Abstract

We evaluated a technique for measuring temporal contrast sensitivities to sine-wave modulation driven by S-cones and rods in the perifovea using triple silent substitution. Isolating stimuli for S-cones and rods were created using an eight-channel, four-primary LED stimulator that has been validated before. Sensitivities were measured at 10 different temporal frequencies between 1 and 28 Hz in three normal observers at 14 different retinal illuminances between 0.07 and 587 photopic troland (phot Td) and at three different retinal illuminances over the same range in one S-cone monochromat. The technique was further validated by measuring bleaching adaptation in two normal subjects, demonstrating sufficient isolation in rods. Good isolation was apparent from the differences in the temporal contrast sensitivity functions and the sensitivity-versus-retinal illuminance functions between S-cones and rods, and also from the results in the S-cone monochromats and the delayed recovery of rod sensitivities after bleaching. The results will help to determine optimal stimulus conditions in future studies. The results in the S-cone monochromat demonstrate the potential clinical value of our protocol.

© 2017 Optical Society of America

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References

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2016 (3)

C. Huchzermeyer and J. Kremers, “Perifoveal L- and M-cone-driven temporal contrast sensitivities at different retinal illuminances,” J. Opt. Soc. Am. A 33, 1989–1998 (2016).
[Crossref]

J. S. Werner, “The Verriest lecture: short-wave-sensitive cone pathways across the life span,” J. Opt. Soc. Am. A 33, A104–A122 (2016).
[Crossref]

J. Maguire, N. R. A. Parry, J. Kremers, D. Kommanapalli, I. J. Murray, and D. J. McKeefry, “Rod electroretinograms elicited by silent substitution stimuli from the light-adapted human eye,” Trans. Vis. Sci. Technol. 5, 13 (2016).
[Crossref]

2015 (3)

J. Flamendorf, E. Agrón, W. T. Wong, D. Thompson, H. E. Wiley, E. L. Doss, S. Al-Holou, F. L. Ferris, E. Y. Chew, and C. Cukras, “Impairments in dark adaptation are associated with age-related macular degeneration severity and reticular pseudodrusen,” Ophthalmology 122, 2053–2062 (2015).
[Crossref]

C. Owsley, G. McGwin, M. E. Clark, G. R. Jackson, M. A. Callahan, L. B. Kline, C. D. Witherspoon, and C. A. Curcio, “Delayed rod-mediated dark adaptation is a functional biomarker for incident early age-related macular degeneration,” Ophthalmology 123, 344–351 (2015).

X. Luo, A. V. Cideciyan, A. Iannaccone, A. J. Roman, L. C. Ditta, B. J. Jennings, S. A. Yatsenko, R. Sheplock, A. Sumaroka, M. Swider, S. B. Schwartz, B. Wissinger, S. Kohl, and S. G. Jacobson, “Blue cone monochromacy: visual function and efficacy outcome measures for clinical trials,” PloS One 10, e0125700 (2015).
[Crossref]

2014 (2)

C. Huchzermeyer, J. Schlomberg, U. Welge-Lüssen, T. T. J. M. Berendschot, J. Pokorny, and J. Kremers, “Macular pigment optical density measured by heterochromatic modulation photometry,” PloS One 9, e110521 (2014).
[Crossref]

H. E. Smithson, “S-cone psychophysics,” Vis. Neurosci. 31, 211–225 (2014).
[Crossref]

2012 (1)

T. J. Sexton, M. Golczak, K. Palczewski, and R. N. V. Gelder, “Melanopsin is highly resistant to light and chemical bleaching in vivo,” J. Biol. Chem. 287, 20888–20897 (2012).
[Crossref]

2011 (1)

B. Feigl, D. Cao, C. P. Morris, and A. J. Zele, “Persons with age-related maculopathy risk genotypes and clinically normal eyes have reduced mesopic vision,” Invest. Ophthalmol. Visual Sci. 52, 1145–1150 (2011).
[Crossref]

2010 (1)

D. Cao, B. B. Lee, and H. Sun, “Combination of rod and cone inputs in parasol ganglion cells of the magnocellular pathway,” J. Vis. 10(11), 4 (2010).
[Crossref]

2009 (1)

C. Ripamonti, W. L. Woo, E. Crowther, and A. Stockman, “The S-cone contribution to luminance depends on the M- and L-cone adaptation levels: silent surrounds?” J. Vis. 9(3), 10 (2009).
[Crossref]

2008 (1)

D. Cao, J. Pokorny, V. C. Smith, and A. J. Zele, “Rod contributions to color perception: linear with rod contrast,” Vis. Res. 48, 2586–2592 (2008).
[Crossref]

2007 (1)

2005 (3)

