Abstract

Cone oil droplets are highly retractile, optically dense spheres located in front of the cone outer segment. Because of their refractile strength, absorbance, and size, these spherical oil droplets have a pronounced influence on the light reaching the photopigment. We used electromagnetic scattering theory to interrelate these factors, and we calculated the light energy distribution around cone oil droplets modeled as isolated spheres. The necessary electromagnetic parameters were determined from anatomical and optical measurements in the turtle retina. Cone and oil-droplet dimensions were determined with a light microscope. The index-of-refraction values for the red, yellow, orange, and clear oil droplets were measured to be 1.69, 1.55, 1.51, and 1.48, respectively, by the technique of immersion matching. The application of the electromagnetic scattering theory suggests that oil droplets significantly increase cone sensitivity. Cone action spectra predicted by this analysis show that the largest increases occur around the absorption maximum of each cone’s photopigment.

© 1983 Optical Society of America

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References

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  1. G. L. Walls, The Vertebrate Eye and Its Adaptive Radiation (Cranbrook Institute of Science, Bloomfield Hills, Mich, 1942).
    [Crossref]
  2. P. A. Liebman and A. M. Granda, “Super dense carotenoid spectra resolved in single cone oil droplets,” Nature 253, 370–372 (1975).
    [Crossref] [PubMed]
  3. H. F. Leeper, “Horizontal cells of the turtle retina: analysis of interconnections between photoreceptor cells and horizontal cells by light microscopy,” J. Comp. Neurol. 182, 795–810 (1978).
    [Crossref] [PubMed]
  4. D. A. Baylor and R. Fettiplace, “Light path and photon capture in turtle photoreceptors,” J. Physiol. 248, 433–464 (1975).
  5. M. L. Wolbarsht, “The function of intraocular color filters,” Fed. Proc. 35, 44–50 (1976).
    [PubMed]
  6. D. A. Baylor and A. L. Hodgkin, “Detection and resolution of visual stimuli by turtle photoreceptors,” J. Physiol. 234, 163–198 (1973).
  7. J. K. Bowmaker and A. Knowles, “The visual pigments and oil droplets of the chicken retina,” Vision Res. 17, 755–764 (1977).
    [Crossref] [PubMed]
  8. G. H. Jacobs, Comparative Color Vision (Academic, New York, 1981).
  9. J. A. Stratton, Electromagnetic Theory (McGraw-Hill, New York, 1941).
  10. H. C. Van de Hulst, Light Scattering by Small Particles (Wiley, New York, 1957).
  11. R. F. Harrington, Time-Harmonic Electromagnetic Fields (McGraw-Hill, New York, 1961).
  12. M. Kerker, The Scattering of Light and Other Electromagnetic Radiation (Academic, New York, 1969).
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    [Crossref]
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    [Crossref] [PubMed]
  17. K. T. Brown, “A linear area centralis extending across the turtle retina and stabilized to the horizon by non-visual cues,” Vision Res. 9, 1053–1062 (1969).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  19. H. Kolb and J. Jones, “Light and electron microscopy of the photoreceptors in the retina of the red eared slider, Pseudemys scripta elegans,” J. Comp. Neurol. 209, 331–338 (1982).
    [Crossref] [PubMed]
  20. P. A. Liebman, Handbook of Sensory Physiology VII/1 (Springer-Verlag, Berlin, 1972).
  21. R. W. Ditchburn, Light (Interscience, New York, 1953).
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    [Crossref]
  23. A. H. Bennett, H. Jupnik, H. Osterberg, and O. W. Richards, Phase Microscopy: Principles and Applications (Wiley, New York, 1951).
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    [Crossref]
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    [Crossref] [PubMed]
  26. J. M. Enoch “Nature of the transmission of energy in the retinal receptors,” J. Opt. Soc. Am. 51, 1122–1127 (1961).
    [Crossref] [PubMed]
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    [Crossref]
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    [Crossref] [PubMed]
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    [Crossref]
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    [Crossref] [PubMed]

1982 (1)

H. Kolb and J. Jones, “Light and electron microscopy of the photoreceptors in the retina of the red eared slider, Pseudemys scripta elegans,” J. Comp. Neurol. 209, 331–338 (1982).
[Crossref] [PubMed]

1978 (1)

H. F. Leeper, “Horizontal cells of the turtle retina: analysis of interconnections between photoreceptor cells and horizontal cells by light microscopy,” J. Comp. Neurol. 182, 795–810 (1978).
[Crossref] [PubMed]

