Abstract

We investigated the low-frequency temporal response of the retina by measuring the corneal electroretinogram elicited by flickering lights. A sum of two temporal sine-wave modulations was used to generate difference frequencies between a 36-Hz standard stimulus and a series of low-frequency stimuli. The response of the retina at the difference frequency did not change as the low-frequency component of the stimulus was varied from 0.5 to 4 Hz. We also replicated an earlier study, stimulating the retina with a sum of two sine waves that were varied in average frequency but keeping the difference frequency constant. These data showed no change in the amplitude of the difference frequency as the average stimulus frequency was varied from 8 to almost 40 Hz. Taken together, the two sets of data support the notion that the in vivo early retinal response is low pass and extends without attenuation to frequencies greater than 30 Hz, in contrast to the sensitivity of the visual system measured by psychophysical techniques.

© 1996 Optical Society of America

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  1. J. L. Brown, “Flicker and intermittent stimulation,” in C. H. Graham, ed., Vision and Visual Perception, (Wiley, New York, 1965), pp. 251–320.
  2. H. de Lange, “Experiments on flicker and some calculations on an electrical analogue of the foveal systems,” Physica 18, 935–950 (1952).
    [CrossRef]
  3. D. H. Kelly, “Flicker,” in Handbook of Sensory Physiology, D. Jameson, L. M. Hurvich, eds., (Springer-Verlag, Berlin, 1972), Vol. VII/4, pp. 273–302.
    [CrossRef]
  4. D. H. Kelly, “Theory of flicker and transient responses. I. Uniform fields,” J. Opt. Soc. Am. 61, 537–546 (1971).
    [CrossRef] [PubMed]
  5. D. H. Kelly, “Diffusion model of linear flicker responses,” J. Opt. Soc. Am. 59, 1665–1670 (1969).
    [CrossRef] [PubMed]
  6. D. H. Kelly, H. R. Wilson, “Human flicker sensitivity two stages of retinal diffusion,” Science 202, 896–899 (1978).
    [CrossRef] [PubMed]
  7. S. A. Burns, A. E. Elsner, M. R. Kreitz, “Analysis of nonlinearities in the flicker ERG,” Optom. Vision Sci. 69, 95–105 (1992).
    [CrossRef]
  8. G. J. Burton, “Evidence for non-linear response processes in the human visual system from measurements on the thresholds of spatial beat frequencies,” Vision Res. 13, 1211–1225 (1973).
    [CrossRef] [PubMed]
  9. D. I. A. MacLeod, D. R. Williams, W. Makous, “A visual nonlinearity fed by single cones,” Vision Res. 32, 347–363 (1992).
    [CrossRef] [PubMed]
  10. L. W. Baitch, D. M. Levi, “Evidence for nonlinear binocular interactions in human visual cortex,” Vision Res. 28, 1139–1143 (1988).
    [CrossRef] [PubMed]
  11. M. P. Regan, D. M. Regan, “A frequency domain technique for characterizing nonlinearities in biological systems,” J. Theor. Biol. 133, 293–317 (1988).
    [CrossRef]
  12. H. Spekreijse, D. Reits, “Sequential analysis of the visual evoked potential system in man: nonlinear analysis of a sandwich system,” Ann. N. Y. Acad. Sci. 388, 72–97 (1982).
    [CrossRef] [PubMed]
  13. Y. Chang, S. A. Burns, M. R. Kreitz, “Red–green flicker photometry and nonlinearities in the flicker electroretinogram,” J. Opt. Soc. Am. A 10, 1413–1422 (1993).
    [CrossRef] [PubMed]
  14. J. L. Schnapf, B. J. Nunn, M. Meister, D. A. Baylor, “Visual transduction in cones of the monkey Macaca fascicularis,” J. Physiol. (London) 427, 681–713 (1990).
  15. R. F. Miller, J. E. Dowling, “Intracellular responses of the Muller (glial) cells of the mudpuppy retina: their relation to b-wave of the electroretinogram,” J. Neurophysiol. 33, 323–341 (1970).
    [PubMed]
