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. 1984 Dec;357:575–607. doi: 10.1113/jphysiol.1984.sp015518

The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis.

D A Baylor, B J Nunn, J L Schnapf
PMCID: PMC1193276  PMID: 6512705

Abstract

Visual transduction in rods of the cynomolgus monkey, Macaca fascicularis, was studied by recording membrane current from single outer segments projecting from small pieces of retina. Light flashes evoked transient outward-going photocurrents with saturating amplitudes of up to 34 pA. A flash causing twenty to fifty photoisomerizations gave a response of half the saturating amplitude. The response-stimulus relation was of the form 1-e-x where x is flash strength. The response to a dim flash usually had a time to peak of 150-250 ms and resembled the impulse response of a series of six low-pass filters. From the average spectral sensitivity of ten rods the rhodopsin was estimated to have a peak absorption near 491 nm. The spectral sensitivity of the rods was in good agreement with the average human scotopic visibility curve determined by Crawford (1949), when the human curve was corrected for lens absorption and self-screening of rhodopsin. Fluctuations in the photocurrent evoked by dim lights were consistent with a quantal event about 0.7 pA in peak amplitude. A steady light causing about 100 photoisomerizations s-1 reduced the flash sensitivity to half the dark-adapted value. At higher background levels the rod rapidly saturated. These results support the idea that dim background light desensitizes human scotopic vision by a mechanism central to the rod outer segments while scotopic saturation may occur within the outer segments. Recovery of the photocurrent after bright flashes was marked by quantized step-like events. The events had the properties expected if bleached rhodopsin in the disks occasionally caused an abrupt blockage of the dark current over about one-twentieth of the length of the outer segment. It is suggested that superposition of these events after bleaching may contribute to the threshold elevation measured psychophysically. The current in darkness showed random fluctuations which disappeared in bright light. The continuous component of the noise had a variance of about 0.03 pA2 and a power spectrum that fell to half near 3 Hz. A second component, consisting of discrete events resembling single-photon responses, was estimated to occur at a rate of 0.006 s-1. It is suggested that the continuous component of the noise may be removed from scotopic vision by a thresholding operation near the rod output.

