Abstract

An indicator of individual retinal receptor response in the mammal is sought. This indicator must represent a detectable physical or chemical change of state in the receptor induced by the transducer of the photoreceptor. A histochemical technique has recently been described which results in differential staining between light-adapted and dark-adapted receptors.

In this experiment an attempt has been made to identify the action spectrum of this reaction in the predominantly rod retina of the albino rat. The action spectrum of this differential staining effect approximates that of rhodopsin.

The staining takes place in the ellipsoid portion of the receptor (in the inner segment). From other investigations, however, rhodopsin is known to be localized in the outer segments of such cells.

© 1964 Optical Society of America

Full Article  |  PDF Article

References

  • View by:
  • |
  • |
  • |

  1. J. M. Enoch, J. Opt. Soc. Am. 53, 71 (1963).
    [Crossref]
  2. J. M. Enoch, Invest. Ophthalmol. 2, 16 (1963).
  3. J. M. Enoch, “Physical Properties of the Retinal Receptor and Response of Retinal Receptors,” Psych. Bull. (to be published).
  4. K. Brown and T. Weisel, J. Physiol. 158, 229 cf. (1961).
  5. G. L. Walls, J. Comp. Psychol. 18, 363 (1934).
    [Crossref]
  6. K. S. Lashley, J. Comp. Psychol. 13, 173 (1932).
    [Crossref]
  7. E. N. Willmer, Ann. Rev. Physiol. 17, 339 (1955).
    [Crossref]
  8. F. Crescitelli and H. Dartnall, Nature 172, 195 (1953).
    [Crossref] [PubMed]
  9. F. D. Collins and R. A. Morton, Biochem. J. 47, 3 (1950).
  10. C. D. B. Bridges, Nature 184, 1727 (1959).
    [Crossref]
  11. C. H. Graham and L. A. Riggs, J. Gen. Psychol 12, 279 (1935).
    [Crossref]
  12. J. Dowling (personal communication).
  13. The fact that the effect is obtained when the dissected retina is exposed to light in vitro also rules out the necessity of absorption of the energy by the choroid or the pigment epithelium for this reaction to occur. Repetition of this experiment in vitro would eliminate reflectance factors.
  14. R. Granit, in The Eye, edited by H. Davson (Academic Press Inc., New York, 1962), Vol. 2, pp. 657 cf.
  15. E. Dodt and J. B. Walther, Arch. Ges. Physiol. 266, 187 (1958).
    [Crossref]
  16. K. Tansley, J. Physiol. 71, 442 (1931).
  17. Biochemist’s Handbook, edited by C. Long (D. Van Nostrand Company, Inc., Princeton, 1961), pp. 622–633.
  18. D. Keilin and E. C. Slater, Brit. Med. Bull. 9, 89 (1953).
  19. F. Sjostrand, J. Cellular Comp. Physiol. 42, 45 (1953).
    [Crossref]
  20. L. G. Elfvin, Exp. Cell Res. 5, 554 (1953).
    [Crossref] [PubMed]
  21. B. Fine, AMA Arch. Ophthalmol. 66, 847 (1961).
    [Crossref]
  22. H. Dartnall, Brit. Med. Bull. 9, 24 (1953).
  23. H. Dartnall, The Visual Pigments (Methuen and Company, Ltd., London, 1957).
  24. G. Wald, J. Gen. Physiol. 21, 795 (1938).
  25. D. Keilin and E. F. Hartree, Proc. Roy. Soc. (London) B127, 167 (1939).
  26. E. Margoliash (these data are found in Refs. 17 and 18).
  27. One may question the validity of plotting the absorption coefficient with the data describing log relative sensitivity (Fig. 6) since the absorption coefficient curves may be varied by changing the thickness of the absorbing layer (d) or by manipulating the concentration (r) of the absorbing material. (The values of d and r used by Margoliash are not given.) However, the author doubts that any such manipulation will provide a reasonable fit to the data presented in this experiment. The ellipsoid layer is only a few microns thick and the concentration of cytochromes cannot be very great.
  28. J. B. Neilands, Ann. Rev. Biochem. 27, 455 (1958).
    [Crossref]
  29. J. Dowling, J. Gen. Physiol. 46, 1287 (1963).
  30. In his article Dr. Cone briefly considers the role played by waveguide modal patterns in Dr. Dowling’s preparations. One tacit assumption made by Dr. Cone in the treatment of these data is that no changes in modal pattern occur during near-total bleaching. One may inquire as to the effect of extensive bleaching of the rhodopsin upon the indexes of refraction and the configuration of the receptor cell, and the interstitial matrix, etc. Small differences in physical characteristics and absorption become important when one considers the receptor as a waveguide. One may ask also whether the conditions employed by Dr. Dowling in his experiment favored the simultaneous transmission of multiple waveguide modal patterns? These questions are not raised in criticism of Dr. Dowling’s experiment, but rather are directed toward generalizations of Dr. Cone’s interpretation.
  31. R. Cone, J. Gen. Physiol. 46, 1267 (1963).
  32. D. Scarpelli and E. Craig, J. Cell Biol. 17, 279 (1963).
  33. N. Matsuo, Folia Ophthalmol. Japan 13, 1 (1962).
  34. Y. A. Vinnikov and L. K. Titova, Federation Proc. (Translation Suppl.) 22, 3 II, T401 (1963).
  35. K. H. Vosteen, Translations of Beltone Institute for Hearing Research, No. 16 (1963).