  16. P. A. Sieving, R. H. Steinberg, “Contribution from proximal retina to intraretinal pattern ERG: the M-wave,” Invest. Ophthalmol. Vis. Sci. 26, 1642–1647 (1985).
    [PubMed]
  17. S. T. Hammett, A. T. Smith, “Temporal beats in the human visual system,” Vision Res. 21, 2833–2840 (1994).
    [CrossRef]
  18. A. Stockman, D. I. A. MacLeod, “Visible beats from invisible flickering lights: evidence that blue-sensitive cones respond to rapid flicker,” Invest. Ophthalmol. Vis. Sci. (Suppl.) 27, 71 (1986).
  19. B. Chen, W. Makous, D. R. Williams, “Serial spatial filters in vision,” Vision Res. 33, 413–427 (1993).
    [CrossRef] [PubMed]
  20. J. D. Victor, R. M. Shapley, B. W. Knight, “Nonlinear analysis of cat retinal ganglion cells in the frequency domain,” Proc. Nat. Acad. Sci. (USA) 74, 3068–3072 (1977).
    [CrossRef]
  21. F. A. Abraham, M. Alpern, D. B. Kirk, “Electroretinograms evoked by sinusoidal excitation of human cones,” J. Physiol. (London) 363, 135–150 (1985).
  22. J. V. Odom, D. Reits, N. Burgers, F. C. C. Riemslag, “Flicker electroretinograms: a system analytic approach,” Optom. Vision Sci. 69, 106–116 (1992).
    [CrossRef]
  23. C. L. Baker, R. F. Hess, B. T. Olsen, E. Zrenner, “Current source density analysis of linear and non-linear components of the primate electroretinogram,” J. Physiol. (London) 407, 155–176 (1988).
  24. P. A. Sieving, R. H. Steinberg, “Contribution from proximal retina to intraretinal pattern ERG the M-wave,” Invest. Ophthalmol. Vis. Sci. 26, 1642–1647 (1985).
    [PubMed]
  25. For a quadratic nonlinearity the difference frequency results from a multiplicative interaction of the two stimulus frequencies. Thus, if we decrease both stimuli by a factor of 2, we can expect the amplitude of the difference frequency to decrease by a factor of 4. The actual value obtained was approximately 5; however, because the S/N ratio of the low-modulation difference frequency did not meet our criteria for inclusion, the only conclusion we can safely draw is that the amplitude of the difference frequency is sensitive to changes in the stimulus. That is, there is no evidence that the response amplitude is saturated.
  26. G. Palm, “On representation and approximation of nonlinear systems,” Bio. Cybern. 34, 49–52 (1979).
    [CrossRef]
  27. S. Wu, S. A. Burns, A. E. Elsner, “Effects of flicker adaptation and temporal gain control on the flicker ERG,” Vision Res. 35, 2943–2953 (1995).
    [CrossRef] [PubMed]
  28. W. S. Baron, R. M. Boynton, R. W. Hammon, “Component analysis of the foveal local electroretinogram elicited with sinusoidal flicker,” Vision Res. 19, 479–490 (1979).
    [CrossRef] [PubMed]
  29. W. S. Baron, R. M. Boynton, “The primate foveal local electroretinogram an indicator of photoreceptor activity,” Vision Res. 14, 491–501 (1974).
    [CrossRef]
  30. R. A. Bush, P. A. Sieving, “Monkey 30 Hz flicker ERG is generated partially by activity post-synaptic to cones. Invest. Ophthalmol. Vis. Sci. (Suppl.) 34, 1273 (1993).
  31. R. A. Bush, P. A. Sieving, “Monkey intraretinal photopic ERG responses in vivoafter glutamate analogs. Invest. Ophthalmol. Vis. Sci. (Suppl.) 36, 445 (1995).
  32. D. I. A. MacLeod, S. He, “Visible flicker from invisible patterns,” Nature 361, 256–258 (1993).
    [CrossRef] [PubMed]

1995 (2)

S. Wu, S. A. Burns, A. E. Elsner, “Effects of flicker adaptation and temporal gain control on the flicker ERG,” Vision Res. 35, 2943–2953 (1995).
[CrossRef] [PubMed]

R. A. Bush, P. A. Sieving, “Monkey intraretinal photopic ERG responses in vivoafter glutamate analogs. Invest. Ophthalmol. Vis. Sci. (Suppl.) 36, 445 (1995).