1977 (1)

J. K. Bowmaker and A. Knowles, “The visual pigments and oil droplets of the chicken retina,” Vision Res. 17, 755–764 (1977).
[Crossref] [PubMed]

1976 (2)

1975 (2)

P. A. Liebman and A. M. Granda, “Super dense carotenoid spectra resolved in single cone oil droplets,” Nature 253, 370–372 (1975).
[Crossref] [PubMed]

D. A. Baylor and R. Fettiplace, “Light path and photon capture in turtle photoreceptors,” J. Physiol. 248, 433–464 (1975).

1973 (2)

D. A. Baylor and A. L. Hodgkin, “Detection and resolution of visual stimuli by turtle photoreceptors,” J. Physiol. 234, 163–198 (1973).

A. M. Snyder and C. Pask, “The Stiles–Crawford effect—explanation and consequences,” Vision Res. 13, 1115–1137 (1973).
[Crossref] [PubMed]

1971 (2)

M. A. Ali, “Les reponses retinometrices: caracteres et mecanismes,” Vision Res. 11, 1225–1288 (1971).
[Crossref] [PubMed]

P. A. Liebman and A. M. Granda, “Microspectrophotometric measurements of visual pigments in two species of turtle, Pseudemys scripta and Chelonia mydas,” Vision Res. 11, 105–114 (1971).
[Crossref] [PubMed]

1970 (1)

A. M. Granda and K. W. Haden, “Retinal oil globule counts and distributions in two species of turtle: Pseudemys scripta elegans(Wied) and Chelonia mydas mydas(Linnaeus),” Vision Res. 10, 79–84 (1970).
[Crossref] [PubMed]

1969 (1)

K. T. Brown, “A linear area centralis extending across the turtle retina and stabilized to the horizon by non-visual cues,” Vision Res. 9, 1053–1062 (1969).
[Crossref] [PubMed]

1967 (1)

1963 (2)

G. K. Strother, “Absorption spectra of retinal oil globules in turkey, turtle and pigeon,” Expl. Cell Res. 29, 349–355 (1963).
[Crossref]

J. M. Enoch, “Optical role of retinal receptors,” J. Opt. Soc. Am. 53, 71–85 (1963).
[Crossref]

1961 (1)

1960 (1)

1957 (1)

R. L. Sidman, “The structure and concentration of solids in photoreceptor cells studied by refractometry and interference microscopy,” J. Biophys. Biochem. Cytol. 3, 15–33 (1957).

1956 (1)

K. Tansley and B. K. Johnson, “The cones of the grass snake’s eyes,” Nature 178, 1285–1286 (1956).
[Crossref]

Ali, M. A.

M. A. Ali, “Les reponses retinometrices: caracteres et mecanismes,” Vision Res. 11, 1225–1288 (1971).
[Crossref] [PubMed]

Baylor, D. A.

D. A. Baylor and R. Fettiplace, “Light path and photon capture in turtle photoreceptors,” J. Physiol. 248, 433–464 (1975).

D. A. Baylor and A. L. Hodgkin, “Detection and resolution of visual stimuli by turtle photoreceptors,” J. Physiol. 234, 163–198 (1973).

Bennett, A. H.

A. H. Bennett, H. Jupnik, H. Osterberg, and O. W. Richards, Phase Microscopy: Principles and Applications (Wiley, New York, 1951).

Bowmaker, J. K.

J. K. Bowmaker and A. Knowles, “The visual pigments and oil droplets of the chicken retina,” Vision Res. 17, 755–764 (1977).
[Crossref] [PubMed]

Brown, K. T.

K. T. Brown, “A linear area centralis extending across the turtle retina and stabilized to the horizon by non-visual cues,” Vision Res. 9, 1053–1062 (1969).
[Crossref] [PubMed]

Detweiler, S. R.

S. R. Detweiler, Vertebrate Photoreceptors (Macmillan, New York, 1943).
[Crossref]

Ditchburn, R. W.

R. W. Ditchburn, Light (Interscience, New York, 1953).

Enoch, J. M.

Fettiplace, R.

D. A. Baylor and R. Fettiplace, “Light path and photon capture in turtle photoreceptors,” J. Physiol. 248, 433–464 (1975).

Granda, A. M.