1963 (6)

J. M. Enoch, J. Opt. Soc. Am. 53, 71 (1963).
[Crossref]

J. M. Enoch, Invest. Ophthalmol. 2, 16 (1963).

J. Dowling, J. Gen. Physiol. 46, 1287 (1963).

R. Cone, J. Gen. Physiol. 46, 1267 (1963).

D. Scarpelli and E. Craig, J. Cell Biol. 17, 279 (1963).

Y. A. Vinnikov and L. K. Titova, Federation Proc. (Translation Suppl.) 22, 3 II, T401 (1963).

1962 (1)

N. Matsuo, Folia Ophthalmol. Japan 13, 1 (1962).

1961 (2)

K. Brown and T. Weisel, J. Physiol. 158, 229 cf. (1961).

B. Fine, AMA Arch. Ophthalmol. 66, 847 (1961).
[Crossref]

1959 (1)

C. D. B. Bridges, Nature 184, 1727 (1959).
[Crossref]

1958 (2)

J. B. Neilands, Ann. Rev. Biochem. 27, 455 (1958).
[Crossref]

E. Dodt and J. B. Walther, Arch. Ges. Physiol. 266, 187 (1958).
[Crossref]

1955 (1)

E. N. Willmer, Ann. Rev. Physiol. 17, 339 (1955).
[Crossref]

1953 (5)

F. Crescitelli and H. Dartnall, Nature 172, 195 (1953).
[Crossref] [PubMed]

D. Keilin and E. C. Slater, Brit. Med. Bull. 9, 89 (1953).

F. Sjostrand, J. Cellular Comp. Physiol. 42, 45 (1953).
[Crossref]

L. G. Elfvin, Exp. Cell Res. 5, 554 (1953).
[Crossref] [PubMed]

H. Dartnall, Brit. Med. Bull. 9, 24 (1953).

1950 (1)

F. D. Collins and R. A. Morton, Biochem. J. 47, 3 (1950).

1939 (1)

D. Keilin and E. F. Hartree, Proc. Roy. Soc. (London) B127, 167 (1939).

1938 (1)

G. Wald, J. Gen. Physiol. 21, 795 (1938).

1935 (1)

C. H. Graham and L. A. Riggs, J. Gen. Psychol 12, 279 (1935).
[Crossref]

1934 (1)

G. L. Walls, J. Comp. Psychol. 18, 363 (1934).
[Crossref]

1932 (1)

K. S. Lashley, J. Comp. Psychol. 13, 173 (1932).
[Crossref]

1931 (1)

K. Tansley, J. Physiol. 71, 442 (1931).

Bridges, C. D. B.

C. D. B. Bridges, Nature 184, 1727 (1959).
[Crossref]

Brown, K.

K. Brown and T. Weisel, J. Physiol. 158, 229 cf. (1961).

Collins, F. D.

F. D. Collins and R. A. Morton, Biochem. J. 47, 3 (1950).

Cone, R.