1994 (1)

S. T. Hammett, A. T. Smith, “Temporal beats in the human visual system,” Vision Res. 21, 2833–2840 (1994).
[CrossRef]

1993 (4)

B. Chen, W. Makous, D. R. Williams, “Serial spatial filters in vision,” Vision Res. 33, 413–427 (1993).
[CrossRef] [PubMed]

D. I. A. MacLeod, S. He, “Visible flicker from invisible patterns,” Nature 361, 256–258 (1993).
[CrossRef] [PubMed]

Y. Chang, S. A. Burns, M. R. Kreitz, “Red–green flicker photometry and nonlinearities in the flicker electroretinogram,” J. Opt. Soc. Am. A 10, 1413–1422 (1993).
[CrossRef] [PubMed]

R. A. Bush, P. A. Sieving, “Monkey 30 Hz flicker ERG is generated partially by activity post-synaptic to cones. Invest. Ophthalmol. Vis. Sci. (Suppl.) 34, 1273 (1993).

1992 (3)

S. A. Burns, A. E. Elsner, M. R. Kreitz, “Analysis of nonlinearities in the flicker ERG,” Optom. Vision Sci. 69, 95–105 (1992).
[CrossRef]

D. I. A. MacLeod, D. R. Williams, W. Makous, “A visual nonlinearity fed by single cones,” Vision Res. 32, 347–363 (1992).
[CrossRef] [PubMed]

J. V. Odom, D. Reits, N. Burgers, F. C. C. Riemslag, “Flicker electroretinograms: a system analytic approach,” Optom. Vision Sci. 69, 106–116 (1992).
[CrossRef]

1990 (1)

J. L. Schnapf, B. J. Nunn, M. Meister, D. A. Baylor, “Visual transduction in cones of the monkey Macaca fascicularis,” J. Physiol. (London) 427, 681–713 (1990).

1988 (3)

C. L. Baker, R. F. Hess, B. T. Olsen, E. Zrenner, “Current source density analysis of linear and non-linear components of the primate electroretinogram,” J. Physiol. (London) 407, 155–176 (1988).

L. W. Baitch, D. M. Levi, “Evidence for nonlinear binocular interactions in human visual cortex,” Vision Res. 28, 1139–1143 (1988).
[CrossRef] [PubMed]

M. P. Regan, D. M. Regan, “A frequency domain technique for characterizing nonlinearities in biological systems,” J. Theor. Biol. 133, 293–317 (1988).
[CrossRef]

1986 (1)

A. Stockman, D. I. A. MacLeod, “Visible beats from invisible flickering lights: evidence that blue-sensitive cones respond to rapid flicker,” Invest. Ophthalmol. Vis. Sci. (Suppl.) 27, 71 (1986).

1985 (3)

P. A. Sieving, R. H. Steinberg, “Contribution from proximal retina to intraretinal pattern ERG: the M-wave,” Invest. Ophthalmol. Vis. Sci. 26, 1642–1647 (1985).
[PubMed]

F. A. Abraham, M. Alpern, D. B. Kirk, “Electroretinograms evoked by sinusoidal excitation of human cones,” J. Physiol. (London) 363, 135–150 (1985).