P. A. Liebman and A. M. Granda, “Super dense carotenoid spectra resolved in single cone oil droplets,” Nature 253, 370–372 (1975).
[Crossref] [PubMed]

P. A. Liebman and A. M. Granda, “Microspectrophotometric measurements of visual pigments in two species of turtle, Pseudemys scripta and Chelonia mydas,” Vision Res. 11, 105–114 (1971).
[Crossref] [PubMed]

A. M. Granda and K. W. Haden, “Retinal oil globule counts and distributions in two species of turtle: Pseudemys scripta elegans(Wied) and Chelonia mydas mydas(Linnaeus),” Vision Res. 10, 79–84 (1970).
[Crossref] [PubMed]

Haden, K. W.

A. M. Granda and K. W. Haden, “Retinal oil globule counts and distributions in two species of turtle: Pseudemys scripta elegans(Wied) and Chelonia mydas mydas(Linnaeus),” Vision Res. 10, 79–84 (1970).
[Crossref] [PubMed]

Harrington, R. F.

R. F. Harrington, Time-Harmonic Electromagnetic Fields (McGraw-Hill, New York, 1961).

Hodgkin, A. L.

D. A. Baylor and A. L. Hodgkin, “Detection and resolution of visual stimuli by turtle photoreceptors,” J. Physiol. 234, 163–198 (1973).

Jacobs, G. H.

G. H. Jacobs, Comparative Color Vision (Academic, New York, 1981).

Jaggers, W. S.

Johnson, B. K.

K. Tansley and B. K. Johnson, “The cones of the grass snake’s eyes,” Nature 178, 1285–1286 (1956).
[Crossref]

Jones, J.

H. Kolb and J. Jones, “Light and electron microscopy of the photoreceptors in the retina of the red eared slider, Pseudemys scripta elegans,” J. Comp. Neurol. 209, 331–338 (1982).
[Crossref] [PubMed]

Jupnik, H.

A. H. Bennett, H. Jupnik, H. Osterberg, and O. W. Richards, Phase Microscopy: Principles and Applications (Wiley, New York, 1951).

Kerker, M.

M. Kerker, The Scattering of Light and Other Electromagnetic Radiation (Academic, New York, 1969).

Knowles, A.

J. K. Bowmaker and A. Knowles, “The visual pigments and oil droplets of the chicken retina,” Vision Res. 17, 755–764 (1977).
[Crossref] [PubMed]

Kolb, H.

H. Kolb and J. Jones, “Light and electron microscopy of the photoreceptors in the retina of the red eared slider, Pseudemys scripta elegans,” J. Comp. Neurol. 209, 331–338 (1982).
[Crossref] [PubMed]

Leeper, H. F.

H. F. Leeper, “Horizontal cells of the turtle retina: analysis of interconnections between photoreceptor cells and horizontal cells by light microscopy,” J. Comp. Neurol. 182, 795–810 (1978).
[Crossref] [PubMed]

Liebman, P. A.

W. S. Jaggers and P. A. Liebman, “Anomalous dispersion of rhodopsin in rod outer segments of the frog,” J. Opt. Soc. Am. 66, 56–59 (1976).
[Crossref]

P. A. Liebman and A. M. Granda, “Super dense carotenoid spectra resolved in single cone oil droplets,” Nature 253, 370–372 (1975).
[Crossref] [PubMed]

P. A. Liebman and A. M. Granda, “Microspectrophotometric measurements of visual pigments in two species of turtle, Pseudemys scripta and Chelonia mydas,” Vision Res. 11, 105–114 (1971).
[Crossref] [PubMed]

P. A. Liebman, Handbook of Sensory Physiology VII/1 (Springer-Verlag, Berlin, 1972).

Osterberg, H.

A. H. Bennett, H. Jupnik, H. Osterberg, and O. W. Richards, Phase Microscopy: Principles and Applications (Wiley, New York, 1951).

Pask, C.

A. M. Snyder and C. Pask, “The Stiles–Crawford effect—explanation and consequences,” Vision Res. 13, 1115–1137 (1973).
[Crossref] [PubMed]

Richards, O. W.

A. H. Bennett, H. Jupnik, H. Osterberg, and O. W. Richards, Phase Microscopy: Principles and Applications (Wiley, New York, 1951).

Sidman, R. L.

R. L. Sidman, “The structure and concentration of solids in photoreceptor cells studied by refractometry and interference microscopy,” J. Biophys. Biochem. Cytol. 3, 15–33 (1957).