R. Cone, J. Gen. Physiol. 46, 1267 (1963).

Craig, E.

D. Scarpelli and E. Craig, J. Cell Biol. 17, 279 (1963).

Crescitelli, F.

F. Crescitelli and H. Dartnall, Nature 172, 195 (1953).
[Crossref] [PubMed]

Dartnall, H.

F. Crescitelli and H. Dartnall, Nature 172, 195 (1953).
[Crossref] [PubMed]

H. Dartnall, Brit. Med. Bull. 9, 24 (1953).

H. Dartnall, The Visual Pigments (Methuen and Company, Ltd., London, 1957).

Dodt, E.

E. Dodt and J. B. Walther, Arch. Ges. Physiol. 266, 187 (1958).
[Crossref]

Dowling, J.

J. Dowling, J. Gen. Physiol. 46, 1287 (1963).

J. Dowling (personal communication).

Elfvin, L. G.

L. G. Elfvin, Exp. Cell Res. 5, 554 (1953).
[Crossref] [PubMed]

Enoch, J. M.

J. M. Enoch, Invest. Ophthalmol. 2, 16 (1963).

J. M. Enoch, J. Opt. Soc. Am. 53, 71 (1963).
[Crossref]

J. M. Enoch, “Physical Properties of the Retinal Receptor and Response of Retinal Receptors,” Psych. Bull. (to be published).

Fine, B.

B. Fine, AMA Arch. Ophthalmol. 66, 847 (1961).
[Crossref]

Graham, C. H.

C. H. Graham and L. A. Riggs, J. Gen. Psychol 12, 279 (1935).
[Crossref]

Granit, R.

R. Granit, in The Eye, edited by H. Davson (Academic Press Inc., New York, 1962), Vol. 2, pp. 657 cf.

Hartree, E. F.

D. Keilin and E. F. Hartree, Proc. Roy. Soc. (London) B127, 167 (1939).

Keilin, D.

D. Keilin and E. C. Slater, Brit. Med. Bull. 9, 89 (1953).

D. Keilin and E. F. Hartree, Proc. Roy. Soc. (London) B127, 167 (1939).

Lashley, K. S.

K. S. Lashley, J. Comp. Psychol. 13, 173 (1932).
[Crossref]

Margoliash, E.

E. Margoliash (these data are found in Refs. 17 and 18).

Matsuo, N.

N. Matsuo, Folia Ophthalmol. Japan 13, 1 (1962).

Morton, R. A.

F. D. Collins and R. A. Morton, Biochem. J. 47, 3 (1950).

Neilands, J. B.

J. B. Neilands, Ann. Rev. Biochem. 27, 455 (1958).
[Crossref]

Riggs, L. A.

C. H. Graham and L. A. Riggs, J. Gen. Psychol 12, 279 (1935).
[Crossref]

Scarpelli, D.

D. Scarpelli and E. Craig, J. Cell Biol. 17, 279 (1963).

Sjostrand, F.

F. Sjostrand, J. Cellular Comp. Physiol. 42, 45 (1953).
[Crossref]

Slater, E. C.

D. Keilin and E. C. Slater, Brit. Med. Bull. 9, 89 (1953).

Tansley, K.

K. Tansley, J. Physiol. 71, 442 (1931).

Titova, L. K.

Y. A. Vinnikov and L. K. Titova, Federation Proc. (Translation Suppl.) 22, 3 II, T401 (1963).

Vinnikov, Y. A.

Y. A. Vinnikov and L. K. Titova, Federation Proc. (Translation Suppl.) 22, 3 II, T401 (1963).

Vosteen, K. H.

K. H. Vosteen, Translations of Beltone Institute for Hearing Research, No. 16 (1963).

Wald, G.

G. Wald, J. Gen. Physiol. 21, 795 (1938).

Walls, G. L.

G. L. Walls, J. Comp. Psychol. 18, 363 (1934).
[Crossref]

Walther, J. B.

E. Dodt and J. B. Walther, Arch. Ges. Physiol. 266, 187 (1958).
[Crossref]

Weisel, T.

K. Brown and T. Weisel, J. Physiol. 158, 229 cf. (1961).

Willmer, E. N.