P. A. Sieving, R. H. Steinberg, “Contribution from proximal retina to intraretinal pattern ERG the M-wave,” Invest. Ophthalmol. Vis. Sci. 26, 1642–1647 (1985).
[PubMed]

1982 (1)

H. Spekreijse, D. Reits, “Sequential analysis of the visual evoked potential system in man: nonlinear analysis of a sandwich system,” Ann. N. Y. Acad. Sci. 388, 72–97 (1982).
[CrossRef] [PubMed]

1979 (2)

G. Palm, “On representation and approximation of nonlinear systems,” Bio. Cybern. 34, 49–52 (1979).
[CrossRef]

W. S. Baron, R. M. Boynton, R. W. Hammon, “Component analysis of the foveal local electroretinogram elicited with sinusoidal flicker,” Vision Res. 19, 479–490 (1979).
[CrossRef] [PubMed]

1978 (1)

D. H. Kelly, H. R. Wilson, “Human flicker sensitivity two stages of retinal diffusion,” Science 202, 896–899 (1978).
[CrossRef] [PubMed]

1977 (1)

J. D. Victor, R. M. Shapley, B. W. Knight, “Nonlinear analysis of cat retinal ganglion cells in the frequency domain,” Proc. Nat. Acad. Sci. (USA) 74, 3068–3072 (1977).
[CrossRef]

1974 (1)

W. S. Baron, R. M. Boynton, “The primate foveal local electroretinogram an indicator of photoreceptor activity,” Vision Res. 14, 491–501 (1974).
[CrossRef]

1973 (1)

G. J. Burton, “Evidence for non-linear response processes in the human visual system from measurements on the thresholds of spatial beat frequencies,” Vision Res. 13, 1211–1225 (1973).
[CrossRef] [PubMed]

1971 (1)

1970 (1)

R. F. Miller, J. E. Dowling, “Intracellular responses of the Muller (glial) cells of the mudpuppy retina: their relation to b-wave of the electroretinogram,” J. Neurophysiol. 33, 323–341 (1970).
[PubMed]

1969 (1)

1952 (1)

H. de Lange, “Experiments on flicker and some calculations on an electrical analogue of the foveal systems,” Physica 18, 935–950 (1952).
[CrossRef]

Abraham, F. A.

F. A. Abraham, M. Alpern, D. B. Kirk, “Electroretinograms evoked by sinusoidal excitation of human cones,” J. Physiol. (London) 363, 135–150 (1985).

Alpern, M.

F. A. Abraham, M. Alpern, D. B. Kirk, “Electroretinograms evoked by sinusoidal excitation of human cones,” J. Physiol. (London) 363, 135–150 (1985).

Baitch, L. W.

L. W. Baitch, D. M. Levi, “Evidence for nonlinear binocular interactions in human visual cortex,” Vision Res. 28, 1139–1143 (1988).
[CrossRef] [PubMed]

Baker, C. L.

C. L. Baker, R. F. Hess, B. T. Olsen, E. Zrenner, “Current source density analysis of linear and non-linear components of the primate electroretinogram,” J. Physiol. (London) 407, 155–176 (1988).

Baron, W. S.

W. S. Baron, R. M. Boynton, R. W. Hammon, “Component analysis of the foveal local electroretinogram elicited with sinusoidal flicker,” Vision Res. 19, 479–490 (1979).
[CrossRef] [PubMed]

W. S. Baron, R. M. Boynton, “The primate foveal local electroretinogram an indicator of photoreceptor activity,” Vision Res. 14, 491–501 (1974).
[CrossRef]

Baylor, D. A.

J. L. Schnapf, B. J. Nunn, M. Meister, D. A. Baylor, “Visual transduction in cones of the monkey Macaca fascicularis,” J. Physiol. (London) 427, 681–713 (1990).

Boynton, R. M.

W. S. Baron, R. M. Boynton, R. W. Hammon, “Component analysis of the foveal local electroretinogram elicited with sinusoidal flicker,” Vision Res. 19, 479–490 (1979).
[CrossRef] [PubMed]

W. S. Baron, R. M. Boynton, “The primate foveal local electroretinogram an indicator of photoreceptor activity,” Vision Res. 14, 491–501 (1974).
[CrossRef]

Brown, J. L.

J. L. Brown, “Flicker and intermittent stimulation,” in C. H. Graham, ed., Vision and Visual Perception, (Wiley, New York, 1965), pp. 251–320.

Burgers, N.

