber (2009b).|
|Fig S1: Example schematics of the simulation environment. Thick black line indicates the plane wave source. Calculations are performed in cylindrical polar coordinates (r, φ, z). φdirection is normal to the plane of the page here. Simulation is surrounded on three sides with perfectly-matched layers (PML) which prevent numerical reflections from the sides of the simulation environment (Oskooi et al. 2010).|
|Fig S2: Histograms of the refractive indices of Xenopus oil droplets as measured at four wavelengths. D values show the result of Hartigans’ dip test, which tests for multimodality in a distribution. None of these distributions demonstrate significant multimodality, indicating that in terms of refractive index, all Xenopus oil droplets measured are from the same population (ie there is not more than one type of oil droplet with respect to refractive index).|
|Fig S3: Calculations of enhancement with and without outer segments as a comparison to the Mie scattering calculations of Ives et al. (1983) for the receptor geometry, refractive indices and oil droplet absorption spectra of the turtle Trachemys scripta elegans. Solid lines show enhancement factors including the outer segment and dashed lines show calculations without. When the outer segment is not present we recover greater enhancement factors that approach those calculated by Ives et al. (1983). This is due to the waveguiding effect of the outer segment, which allows it to confine light to its volume even without the presence of the oil droplet. Red lines – LWS cone. Green lines – MWS cone. Blue lines – SWS cone.|
|Fig. S4: Absorption coefficients and optical properties of the oil droplets of T. scripta elegans. Absorption coefficient modelled using the methods of Wilby et al. (2015). Solid lines show model spectra. Dotted lines show spectra from Strother (1963) and Liebman & Granda (1971). Calculated extinction coefficient and real refractive index. Circles show refractive index values from Ives et al. (1983) and the spectral range over which these were measured. Red lines – LWS cone. Green lines – MWS cone. Blue lines – SWS cone.|