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Selected References

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  1. Adelson E. H. Saturation and adaptation in the rod system. Vision Res. 1982;22(10):1299–1312. doi: 10.1016/0042-6989(82)90143-2. [DOI] [PubMed] [Google Scholar]
  2. Alpern M., Pugh E. N., Jr The density and photosensitivity of human rhodopsin in the living retina. J Physiol. 1974 Mar;237(2):341–370. doi: 10.1113/jphysiol.1974.sp010485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Attwell D., Wilson M. Behaviour of the rod network in the tiger salamander retina mediated by membrane properties of individual rods. J Physiol. 1980 Dec;309:287–315. doi: 10.1113/jphysiol.1980.sp013509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BARLOW H. B. Increment thresholds at low intensities considered as signal/noise discriminations. J Physiol. 1957 May 23;136(3):469–488. doi: 10.1113/jphysiol.1957.sp005774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. BLOUGH D. S., SCHRIER A. M. Scotopic spectral sensitivity in the monkey. Science. 1963 Feb 8;139(3554):493–494. doi: 10.1126/science.139.3554.493. [DOI] [PubMed] [Google Scholar]
  6. Bader C. R., Macleish P. R., Schwartz E. A. A voltage-clamp study of the light response in solitary rods of the tiger salamander. J Physiol. 1979 Nov;296:1–26. doi: 10.1113/jphysiol.1979.sp012988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Baylor D. A., Fettiplace R. Kinetics of synaptic transfer from receptors to ganglion cells in turtle retina. J Physiol. 1977 Oct;271(2):425–448. doi: 10.1113/jphysiol.1977.sp012007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Baylor D. A., Hodgkin A. L. Detection and resolution of visual stimuli by turtle photoreceptors. J Physiol. 1973 Oct;234(1):163–198. doi: 10.1113/jphysiol.1973.sp010340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Baylor D. A., Hodgkin A. L., Lamb T. D. The electrical response of turtle cones to flashes and steps of light. J Physiol. 1974 Nov;242(3):685–727. doi: 10.1113/jphysiol.1974.sp010731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Baylor D. A., Lamb T. D. Local effects of bleaching in retinal rods of the toad. J Physiol. 1982 Jul;328:49–71. doi: 10.1113/jphysiol.1982.sp014252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Baylor D. A., Lamb T. D., Yau K. W. Responses of retinal rods to single photons. J Physiol. 1979 Mar;288:613–634. [PMC free article] [PubMed] [Google Scholar]
  12. Baylor D. A., Lamb T. D., Yau K. W. The membrane current of single rod outer segments. J Physiol. 1979 Mar;288:589–611. [PMC free article] [PubMed] [Google Scholar]
  13. Baylor D. A., Matthews G., Nunn B. J. Location and function of voltage-sensitive conductances in retinal rods of the salamander, Ambystoma tigrinum. J Physiol. 1984 Sep;354:203–223. doi: 10.1113/jphysiol.1984.sp015372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Baylor D. A., Matthews G., Yau K. W. Temperature effects on the membrane current of retinal rods of the toad. J Physiol. 1983 Apr;337:723–734. doi: 10.1113/jphysiol.1983.sp014651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Baylor D. A., Matthews G., Yau K. W. Two components of electrical dark noise in toad retinal rod outer segments. J Physiol. 1980 Dec;309:591–621. doi: 10.1113/jphysiol.1980.sp013529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Bowmaker J. K., Dartnall H. J., Mollon J. D. Microspectrophotometric demonstration of four classes of photoreceptor in an old world primate, Macaca fascicularis. J Physiol. 1980 Jan;298:131–143. doi: 10.1113/jphysiol.1980.sp013071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Bowmaker J. K., Dartnall H. J. Visual pigments of rods and cones in a human retina. J Physiol. 1980 Jan;298:501–511. doi: 10.1113/jphysiol.1980.sp013097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Bridges C. D., Quilliam T. A. Visual pigments of men, moles and hedgehogs. Vision Res. 1973 Dec;13(12):2417–2421. doi: 10.1016/0042-6989(73)90239-3. [DOI] [PubMed] [Google Scholar]
  19. Bruch T. A. Rod-cone independence in dark adaptation. Vision Res. 1976;16(6):591–600. doi: 10.1016/0042-6989(76)90005-5. [DOI] [PubMed] [Google Scholar]
  20. Dartnall H. J., Bowmaker J. K., Mollon J. D. Human visual pigments: microspectrophotometric results from the eyes of seven persons. Proc R Soc Lond B Biol Sci. 1983 Nov 22;220(1218):115–130. doi: 10.1098/rspb.1983.0091. [DOI] [PubMed] [Google Scholar]
  21. De Valois R. L., Morgan H. C., Polson M. C., Mead W. R., Hull E. M. Psychophysical studies of monkey vision. I. Macaque luminosity and color vision tests. Vision Res. 1974 Jan;14(1):53–67. doi: 10.1016/0042-6989(74)90116-3. [DOI] [PubMed] [Google Scholar]
  22. Detwiler P. B., Conner J. D., Bodoia R. D. Gigaseal patch clamp recordings from outer segments of intact retinal rods. Nature. 1982 Nov 4;300(5887):59–61. doi: 10.1038/300059a0. [DOI] [PubMed] [Google Scholar]
  23. Detwiler P. B., Hodgkin A. L., McNaughton P. A. Temporal and spatial characteristics of the voltage response of rods in the retina of the snapping turtle. J Physiol. 1980 Mar;300:213–250. doi: 10.1113/jphysiol.1980.sp013159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. FUORTES M. G., GUNKEL R. D., RUSHTON W. A. Increment thresholds in a subject deficient in cone vision. J Physiol. 1961 Apr;156:179–192. doi: 10.1113/jphysiol.1961.sp006667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. FUORTES M. G., YEANDLE S. PROBABILITY OF OCCURRENCE OF DISCRETE POTENTIAL WAVES IN THE EYE OF LIMULUS. J Gen Physiol. 1964 Jan;47:443–463. doi: 10.1085/jgp.47.3.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Fain G. L. Sensitivity of toad rods: Dependence on wave-length and background illumination. J Physiol. 1976 Sep;261(1):71–101. doi: 10.1113/jphysiol.1976.sp011549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hagins W. A., Penn R. D., Yoshikami S. Dark current and photocurrent in retinal rods. Biophys J. 1970 May;10(5):380–412. doi: 10.1016/S0006-3495(70)86308-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Katz B., Miledi R. The statistical nature of the acetycholine potential and its molecular components. J Physiol. 1972 Aug;224(3):665–699. doi: 10.1113/jphysiol.1972.sp009918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lamb T. D. Effects of temperature changes on toad rod photocurrents. J Physiol. 1984 Jan;346:557–578. doi: 10.1113/jphysiol.1984.sp015041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lamb T. D., McNaughton P. A., Yau K. W. Spatial spread of activation and background desensitization in toad rod outer segments. J Physiol. 1981;319:463–496. doi: 10.1113/jphysiol.1981.sp013921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lamb T. D. Spontaneous quantal events induced in toad rods by pigment bleaching. Nature. 1980 Sep 25;287(5780):349–351. doi: 10.1038/287349a0. [DOI] [PubMed] [Google Scholar]
  32. Monjan A. A. Chromatic adaptation in the macaque. J Comp Physiol Psychol. 1966 Aug;62(1):76–83. doi: 10.1037/h0023481. [DOI] [PubMed] [Google Scholar]
  33. Naka K. I., Rushton W. A. S-potentials from colour units in the retina of fish (Cyprinidae). J Physiol. 1966 Aug;185(3):536–555. doi: 10.1113/jphysiol.1966.sp008001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Nunn B. J., Baylor D. A. Visual transduction in retinal rods of the monkey Macaca fascicularis. Nature. 1982 Oct 21;299(5885):726–728. doi: 10.1038/299726a0. [DOI] [PubMed] [Google Scholar]
  35. Nunn B. J., Schnapf J. L., Baylor D. A. Spectral sensitivity of single cones in the retina of Macaca fascicularis. Nature. 1984 May 17;309(5965):264–266. doi: 10.1038/309264a0. [DOI] [PubMed] [Google Scholar]
  36. Penn R. D., Hagins W. A. Kinetics of the photocurrent of retinal rods. Biophys J. 1972 Aug;12(8):1073–1094. doi: 10.1016/S0006-3495(72)86145-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. RUSHTON W. A. VISUAL ADAPTATION. Proc R Soc Lond B Biol Sci. 1965 Mar 16;162:20–46. doi: 10.1098/rspb.1965.0024. [DOI] [PubMed] [Google Scholar]
  38. Schnapf J. L., Copenhagen D. R. Differences in the kinetics of rod and cone synaptic transmission. Nature. 1982 Apr 29;296(5860):862–864. doi: 10.1038/296862a0. [DOI] [PubMed] [Google Scholar]
  39. Schnapf J. L. Dependence of the single photon response on longitudinal position of absorption in toad rod outer segments. J Physiol. 1983 Oct;343:147–159. doi: 10.1113/jphysiol.1983.sp014886. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Scholes J. Discontinuity of the excitation process in locust visual cells. Cold Spring Harb Symp Quant Biol. 1965;30:517–527. doi: 10.1101/sqb.1965.030.01.050. [DOI] [PubMed] [Google Scholar]
  41. WALD G., BROWN P. K. Human rhodopsin. Science. 1958 Jan 31;127(3292):222–226. doi: 10.1126/science.127.3292.222. [DOI] [PubMed] [Google Scholar]
  42. Zwas F., Alpern M. The density of human rhodopsin in the rods. Vision Res. 1976;16(2):121–127. doi: 10.1016/0042-6989(76)90088-2. [DOI] [PubMed] [Google Scholar]

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