J. V. Odom, D. Reits, N. Burgers, F. C. C. Riemslag, “Flicker electroretinograms: a system analytic approach,” Optom. Vision Sci. 69, 106–116 (1992).
[CrossRef]

Burns, S. A.

S. Wu, S. A. Burns, A. E. Elsner, “Effects of flicker adaptation and temporal gain control on the flicker ERG,” Vision Res. 35, 2943–2953 (1995).
[CrossRef] [PubMed]

Y. Chang, S. A. Burns, M. R. Kreitz, “Red–green flicker photometry and nonlinearities in the flicker electroretinogram,” J. Opt. Soc. Am. A 10, 1413–1422 (1993).
[CrossRef] [PubMed]

S. A. Burns, A. E. Elsner, M. R. Kreitz, “Analysis of nonlinearities in the flicker ERG,” Optom. Vision Sci. 69, 95–105 (1992).
[CrossRef]

Burton, G. J.

G. J. Burton, “Evidence for non-linear response processes in the human visual system from measurements on the thresholds of spatial beat frequencies,” Vision Res. 13, 1211–1225 (1973).
[CrossRef] [PubMed]

Bush, R. A.

R. A. Bush, P. A. Sieving, “Monkey intraretinal photopic ERG responses in vivoafter glutamate analogs. Invest. Ophthalmol. Vis. Sci. (Suppl.) 36, 445 (1995).

R. A. Bush, P. A. Sieving, “Monkey 30 Hz flicker ERG is generated partially by activity post-synaptic to cones. Invest. Ophthalmol. Vis. Sci. (Suppl.) 34, 1273 (1993).

Chang, Y.

Chen, B.

B. Chen, W. Makous, D. R. Williams, “Serial spatial filters in vision,” Vision Res. 33, 413–427 (1993).
[CrossRef] [PubMed]

de Lange, H.

H. de Lange, “Experiments on flicker and some calculations on an electrical analogue of the foveal systems,” Physica 18, 935–950 (1952).
[CrossRef]

Dowling, J. E.

R. F. Miller, J. E. Dowling, “Intracellular responses of the Muller (glial) cells of the mudpuppy retina: their relation to b-wave of the electroretinogram,” J. Neurophysiol. 33, 323–341 (1970).
[PubMed]

Elsner, A. E.

S. Wu, S. A. Burns, A. E. Elsner, “Effects of flicker adaptation and temporal gain control on the flicker ERG,” Vision Res. 35, 2943–2953 (1995).
[CrossRef] [PubMed]

S. A. Burns, A. E. Elsner, M. R. Kreitz, “Analysis of nonlinearities in the flicker ERG,” Optom. Vision Sci. 69, 95–105 (1992).
[CrossRef]

Hammett, S. T.

S. T. Hammett, A. T. Smith, “Temporal beats in the human visual system,” Vision Res. 21, 2833–2840 (1994).
[CrossRef]

Hammon, R. W.

W. S. Baron, R. M. Boynton, R. W. Hammon, “Component analysis of the foveal local electroretinogram elicited with sinusoidal flicker,” Vision Res. 19, 479–490 (1979).
[CrossRef] [PubMed]

He, S.

D. I. A. MacLeod, S. He, “Visible flicker from invisible patterns,” Nature 361, 256–258 (1993).
[CrossRef] [PubMed]

Hess, R. F.

C. L. Baker, R. F. Hess, B. T. Olsen, E. Zrenner, “Current source density analysis of linear and non-linear components of the primate electroretinogram,” J. Physiol. (London) 407, 155–176 (1988).

Kelly, D. H.

D. H. Kelly, H. R. Wilson, “Human flicker sensitivity two stages of retinal diffusion,” Science 202, 896–899 (1978).
[CrossRef] [PubMed]

D. H. Kelly, “Theory of flicker and transient responses. I. Uniform fields,” J. Opt. Soc. Am. 61, 537–546 (1971).
[CrossRef] [PubMed]

D. H. Kelly, “Diffusion model of linear flicker responses,” J. Opt. Soc. Am. 59, 1665–1670 (1969).
[CrossRef] [PubMed]

D. H. Kelly, “Flicker,” in Handbook of Sensory Physiology, D. Jameson, L. M. Hurvich, eds., (Springer-Verlag, Berlin, 1972), Vol. VII/4, pp. 273–302.
[CrossRef]

Kirk, D. B.