Snyder, A. M.

A. M. Snyder and C. Pask, “The Stiles–Crawford effect—explanation and consequences,” Vision Res. 13, 1115–1137 (1973).
[Crossref] [PubMed]

Stratton, J. A.

J. A. Stratton, Electromagnetic Theory (McGraw-Hill, New York, 1941).

Strother, G. K.

G. K. Strother, “Absorption spectra of retinal oil globules in turkey, turtle and pigeon,” Expl. Cell Res. 29, 349–355 (1963).
[Crossref]

Tansley, K.

K. Tansley and B. K. Johnson, “The cones of the grass snake’s eyes,” Nature 178, 1285–1286 (1956).
[Crossref]

Van de Hulst, H. C.

H. C. Van de Hulst, Light Scattering by Small Particles (Wiley, New York, 1957).

Walls, G. L.

G. L. Walls, The Vertebrate Eye and Its Adaptive Radiation (Cranbrook Institute of Science, Bloomfield Hills, Mich, 1942).
[Crossref]

Wolbarsht, M. L.

M. L. Wolbarsht, “The function of intraocular color filters,” Fed. Proc. 35, 44–50 (1976).
[PubMed]

Expl. Cell Res. (1)

G. K. Strother, “Absorption spectra of retinal oil globules in turkey, turtle and pigeon,” Expl. Cell Res. 29, 349–355 (1963).
[Crossref]

Fed. Proc. (1)

M. L. Wolbarsht, “The function of intraocular color filters,” Fed. Proc. 35, 44–50 (1976).
[PubMed]

J. Biophys. Biochem. Cytol. (1)

R. L. Sidman, “The structure and concentration of solids in photoreceptor cells studied by refractometry and interference microscopy,” J. Biophys. Biochem. Cytol. 3, 15–33 (1957).

J. Comp. Neurol. (2)

H. Kolb and J. Jones, “Light and electron microscopy of the photoreceptors in the retina of the red eared slider, Pseudemys scripta elegans,” J. Comp. Neurol. 209, 331–338 (1982).
[Crossref] [PubMed]

H. F. Leeper, “Horizontal cells of the turtle retina: analysis of interconnections between photoreceptor cells and horizontal cells by light microscopy,” J. Comp. Neurol. 182, 795–810 (1978).
[Crossref] [PubMed]

J. Opt. Soc. Am. (5)

J. Physiol. (2)

D. A. Baylor and R. Fettiplace, “Light path and photon capture in turtle photoreceptors,” J. Physiol. 248, 433–464 (1975).

D. A. Baylor and A. L. Hodgkin, “Detection and resolution of visual stimuli by turtle photoreceptors,” J. Physiol. 234, 163–198 (1973).

Nature (2)

P. A. Liebman and A. M. Granda, “Super dense carotenoid spectra resolved in single cone oil droplets,” Nature 253, 370–372 (1975).
[Crossref] [PubMed]

K. Tansley and B. K. Johnson, “The cones of the grass snake’s eyes,” Nature 178, 1285–1286 (1956).
[Crossref]

Vision Res. (6)

M. A. Ali, “Les reponses retinometrices: caracteres et mecanismes,” Vision Res. 11, 1225–1288 (1971).
[Crossref] [PubMed]

A. M. Snyder and C. Pask, “The Stiles–Crawford effect—explanation and consequences,” Vision Res. 13, 1115–1137 (1973).
[Crossref] [PubMed]

P. A. Liebman and A. M. Granda, “Microspectrophotometric measurements of visual pigments in two species of turtle, Pseudemys scripta and Chelonia mydas,” Vision Res. 11, 105–114 (1971).
[Crossref] [PubMed]

K. T. Brown, “A linear area centralis extending across the turtle retina and stabilized to the horizon by non-visual cues,” Vision Res. 9, 1053–1062 (1969).
[Crossref] [PubMed]

A. M. Granda and K. W. Haden, “Retinal oil globule counts and distributions in two species of turtle: Pseudemys scripta elegans(Wied) and Chelonia mydas mydas(Linnaeus),” Vision Res. 10, 79–84 (1970).
[Crossref] [PubMed]

J. K. Bowmaker and A. Knowles, “The visual pigments and oil droplets of the chicken retina,” Vision Res. 17, 755–764 (1977).
[Crossref] [PubMed]

Other (10)