E. N. Willmer, Ann. Rev. Physiol. 17, 339 (1955).
[Crossref]

AMA Arch. Ophthalmol. (1)

B. Fine, AMA Arch. Ophthalmol. 66, 847 (1961).
[Crossref]

Ann. Rev. Biochem. (1)

J. B. Neilands, Ann. Rev. Biochem. 27, 455 (1958).
[Crossref]

Ann. Rev. Physiol. (1)

E. N. Willmer, Ann. Rev. Physiol. 17, 339 (1955).
[Crossref]

Arch. Ges. Physiol. (1)

E. Dodt and J. B. Walther, Arch. Ges. Physiol. 266, 187 (1958).
[Crossref]

Biochem. J. (1)

F. D. Collins and R. A. Morton, Biochem. J. 47, 3 (1950).

Brit. Med. Bull. (2)

D. Keilin and E. C. Slater, Brit. Med. Bull. 9, 89 (1953).

H. Dartnall, Brit. Med. Bull. 9, 24 (1953).

Exp. Cell Res. (1)

L. G. Elfvin, Exp. Cell Res. 5, 554 (1953).
[Crossref] [PubMed]

Federation Proc. (Translation Suppl.) (1)

Y. A. Vinnikov and L. K. Titova, Federation Proc. (Translation Suppl.) 22, 3 II, T401 (1963).

Folia Ophthalmol. Japan (1)

N. Matsuo, Folia Ophthalmol. Japan 13, 1 (1962).

Invest. Ophthalmol. (1)

J. M. Enoch, Invest. Ophthalmol. 2, 16 (1963).

J. Cell Biol. (1)

D. Scarpelli and E. Craig, J. Cell Biol. 17, 279 (1963).

J. Cellular Comp. Physiol. (1)

F. Sjostrand, J. Cellular Comp. Physiol. 42, 45 (1953).
[Crossref]

J. Comp. Psychol. (2)

G. L. Walls, J. Comp. Psychol. 18, 363 (1934).
[Crossref]

K. S. Lashley, J. Comp. Psychol. 13, 173 (1932).
[Crossref]

J. Gen. Physiol. (3)

R. Cone, J. Gen. Physiol. 46, 1267 (1963).

J. Dowling, J. Gen. Physiol. 46, 1287 (1963).

G. Wald, J. Gen. Physiol. 21, 795 (1938).

J. Gen. Psychol (1)

C. H. Graham and L. A. Riggs, J. Gen. Psychol 12, 279 (1935).
[Crossref]

J. Opt. Soc. Am. (1)

J. Physiol. (2)

K. Brown and T. Weisel, J. Physiol. 158, 229 cf. (1961).

K. Tansley, J. Physiol. 71, 442 (1931).

Nature (2)

C. D. B. Bridges, Nature 184, 1727 (1959).
[Crossref]

F. Crescitelli and H. Dartnall, Nature 172, 195 (1953).
[Crossref] [PubMed]

Proc. Roy. Soc. (London) (1)

D. Keilin and E. F. Hartree, Proc. Roy. Soc. (London) B127, 167 (1939).

Other (10)

E. Margoliash (these data are found in Refs. 17 and 18).

One may question the validity of plotting the absorption coefficient with the data describing log relative sensitivity (Fig. 6) since the absorption coefficient curves may be varied by changing the thickness of the absorbing layer (d) or by manipulating the concentration (r) of the absorbing material. (The values of d and r used by Margoliash are not given.) However, the author doubts that any such manipulation will provide a reasonable fit to the data presented in this experiment. The ellipsoid layer is only a few microns thick and the concentration of cytochromes cannot be very great.

H. Dartnall, The Visual Pigments (Methuen and Company, Ltd., London, 1957).

K. H. Vosteen, Translations of Beltone Institute for Hearing Research, No. 16 (1963).

In his article Dr. Cone briefly considers the role played by waveguide modal patterns in Dr. Dowling’s preparations. One tacit assumption made by Dr. Cone in the treatment of these data is that no changes in modal pattern occur during near-total bleaching. One may inquire as to the effect of extensive bleaching of the rhodopsin upon the indexes of refraction and the configuration of the receptor cell, and the interstitial matrix, etc. Small differences in physical characteristics and absorption become important when one considers the receptor as a waveguide. One may ask also whether the conditions employed by Dr. Dowling in his experiment favored the simultaneous transmission of multiple waveguide modal patterns? These questions are not raised in criticism of Dr. Dowling’s experiment, but rather are directed toward generalizations of Dr. Cone’s interpretation.