F. A. Abraham, M. Alpern, D. B. Kirk, “Electroretinograms evoked by sinusoidal excitation of human cones,” J. Physiol. (London) 363, 135–150 (1985).

Knight, B. W.

J. D. Victor, R. M. Shapley, B. W. Knight, “Nonlinear analysis of cat retinal ganglion cells in the frequency domain,” Proc. Nat. Acad. Sci. (USA) 74, 3068–3072 (1977).
[CrossRef]

Kreitz, M. R.

Y. Chang, S. A. Burns, M. R. Kreitz, “Red–green flicker photometry and nonlinearities in the flicker electroretinogram,” J. Opt. Soc. Am. A 10, 1413–1422 (1993).
[CrossRef] [PubMed]

S. A. Burns, A. E. Elsner, M. R. Kreitz, “Analysis of nonlinearities in the flicker ERG,” Optom. Vision Sci. 69, 95–105 (1992).
[CrossRef]

Levi, D. M.

L. W. Baitch, D. M. Levi, “Evidence for nonlinear binocular interactions in human visual cortex,” Vision Res. 28, 1139–1143 (1988).
[CrossRef] [PubMed]

MacLeod, D. I. A.

D. I. A. MacLeod, S. He, “Visible flicker from invisible patterns,” Nature 361, 256–258 (1993).
[CrossRef] [PubMed]

D. I. A. MacLeod, D. R. Williams, W. Makous, “A visual nonlinearity fed by single cones,” Vision Res. 32, 347–363 (1992).
[CrossRef] [PubMed]

A. Stockman, D. I. A. MacLeod, “Visible beats from invisible flickering lights: evidence that blue-sensitive cones respond to rapid flicker,” Invest. Ophthalmol. Vis. Sci. (Suppl.) 27, 71 (1986).

Makous, W.

B. Chen, W. Makous, D. R. Williams, “Serial spatial filters in vision,” Vision Res. 33, 413–427 (1993).
[CrossRef] [PubMed]

D. I. A. MacLeod, D. R. Williams, W. Makous, “A visual nonlinearity fed by single cones,” Vision Res. 32, 347–363 (1992).
[CrossRef] [PubMed]

Meister, M.

J. L. Schnapf, B. J. Nunn, M. Meister, D. A. Baylor, “Visual transduction in cones of the monkey Macaca fascicularis,” J. Physiol. (London) 427, 681–713 (1990).

Miller, R. F.

R. F. Miller, J. E. Dowling, “Intracellular responses of the Muller (glial) cells of the mudpuppy retina: their relation to b-wave of the electroretinogram,” J. Neurophysiol. 33, 323–341 (1970).
[PubMed]

Nunn, B. J.

J. L. Schnapf, B. J. Nunn, M. Meister, D. A. Baylor, “Visual transduction in cones of the monkey Macaca fascicularis,” J. Physiol. (London) 427, 681–713 (1990).

Odom, J. V.

J. V. Odom, D. Reits, N. Burgers, F. C. C. Riemslag, “Flicker electroretinograms: a system analytic approach,” Optom. Vision Sci. 69, 106–116 (1992).
[CrossRef]

Olsen, B. T.

C. L. Baker, R. F. Hess, B. T. Olsen, E. Zrenner, “Current source density analysis of linear and non-linear components of the primate electroretinogram,” J. Physiol. (London) 407, 155–176 (1988).

Palm, G.

G. Palm, “On representation and approximation of nonlinear systems,” Bio. Cybern. 34, 49–52 (1979).
[CrossRef]

Regan, D. M.

M. P. Regan, D. M. Regan, “A frequency domain technique for characterizing nonlinearities in biological systems,” J. Theor. Biol. 133, 293–317 (1988).
[CrossRef]

Regan, M. P.