M. J. H. Puts, J. Pokorny, J. Quinlan, and L. Glennie, “Audiophile hardware in vision science; the soundcard as a digital to analog converter,” J. Neurosci. Methods 142, 77–81 (2005).
[Crossref]

D. Cao, J. Pokorny, and V. C. Smith, “Matching rod percepts with cone stimuli,” Vis. Res. 45, 2119–2128 (2005).
[Crossref]

D. M. Dacey, H.-W. Liao, B. B. Peterson, F. R. Robinson, V. C. Smith, J. Pokorny, K.-W. Yau, and P. D. Gamlin, “Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN,” Nature 433, 749–754 (2005).
[Crossref]

2004 (1)

J. Pokorny, H. Smithson, and J. Quinlan, “Photostimulator allowing independent control of rods and the three cone types,” Vis. Neurosci. 21, 263–267 (2004).
[Crossref]

2002 (2)

D. M. Berson, F. A. Dunn, and M. Takao, “Phototransduction by retinal ganglion cells that set the circadian clock,” Science 295, 1070–1073 (2002).
[Crossref]

A. G. Shapiro, “Cone-specific mediation of rod sensitivity in trichromatic observers,” Invest. Ophthalmol. Visual Sci. 43, 898–905 (2002).

2001 (2)

H. Sun, J. Pokorny, and V. C. Smith, “Rod-cone interactions assessed in inferred magnocellular and parvocellular postreceptoral pathways,” J. Vis. 1(1), 42–54 (2001).
[Crossref]

H. Sun, J. Pokorny, and V. C. Smith, “Control of the modulation of human photoreceptors,” Color Res. Appl. 26, S69–S75 (2001).
[Crossref]

2000 (1)

A. Stockman and L. T. Sharpe, “The spectral sensitivities of the middle- and long-wavelength-sensitive cones derived from measurements in observers of known genotype,” Vis. Res. 40, 1711–1737 (2000).
[Crossref]

1999 (4)

L. T. Sharpe and A. Stockman, “Rod pathways: the importance of seeing nothing,” Trends Neurosci. 22, 497–504 (1999).
[Crossref]

J. Kremers and S. Meierkord, “Rod-cone-interactions in deuteranopic observers: models and dynamics,” Vis. Res. 39, 3372–3385 (1999).
[Crossref]

A. Stockman, L. T. Sharpe, and C. Fach, “The spectral sensitivity of the human short-wavelength sensitive cones derived from thresholds and color matches,” Vis. Res. 39, 2901–2927 (1999).
[Crossref]

G. Haegerstrom-Portnoy and W. A. Verdon, “Rods induce transient tritanopia in blue cone monochromats,” Vis. Res. 39, 2275–2284 (1999).
[Crossref]

1996 (2)

1994 (1)

S. L. Buck and R. Knight, “Partial additivity of rod signals with M- and L-cone signals in increment detection,” Vis. Res. 34, 2537–2545 (1994).
[Crossref]

1993 (1)

1992 (3)

B. J. Lachenmayr and M. Gleissner, “Flicker perimetry resists retinal image degradation,” Invest. Ophthalmol. Visual Sci. 33, 3539–3542 (1992).

N. Graham and D. C. Hood, “Modeling the dynamics of light adaptation: the merging of two traditions,” Vis. Res. 32, 1373–1393 (1992).
[Crossref]

R. A. Bone, J. T. Landrum, and A. Cains, “Optical density spectra of the macular pigment in vivo and in vitro,” Vis. Res. 32, 105–110 (1992).
[Crossref]

1991 (3)

A. Stockman, D. I. A. MacLeod, and D. D. DePriest, “The temporal properties of the human short-wave photoreceptors and their associated pathways,” Vis. Res. 31, 189–208 (1991).
[Crossref]

C. A. Curcio, K. A. Allen, K. R. Sloan, C. L. Lerea, J. B. Hurley, I. B. Klock, and A. H. Milam, “Distribution and morphology of human cone photoreceptors stained with anti-blue opsin,” J. Comp. Neurol. 312, 610–624 (1991).
[Crossref]

C. H. Sung, C. M. Davenport, J. C. Hennessey, I. H. Maumenee, S. G. Jacobson, J. R. Heckenlively, R. Nowakowski, G. Fishman, P. Gouras, and J. Nathans, “Rhodopsin mutations in autosomal dominant retinitis pigmentosa,” Proc. Natl. Acad. Sci. USA 88, 6481–6485 (1991).
[Crossref]

1989 (4)

V. C. Greenstein, D. C. Hood, R. Ritch, D. Steinberger, and R. E. Carr, “S (blue) cone pathway vulnerability in retinitis pigmentosa, diabetes and glaucoma,” Invest. Ophthalmol. Visual Sci. 30, 1732–1737 (1989).

