Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1988 Oct;404:323–347. doi: 10.1113/jphysiol.1988.sp017292

The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque retina.

B B Lee 1, P R Martin 1, A Valberg 1
PMCID: PMC1190828  PMID: 3253435

Abstract

1. Heterochromatic flicker photometry is a way of measuring the spectral sensitivity of the human eye. Two lights of different colour are sinusoidally alternated at, typically, 10-20 Hz, and their relative intensities adjusted by the observer until the sensation of flicker is minimized. This technique has been used to define the human photopic luminosity, or V lambda, function on which photometry is based. 2. We have studied the responses of macaque retinal ganglion cells using this stimulus paradigm. The responses of the phasic ganglion cells go through a minimum at relative radiances very similar to that predicted from the V lambda function. At this point, defined as equal luminance, an abrupt change in response phase was observed. A small residual response at twice the flicker frequency was apparent under some conditions. 3. The spectral sensitivity of parafoveal phasic cells measured in this way corresponded very closely to that of human observers minimizing flicker on the same apparatus. 4. Minima in phasic cell activity were independent of flicker frequency, as is the case in the psychophysical task. 5. The response minima of phasic cells obey the laws of additivity and transitivity which are important characteristics of heterochromatic flicker photometry. 6. As the relative intensities of the lights were altered responses of tonic, spectrally opponent cells usually underwent a gradual phase change with vigorous responses at equal luminance. The responses of tonic cells treated individually or as a population could not be related to the V lambda function in any meaningful way. 7. We conclude that the phasic, magnocellular cell system of the primate visual pathway underlies performance in the psychophysical task of heterochromatic flicker photometry. It is likely that other tasks in which spectral sensitivity conforms to the V lambda function also rely on this cell system.