M. P. Regan, D. M. Regan, “A frequency domain technique for characterizing nonlinearities in biological systems,” J. Theor. Biol. 133, 293–317 (1988).
[CrossRef]

Reits, D.

J. V. Odom, D. Reits, N. Burgers, F. C. C. Riemslag, “Flicker electroretinograms: a system analytic approach,” Optom. Vision Sci. 69, 106–116 (1992).
[CrossRef]

H. Spekreijse, D. Reits, “Sequential analysis of the visual evoked potential system in man: nonlinear analysis of a sandwich system,” Ann. N. Y. Acad. Sci. 388, 72–97 (1982).
[CrossRef] [PubMed]

Riemslag, F. C. C.

J. V. Odom, D. Reits, N. Burgers, F. C. C. Riemslag, “Flicker electroretinograms: a system analytic approach,” Optom. Vision Sci. 69, 106–116 (1992).
[CrossRef]

Schnapf, J. L.

J. L. Schnapf, B. J. Nunn, M. Meister, D. A. Baylor, “Visual transduction in cones of the monkey Macaca fascicularis,” J. Physiol. (London) 427, 681–713 (1990).

Shapley, R. M.

J. D. Victor, R. M. Shapley, B. W. Knight, “Nonlinear analysis of cat retinal ganglion cells in the frequency domain,” Proc. Nat. Acad. Sci. (USA) 74, 3068–3072 (1977).
[CrossRef]

Sieving, P. A.

R. A. Bush, P. A. Sieving, “Monkey intraretinal photopic ERG responses in vivoafter glutamate analogs. Invest. Ophthalmol. Vis. Sci. (Suppl.) 36, 445 (1995).

R. A. Bush, P. A. Sieving, “Monkey 30 Hz flicker ERG is generated partially by activity post-synaptic to cones. Invest. Ophthalmol. Vis. Sci. (Suppl.) 34, 1273 (1993).

P. A. Sieving, R. H. Steinberg, “Contribution from proximal retina to intraretinal pattern ERG the M-wave,” Invest. Ophthalmol. Vis. Sci. 26, 1642–1647 (1985).
[PubMed]

P. A. Sieving, R. H. Steinberg, “Contribution from proximal retina to intraretinal pattern ERG: the M-wave,” Invest. Ophthalmol. Vis. Sci. 26, 1642–1647 (1985).
[PubMed]

Smith, A. T.

S. T. Hammett, A. T. Smith, “Temporal beats in the human visual system,” Vision Res. 21, 2833–2840 (1994).
[CrossRef]

Spekreijse, H.

H. Spekreijse, D. Reits, “Sequential analysis of the visual evoked potential system in man: nonlinear analysis of a sandwich system,” Ann. N. Y. Acad. Sci. 388, 72–97 (1982).
[CrossRef] [PubMed]

Steinberg, R. H.

P. A. Sieving, R. H. Steinberg, “Contribution from proximal retina to intraretinal pattern ERG: the M-wave,” Invest. Ophthalmol. Vis. Sci. 26, 1642–1647 (1985).
[PubMed]

P. A. Sieving, R. H. Steinberg, “Contribution from proximal retina to intraretinal pattern ERG the M-wave,” Invest. Ophthalmol. Vis. Sci. 26, 1642–1647 (1985).
[PubMed]

Stockman, A.

A. Stockman, D. I. A. MacLeod, “Visible beats from invisible flickering lights: evidence that blue-sensitive cones respond to rapid flicker,” Invest. Ophthalmol. Vis. Sci. (Suppl.) 27, 71 (1986).

Victor, J. D.

J. D. Victor, R. M. Shapley, B. W. Knight, “Nonlinear analysis of cat retinal ganglion cells in the frequency domain,” Proc. Nat. Acad. Sci. (USA) 74, 3068–3072 (1977).
[CrossRef]

Williams, D. R.