G. H. Jacobs, Comparative Color Vision (Academic, New York, 1981).

J. A. Stratton, Electromagnetic Theory (McGraw-Hill, New York, 1941).

H. C. Van de Hulst, Light Scattering by Small Particles (Wiley, New York, 1957).

R. F. Harrington, Time-Harmonic Electromagnetic Fields (McGraw-Hill, New York, 1961).

M. Kerker, The Scattering of Light and Other Electromagnetic Radiation (Academic, New York, 1969).

G. L. Walls, The Vertebrate Eye and Its Adaptive Radiation (Cranbrook Institute of Science, Bloomfield Hills, Mich, 1942).
[Crossref]

S. R. Detweiler, Vertebrate Photoreceptors (Macmillan, New York, 1943).
[Crossref]

P. A. Liebman, Handbook of Sensory Physiology VII/1 (Springer-Verlag, Berlin, 1972).

R. W. Ditchburn, Light (Interscience, New York, 1953).

A. H. Bennett, H. Jupnik, H. Osterberg, and O. W. Richards, Phase Microscopy: Principles and Applications (Wiley, New York, 1951).

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Figures (5)

Fig. 1
Fig. 1

Cone oil droplets in the turtle retina. (a) Radial thick section of the photoreceptor layer. The fixation and the staining procedure used in preparing this tissue section caused the apparent color of the oil droplets to differ from that shown in (b). PE, pigment epithelial cells; CB, cell bodies; P, photoreceptor pedicles (synaptic endings); ROD, rod photoreceptor; ROS, rod outer segment; COS, cone outer segment; PG, pigment granules within the pigment epithelial cells. Oil droplets: RO, red; YO, yellow; OO, orange; CO, clear. Scale bar on lower right is 10 μm. (b) Flat mount from peripheral retina showing the highly refractile and intensely colored oil droplets. Oil droplets: RO, red; YO, yellow; OO, orange; CO, clear. Scale bar on lower right is 20 μm. A color plate showing this coloration can be seen in Ref. 19.

Fig. 2
Fig. 2

Oil-droplet diameter as a function of retinal location. The diameters of red (○), yellow (*), and clear (X) oil droplets have been measured along a line perpendicular to the visual streak. The visual streak is located at the position 0, and the measurements extend to the ora serrata.

Fig. 3
Fig. 3

Intensity enhancement behind an oil-dropletlike sphere. (a) The enhancement factors behind a 5-μm-diameter sphere are plotted along lines separated by 1.5-μm increments. The hatched region represents the location of a 10-μm-long outer segment, and the marks on the right-hand side indicate the baseline (zero enhancement) for each curve. Bar is 2.5 μm. (b) Third curve from the sphere surface in (a) is magnified and replotted with the ordinate indicating the magnitude of the enhancement factor.

Fig. 4
Fig. 4

Volume average enhancement factors for red, yellow, and clear oil droplets at different wavelengths of illumination. The two curves in each plot represent enhancement factors associated with peripheral (solid line) and visual streak (dashed line) oil droplets. (a) Red oil droplet. Refractive index, real component = 1.69. Diameter peripheral, 5.00 μm; visual streak, 3.00 μm. (b) Yellow oil droplet. Refractive index, real component, 1.55. Diameter: peripheral, 4.34 μm; visual streak, 2.60 μm. (c) Clear oil droplet. Refractive index, real component, 1.48. Diameter: peripheral, 3.82 μm; visual streak, 2.30 μm. For these calculations, the imaginary component of the refractive index was derived from the data of Liebman and Granda2 and Strother.15

Fig. 5
Fig. 5

Cone action spectra. Predicted cone sensitivities (X) are based on the volume average enhancement factors of Figs. 4(a)–4(c) and the relative photopigment absorbance data of Liebman and Granda.16 Predictions for the green- and the blue-sensitive cones were not extended to wavelengths greater than 620 and 550 nm, respectively, because of the poor signal-to-noise ratio present in the photopigment absorbance measurement at long wavelengths. Cone sensitivities recorded intracellularly (○) have been plotted for comparison.6 (a) Red-sensitive cone; (b) green-sensitive cone; (c) blue-sensitive cone.

Tables (3)

Tables Icon

Table 1 Oil-Droplet Diameter as a Function of Cone Type and Turtle Size

Tables Icon

Table 2 Outer Segment Dimensionsa

Tables Icon

Table 3 Oil-Droplet Index of Refraction Values (Real Component)a