J. M. Enoch, “Physical Properties of the Retinal Receptor and Response of Retinal Receptors,” Psych. Bull. (to be published).

Biochemist’s Handbook, edited by C. Long (D. Van Nostrand Company, Inc., Princeton, 1961), pp. 622–633.

J. Dowling (personal communication).

The fact that the effect is obtained when the dissected retina is exposed to light in vitro also rules out the necessity of absorption of the energy by the choroid or the pigment epithelium for this reaction to occur. Repetition of this experiment in vitro would eliminate reflectance factors.

R. Granit, in The Eye, edited by H. Davson (Academic Press Inc., New York, 1962), Vol. 2, pp. 657 cf.

Cited By

OSA participates in Crossref's Cited-By Linking service. Citing articles from OSA journals and other participating publishers are listed here.

Alert me when this article is cited.


Figures (7)

Fig. 1
Fig. 1

These are schematic drawings of typical retinal receptors. The cell to the left is a cone, and that to the right is a rod. Light ordinarily travels from the bottom of the page upward. The nucleus n, the external limiting membrane l, the ellipsoid e, and the outer segment o are indicated. The staining referred to in this paper takes place in the mitochondria-rich ellipsoid, and the photosensitive pigment has been localized in the outer segment. These drawings are taken from the work of the late G. L. Walls [G. L. Walls, The Vertebrate Eye (Cranbrook Institute of Science, Bloomfield Hills, Michigan, 1942)].

Fig. 2
Fig. 2

This figure is a schematic drawing of the instrument employed in this experiment.

Fig. 3
Fig. 3

Half-peak-magnitude bandwidths of the stimuli presented to the rat eyes are plotted as a function of wavelength.

Fig. 4
Fig. 4

This figure provides the reader with some concept of the nature of these data, and with some appreciation of interlot variability (main experiment) at λ=500 mμ. The black dots indicate positive judgments (stain or more stain observed in the light-adapted retinas), x’s indicate a mixed judgment by the three observers, and the open circles indicate no difference in observed stain between light- and dark-adapted retinas.

Fig. 5
Fig. 5

Summary data are presented. They have been taken from Column 6 of Table II A (black dots) and Table II B (white dot). These data represent the relative sensitivity of the staining reaction at the various wavelengths tested. These points are superimposed upon Dartnall’s visual pigment 502 (rhodopsin).22 Below one finds the representative peaks of the cytochromes. It will be noted that the β peak of cytochrome c most closely approaches the peak of this author’s data (500 mμ).

Fig. 6
Fig. 6

The same data which were plotted in Fig. 5 are reproduced at the bottom of this figure. They are superimposed on two sets of representative data describing cytochrome c in the oxidized (solid line) and the reduced state (dashed line). The absorption coefficient is derived from the function

Fig. 7
Fig. 7

These data were obtained from Lot 15. Note, the ordinate in this figure is not the same as in Fig. 4 (see text). The mean threshold values obtained during the main experiment (Column 5 of Table II A) are shown as dashed horizontal lines. The assigned thresholds for this lot are indicated as solid horizontal lines. The black dots indicate positive judgments (stain or more stain observed in the light-adapted retinas), x’s indicate a mixed judgment by the three observers, and the open circles indicate no difference in observed stain between light- and dark-adapted retinas.

Tables (3)

Tables Icon

Table I Incubation medium.

Tables Icon

Table II Threshold values.

Tables Icon

Table III Reflectance of oxalated rabbit blood, Dodt and Walther.a

Equations (4)

Equations on this page are rendered with MathJax. Learn more.

N = Q / q = Q / h ν = Q λ / h c = Q λ k ,
N = Q ( in ergs ) × λ ( in m μ ) × 5.03 × 10 8 .
N / t = P ( in μ W ) × λ ( in m μ ) × 5.03 × 10 9 ,
= ( 1 / d r ) log ( P 0 / P t ) ,