L. T. Sharpe, A. Stockman, and D. I. MacLeod, “Rod flicker perception: scotopic duality, phase lags and destructive interference,” Vis. Res. 29, 1539–1559 (1989).
[Crossref]

L. T. Sharpe, C. Fach, K. Nordby, and A. Stockman, “The incremental threshold of the rod visual system and Weber’s law,” Science 244, 354–356 (1989).
[Crossref]

R. F. Hess, K. T. Mullen, and E. Zrenner, “Human photopic vision with only short wavelength cones: post-receptoral properties,” J. Physiol. 417, 151–172 (1989).
[Crossref]

1987 (1)

J. S. Werner, S. K. Donnelly, and R. Kliegl, “Aging and human macular pigment density: appended with translations from the work of Max Schultze and Ewald Hering,” Vis. Res. 27, 257–268 (1987).
[Crossref]

1984 (3)

K. R. Alexander and G. A. Fishman, “Rod-cone interaction in flicker perimetry,” Br. J. Ophthalmol. 68, 303–309 (1984).
[Crossref]

N. J. Coletta and A. J. Adams, “Rod-cone interaction in flicker detection,” Vis. Res. 24, 1333–1340 (1984).
[Crossref]

D. C. Hood, N. I. Benimoff, and V. C. Greenstein, “The response range of the blue-cone pathways: a source of vulnerability to disease,” Invest. Ophthalmol. Visual Sci. 25, 864–867 (1984).

1983 (1)

S. H. Goldberg, T. E. Frumkes, and R. W. Nygaard, “Inhibitory influence of unstimulated rods in the human retina: evidence provided by examining cone flicker,” Science 221, 180–182 (1983).
[Crossref]

1982 (3)

J. D. Conner, “The temporal properties of rod vision,” J. Physiol. 332, 139–155 (1982).
[Crossref]

O. Estevez and H. Spekreijse, “The ‘silent substitution’ method in visual research,” Vis. Res. 22, 681–691 (1982).
[Crossref]

R. W. Nygaard and T. E. Frumkes, “Calibration of the retinal illuminance provided by Maxwellian views,” Vis. Res. 22, 433–434 (1982).
[Crossref]

1981 (2)

C. R. Genter and N. Weisstein, “Flickering phantoms: a motion illusion without motion,” Vis. Res. 21, 963–966 (1981).
[Crossref]

D. R. Williams, D. I. A. MacLeod, and M. M. Hayhoe, “Punctate sensitivity of the blue-sensitive mechanism,” Vis. Res. 21, 1357–1375 (1981).
[Crossref]

1980 (1)

J. J. Wisowaty and R. M. Boynton, “Temporal modulation sensitivity of the blue mechanism: measurements made without chromatic adaptation,” Vis. Res. 20, 895–909 (1980).
[Crossref]

1978 (1)

R. M. Boynton and P. K. Kaiser, “Temporal analog of the minimally distinct border,” Vis. Res. 18, 111–113 (1978).
[Crossref]

1977 (2)

1975 (1)

E. N. Pugh, “Rushton’s paradox: rod dark adaptation after flash photolysis,” J. Physiol. 248, 413–431 (1975).
[Crossref]

1974 (1)

1973 (1)

D. H. Kelly and R. E. Savoie, “A study of sine-wave contrast sensitivity by two psychophysical methods,” Percept. Psychophys. 14, 313–318 (1973).
[Crossref]

1972 (1)

D. I. MacLeod, “Rods cancel cones in flicker,” Nature 235, 173–174 (1972).
[Crossref]

1967 (1)

M. M. Taylor and C. D. Creelman, “PEST: efficient estimates on probability functions,” J. Acoust. Soc. Am. 41, 782–787 (1967).http://www.cvrl.org/.
[Crossref]

1966 (1)

G. S. Brindley, J. J. Du Croz, and W. A. Rushton, “The flicker fusion frequency of the blue-sensitive mechanism of colour vision,” J. Physiol. 183, 497–500 (1966).
[Crossref]

1954 (1)

1949 (1)

B. H. Crawford, “The scotopic visibility function,” Proc. Phys. Soc. B 62, 321–334 (1949).
[Crossref]

1945 (1)

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X. Luo, A. V. Cideciyan, A. Iannaccone, A. J. Roman, L. C. Ditta, B. J. Jennings, S. A. Yatsenko, R. Sheplock, A. Sumaroka, M. Swider, S. B. Schwartz, B. Wissinger, S. Kohl, and S. G. Jacobson, “Blue cone monochromacy: visual function and efficacy outcome measures for clinical trials,” PloS One 10, e0125700 (2015).
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C. Owsley, G. McGwin, M. E. Clark, G. R. Jackson, M. A. Callahan, L. B. Kline, C. D. Witherspoon, and C. A. Curcio, “Delayed rod-mediated dark adaptation is a functional biomarker for incident early age-related macular degeneration,” Ophthalmology 123, 344–351 (2015).