Full text

PDF
323

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baylor D. A., Nunn B. J., Schnapf J. L. Spectral sensitivity of cones of the monkey Macaca fascicularis. J Physiol. 1987 Sep;390:145–160. doi: 10.1113/jphysiol.1987.sp016691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Boynton R. M., Kaiser P. K. Vision: the additivity law made to work for heterochromatic photometry with bipartite fields. Science. 1968 Jul 26;161(3839):366–368. doi: 10.1126/science.161.3839.366. [DOI] [PubMed] [Google Scholar]
  5. Creutzfeldt O. D., Lee B. B., Elepfandt A. A quantitative study of chromatic organisation and receptive fields of cells in the lateral geniculate body of the rhesus monkey. Exp Brain Res. 1979 May 2;35(3):527–545. doi: 10.1007/BF00236770. [DOI] [PubMed] [Google Scholar]
  6. Crook J. M., Lee B. B., Tigwell D. A., Valberg A. Thresholds to chromatic spots of cells in the macaque geniculate nucleus as compared to detection sensitivity in man. J Physiol. 1987 Nov;392:193–211. doi: 10.1113/jphysiol.1987.sp016776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DE LANGE DZN H. Research into the dynamic nature of the human fovea-cortex systems with intermittent and modulated light. II. Phase shift in brithtness and delay in color perception. J Opt Soc Am. 1958 Nov;48(11):784–789. doi: 10.1364/josa.48.000784. [DOI] [PubMed] [Google Scholar]
  8. De Monasterio F. M., Gouras P. Functional properties of ganglion cells of the rhesus monkey retina. J Physiol. 1975 Sep;251(1):167–195. doi: 10.1113/jphysiol.1975.sp011086. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Derrington A. M., Krauskopf J., Lennie P. Chromatic mechanisms in lateral geniculate nucleus of macaque. J Physiol. 1984 Dec;357:241–265. doi: 10.1113/jphysiol.1984.sp015499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Derrington A. M., Lennie P. Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J Physiol. 1984 Dec;357:219–240. doi: 10.1113/jphysiol.1984.sp015498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dreher B., Fukada Y., Rodieck R. W. Identification, classification and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of old-world primates. J Physiol. 1976 Jun;258(2):433–452. doi: 10.1113/jphysiol.1976.sp011429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. ENROTH C. Spike frequency and flicker fusion frequency in retinal ganglion cells. Acta Physiol Scand. 1953 Jun 26;29(1):19–21. doi: 10.1111/j.1748-1716.1953.tb00993.x. [DOI] [PubMed] [Google Scholar]
  14. Frascella J., Lehmkuhle S. An electrophysiological assessment of X and Y cells as pattern and flicker detectors in the dorsal lateral geniculate nucleus of the cat. Exp Brain Res. 1984;55(1):117–126. doi: 10.1007/BF00240505. [DOI] [PubMed] [Google Scholar]
  15. Gouras P., Zrenner E. Enchancement of luminance flicker by color-opponent mechanisms. Science. 1979 Aug 10;205(4406):587–589. doi: 10.1126/science.109925. [DOI] [PubMed] [Google Scholar]
  16. Hicks T. P., Lee B. B., Vidyasagar T. R. The responses of cells in macaque lateral geniculate nucleus to sinusoidal gratings. J Physiol. 1983 Apr;337:183–200. doi: 10.1113/jphysiol.1983.sp014619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ingling C. R., Jr, Huong-Peng Tsou B., Gast T. J., Burns S. A., Emerick J. O., Riesenberg L. The achromatic channel. I. The non-linearity of minimum-border and flicker matches. Vision Res. 1978;18(4):379–390. doi: 10.1016/0042-6989(78)90047-0. [DOI] [PubMed] [Google Scholar]
  18. Kaiser P. K. Sensation luminance: a new name to distinguish CIE luminance from luminance dependent on an individual's spectral sensitivity. Vision Res. 1988;28(3):455–456. doi: 10.1016/0042-6989(88)90186-1. [DOI] [PubMed] [Google Scholar]
  19. Kaplan E., Shapley R. M. X and Y cells in the lateral geniculate nucleus of macaque monkeys. J Physiol. 1982 Sep;330:125–143. doi: 10.1113/jphysiol.1982.sp014333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kelly D. H., van Norren D. Two-band model of heterochromatic flicker. J Opt Soc Am. 1977 Aug;67(8):1081–1091. doi: 10.1364/josa.67.001081. [DOI] [PubMed] [Google Scholar]
  21. Lee B. B., Valberg A., Tigwell D. A., Tryti J. An account of responses of spectrally opponent neurons in macaque lateral geniculate nucleus to successive contrast. Proc R Soc Lond B Biol Sci. 1987 Apr 22;230(1260):293–314. doi: 10.1098/rspb.1987.0021. [DOI] [PubMed] [Google Scholar]
  22. Maffei L., Cervetto L., Fiorentini A. Transfer characteristics of excitation and inhibition in cat retinal ganglion cells. J Neurophysiol. 1970 Mar;33(2):276–284. doi: 10.1152/jn.1970.33.2.276. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Perry V. H., Oehler R., Cowey A. Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience. 1984 Aug;12(4):1101–1123. doi: 10.1016/0306-4522(84)90006-x. [DOI] [PubMed] [Google Scholar]
  25. Schiller P. H., Colby C. L. The responses of single cells in the lateral geniculate nucleus of the rhesus monkey to color and luminance contrast. Vision Res. 1983;23(12):1631–1641. doi: 10.1016/0042-6989(83)90177-3. [DOI] [PubMed] [Google Scholar]
  26. Spekreijse H., van Norren D., van den Berg T. J. Flicker responses in monkey lateral geniculate nucleus and human perception of flicker. Proc Natl Acad Sci U S A. 1971 Nov;68(11):2802–2805. doi: 10.1073/pnas.68.11.2802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stromeyer C. F., 3rd, Cole G. R., Kronauer R. E. Chromatic suppression of cone inputs to the luminance flicker mechanism. Vision Res. 1987;27(7):1113–1137. doi: 10.1016/0042-6989(87)90026-5. [DOI] [PubMed] [Google Scholar]
  28. Valberg A., Lee B. B., Tigwell D. A. Neurones with strong inhibitory S-cone inputs in the macaque lateral geniculate nucleus. Vision Res. 1986;26(7):1061–1064. doi: 10.1016/0042-6989(86)90040-4. [DOI] [PubMed] [Google Scholar]
  29. Valberg A., Lee B. B., Tryti J. Simulation of responses of spectrally-opponent neurones in the macaque lateral geniculate nucleus to chromatic and achromatic light stimuli. Vision Res. 1987;27(6):867–882. doi: 10.1016/0042-6989(87)90003-4. [DOI] [PubMed] [Google Scholar]
  30. Valberg A., Seim T., Lee B. B., Tryti J. Reconstruction of equidistant color space from responses of visual neurones of macaques. J Opt Soc Am A. 1986 Oct;3(10):1726–1734. doi: 10.1364/josaa.3.001726. [DOI] [PubMed] [Google Scholar]
  31. WALRAVEN P. L., LEEBEEK H. J. PHASE SHIFT OF SINUSOIDALLY ALTERNATING COLORED STIMULI. J Opt Soc Am. 1964 Jan;54:78–82. doi: 10.1364/josa.54.000078. [DOI] [PubMed] [Google Scholar]
  32. Wagner G., Boynton R. M. Comparison of four methods of heterochromatic photometry. J Opt Soc Am. 1972 Dec;62(12):1508–1515. doi: 10.1364/josa.62.001508. [DOI] [PubMed] [Google Scholar]
  33. Wiesel T. N., Hubel D. H. Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. J Neurophysiol. 1966 Nov;29(6):1115–1156. doi: 10.1152/jn.1966.29.6.1115. [DOI] [PubMed] [Google Scholar]
  34. de Monasterio F. M. Properties of concentrically organized X and Y ganglion cells of macaque retina. J Neurophysiol. 1978 Nov;41(6):1394–1417. doi: 10.1152/jn.1978.41.6.1394. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES