J Exp Biol
January 1, 2017;
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.
J Exp Biol
sensory perception of light stimulus
[+] 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. 2. Simulated enhancement factor curves for three model photoreceptors. Based on the dimensions of cones in (A) birds (lOS=30 μm, dOS=1.5 μm,
dOD=3 μm), (B) frogs (lOS=12 μm, tapering dOS=4.5–0 μm, dOD=6.2 μm) and (C) turtles (lOS=10 μm, tapering dOS=3–1 μm, dOD=5 μm), where lOS is the outer
segment length, and dOS and dOD are the diameters of the outer segment and the oil droplet, respectively. Families of curves were calculated for a wavelengthinvariant
value of the refractive index of the oil droplet, nOD, increasing in steps of 0.05 from 1.45 to 1.8. Grey regions show enhancement factors <1, corresponding
to loss of light because of the oil droplet. Thick light blue lines show DG. In all three cases, the higher the refractive index of the oil droplet, the lower the
enhancement factor. In no case did the enhancement factor approach DG.
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.