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Figures (7)

Fig. 1.
Fig. 1. tCSFs of three normal, trichromatic subjects for S-cone- (blue triangles, dotted lines) and rod-isolating stimuli (black diamonds, broken lines) at the different retinal illuminances. As a reference, the tCSFs for L-cones (red squares) and M-cones (green circles) are shown in the background [3].
Fig. 2.
Fig. 2. SVI curves for the S-cone-isolating stimuli at different temporal frequencies (blue triangles, dotted lines). This plot shows the averaged data of the three color normal observers (error bars: standard deviation). The SVI curves for L- and M-cones are shown for reference (L-cones, red squares; M-cones, green circles) [3].
Fig. 3.
Fig. 3. Parameters obtained from fits of a combined linear model to the SVI data. The fits are shown together with the SVI curves in Figs. 2 (for S-cones) and 6 (for rods). The upper plot shows the estimated Weber threshold of the model for L-, M-, and S-cones as a function of temporal frequency (L-cones, red squares; M-cones, green circles; S-cones, blue triangles). The lower plot shows the slope of the ascending portion of the combined model from L-, M- and S-cones and of a simple linear model for rods (black diamonds). The latter was chosen because the rod data were not well described by the combined linear model under most circumstances.
Fig. 4.
Fig. 4. Dark adaptation after bleaching. The contrast threshold to a sinusoidal stimulus at low mesopic retinal illuminance (mean: 0.59 phot Td) is shown as a function of time after bleaching with an intense (50,000 phot Td) white light for 4 min (subject JK; L-cones, red squares; M-cones, green circles; rods, black diamonds). Exponential functions were fit to the threshold data. The baseline thresholds before bleaching are shown as horizontal lines (L-cones, red solid line; M-cones, green dashed line; rods, black broken line).
Fig. 5.
Fig. 5. Recovery of contrast threshold with time for rod-isolating stimuli at 4 Hz and 10 Hz and at different retinal illuminances (mean: 0.59 phot Td) after bleaching with a 20,000 phot Td white light for 2 min (subject CH). Again, exponential functions were fitted to these measurements.
Fig. 6.
Fig. 6. Averaged SVI curves of the three color-normal observers for rod-isolating stimuli for different temporal frequencies (black diamonds). The combined linear model did not describe these data well. Therefore, we show a simple linear model that has been fit to the rod data. Error bars represent the standard deviation. As in Fig. 2, the SVI curves for L- and M-cones are shown for reference (L-cones, red squares; M-cones, green circles) [3].
Fig. 7.
Fig. 7. tCSFs to S-cone and rod-isolating stimuli at three different retinal illuminances in one subject with S-cone monochromacy (S-cones, blue triangles; rods, black diamonds). With our protocol, good measurements were possible despite severe visual disability, glare sensitivity, and fixation nystagmus. For comparison, a smoothed curve and the standard error of the mean (SEM) fitted to the tCSFs of the normal subjects is also shown.

Tables (4)

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Table 1. LED Contrasts at the Instrument Gamut for the Four Different Isolating Stimulia

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Table 2. Calculation of Residual Modulation in the Targeted and the “Silenced” Photoreceptor Types When Assumptions That Were Made for the Calculation of the Stimuli Do Not Holda

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Table 3. Parameters of the Exponential Functions That Were Fitted to the Dark Adaptation Thresholds after Bleaching: Comparison between Photoreceptor Types

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Table 4. Parameters of the Exponential Functions That Were Fitted to the Dark Adaptation Thresholds after Bleaching: Rod Thresholds at Different Conditionsa

Equations (3)

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D media = ( . 225 + 3.1 × 10 5 · age 2 ) × ( 400 λ ) 4 + 14.19 × 10.68 × exp ( [ . 057 × ( λ 273 ) ] 2 ) + 2.13 ( . 998 6.3 × 10 5 × age 2 ) × exp ( [ . 029 ( λ 370 ) ] 2 ) + 11.95 ( . 059 + 18.6 × 10 5 × age 2 ) × exp ( [ . 021 ( λ 325 ) ] 2 ) + 1.43 ( . 016 + 13.2 × 10 5 × age 2 ) × exp ( [ . 008 ( λ 325 ) ] 2 ) + . 111 .
S = { I weber · a + b = const. for    I > I weber I · a + b for    I I weber .
Threshold ( t ) = a + b · e t τ ,

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