B. Chen, W. Makous, D. R. Williams, “Serial spatial filters in vision,” Vision Res. 33, 413–427 (1993).
[CrossRef] [PubMed]

D. I. A. MacLeod, D. R. Williams, W. Makous, “A visual nonlinearity fed by single cones,” Vision Res. 32, 347–363 (1992).
[CrossRef] [PubMed]

Wilson, H. R.

D. H. Kelly, H. R. Wilson, “Human flicker sensitivity two stages of retinal diffusion,” Science 202, 896–899 (1978).
[CrossRef] [PubMed]

Wu, S.

S. Wu, S. A. Burns, A. E. Elsner, “Effects of flicker adaptation and temporal gain control on the flicker ERG,” Vision Res. 35, 2943–2953 (1995).
[CrossRef] [PubMed]

Zrenner, E.

C. L. Baker, R. F. Hess, B. T. Olsen, E. Zrenner, “Current source density analysis of linear and non-linear components of the primate electroretinogram,” J. Physiol. (London) 407, 155–176 (1988).

Ann. N. Y. Acad. Sci. (1)

H. Spekreijse, D. Reits, “Sequential analysis of the visual evoked potential system in man: nonlinear analysis of a sandwich system,” Ann. N. Y. Acad. Sci. 388, 72–97 (1982).
[CrossRef] [PubMed]

Bio. Cybern. (1)

G. Palm, “On representation and approximation of nonlinear systems,” Bio. Cybern. 34, 49–52 (1979).
[CrossRef]

Invest. Ophthalmol. Vis. Sci. (2)

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Other (3)

For a quadratic nonlinearity the difference frequency results from a multiplicative interaction of the two stimulus frequencies. Thus, if we decrease both stimuli by a factor of 2, we can expect the amplitude of the difference frequency to decrease by a factor of 4. The actual value obtained was approximately 5; however, because the S/N ratio of the low-modulation difference frequency did not meet our criteria for inclusion, the only conclusion we can safely draw is that the amplitude of the difference frequency is sensitive to changes in the stimulus. That is, there is no evidence that the response amplitude is saturated.

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[CrossRef]

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Figures (4)

Fig. 1
Fig. 1

Logic of the variable stimulus experiment. The retina is stimulated with the sum of a 36-Hz sine-wave stimulus (Fs) and a 0.5-Hz sine wave, and a response is generated at the difference frequency (Fs − F1), as well as at other sum and difference frequencies. If the low-frequency stimulus is changed to F2, then the difference-frequency response changes frequency (Fs − F2). As long as the difference frequencies are nearly the same, we can treat the response of later retinal processing as identical. Thus changes in the response amplitude with changes in the variable frequency must arise from differences in the transmission of the low-frequency response to the nonlinearity.

Fig. 2
Fig. 2

Magnitude of the discrete Fourier transform from 24 to 36 Hz when the variable frequency stimulus was either 1, 2, 4, or 8 Hz (bottom to top, respectively). There are reliable response components both at 36 Hz (Fs) and at the difference frequency. Whereas the response amplitude at the difference frequency is relatively unchanged as the variable frequency changed from 1 to 4 Hz, it decreased for the 8-Hz condition (when Fs − F2 was 28 Hz). The responses have been displaced vertically for clarity of presentation.

Fig. 3
Fig. 3

Results for both conditions for each subject. (a) Plot of results of the standard technique for the sum of two sine waves for each observer. In this technique the difference frequency was always at 8 Hz, and the amplitude of the response at 8 Hz is plotted as a function of the average stimulus frequency. (b) Plot of the amplitude of the ERG response at the difference frequency when the eye was stimulated with the sum of a low-frequency stimulus and a 36-Hz stimulus, both at modulations of 0.5. The amplitude at the difference frequency is plotted as a function of the frequency of the low-frequency stimulus.

Fig. 4
Fig. 4

Comparison of the frequency response deduced for the initial linear filter (open symbols) and the total retinal response (filled symbols). Results have been averaged across subjects and have been normalized to a value of 1.0 at their estimated peaks. Most results from conditions that are believed to violate the assumptions of the methods (see text) have been omitted from the average, although the results from both experiments at 8 Hz are included for completeness.

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