Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1987 Aug;389:1–21. doi: 10.1113/jphysiol.1987.sp016643

Inhibitory interactions in the human vision system revealed in pattern-evoked potentials.

D C Burr 1, M C Morrone 1
PMCID: PMC1192067  PMID: 3681721

Abstract

1. Visual evoked potentials (v.e.p.s) were recorded from human adults to investigate orientation-specific neural interactions. The stimuli were the sum of two gratings, sinusoidally modulated in space and time at different frequencies. Recordings were made for one grating (test) alone, and with another superimposed grating (mask), oriented parallel or orthogonal to the test. The amplitude and phase of the v.e.p.s at twice the test modulation frequency (second harmonic) was measured as a function of test contrast to produce contrast-response curves. 2. Orthogonal masks attenuated considerably the amplitude of v.e.p.s. The attenuation at any given contrast was approximately proportional, or multiplicative, lowering the slope of the contrast-response curve, without affecting significantly the extrapolated threshold. Parallel masks also attenuated v.e.p. amplitudes but in a different way, leaving the slope of the contrast-response curves unchanged, while elevating threshold. 3. The attenuation by orthogonal masks occurred over a wide range of test spatial frequencies, from 0.8 to 8 cycles/deg. For any given test spatial frequency, the most effective masks were those of spatial frequency similar to or lower than the test. Masks of spatial frequency 1.5 octaves higher than the test did not attenuate v.e.p. amplitudes. 4. The mask temporal frequency for maximal attenuation of v.e.p. amplitude was around 12 Hz, with stationary masks having little effect. 5. Under most conditions, the phase of the second harmonic of the v.e.p., increased with increasing contrast (phase advance). Superimposition of a parallel mask abolished phase advance, while orthogonal masks increased it. 6. Comparisons with single cortical unit and evoked potential recordings in cats suggest that the attenuation by orthogonal masks reflects intracortical inhibitory interactions between cell populations of different orientation preference.

Full text

PDF
1

Selected References

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

  1. Albrecht D. G., Farrar S. B., Hamilton D. B. Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. J Physiol. 1984 Feb;347:713–739. doi: 10.1113/jphysiol.1984.sp015092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Albrecht D. G., Hamilton D. B. Striate cortex of monkey and cat: contrast response function. J Neurophysiol. 1982 Jul;48(1):217–237. doi: 10.1152/jn.1982.48.1.217. [DOI] [PubMed] [Google Scholar]
  3. Anderson S. J., Burr D. C. Spatial and temporal selectivity of the human motion detection system. Vision Res. 1985;25(8):1147–1154. doi: 10.1016/0042-6989(85)90104-x. [DOI] [PubMed] [Google Scholar]
  4. Benevento L. A., Creutzfeldt O. D., Kuhnt U. Significance of intracortical inhibition in the visual cortex. Nat New Biol. 1972 Jul 26;238(82):124–126. doi: 10.1038/newbio238124a0. [DOI] [PubMed] [Google Scholar]
  5. Berardi N., Morrone M. C. The role of gamma-aminobutyric acid mediated inhibition in the response properties of cat lateral geniculate nucleus neurones. J Physiol. 1984 Dec;357:505–523. doi: 10.1113/jphysiol.1984.sp015514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bishop P. O., Coombs J. S., Henry G. H. Receptive fields of simple cells in the cat striate cortex. J Physiol. 1973 May;231(1):31–60. doi: 10.1113/jphysiol.1973.sp010218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blakemore C., Hague B. Evidence for disparity detecting neurones in the human visual system. J Physiol. 1972 Sep;225(2):437–455. doi: 10.1113/jphysiol.1972.sp009948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bobak P., Bodis-Wollner I., Harnois C., Thornton J. VEPs in humans reveal high and low spatial contrast mechanisms. Invest Ophthalmol Vis Sci. 1984 Aug;25(8):980–983. [PubMed] [Google Scholar]
  9. Burr D. C., Ross J., Morrone M. C. Local regulation of luminance gain. Vision Res. 1985;25(5):717–727. doi: 10.1016/0042-6989(85)90178-6. [DOI] [PubMed] [Google Scholar]
  10. Burr D., Morrone C., Maffei L. Intra-cortical inhibition prevents simple cells from responding to textured visual patterns. Exp Brain Res. 1981;43(3-4):455–458. doi: 10.1007/BF00238391. [DOI] [PubMed] [Google Scholar]
  11. Campbell F. W., Kulikowski J. J. Orientational selectivity of the human visual system. J Physiol. 1966 Nov;187(2):437–445. doi: 10.1113/jphysiol.1966.sp008101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Campbell F. W., Maffei L. Electrophysiological evidence for the existence of orientation and size detectors in the human visual system. J Physiol. 1970 May;207(3):635–652. doi: 10.1113/jphysiol.1970.sp009085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Daugman J. G. Two-dimensional spectral analysis of cortical receptive field profiles. Vision Res. 1980;20(10):847–856. doi: 10.1016/0042-6989(80)90065-6. [DOI] [PubMed] [Google Scholar]
  14. Dean A. F. The relationship between response amplitude and contrast for cat striate cortical neurones. J Physiol. 1981 Sep;318:413–427. doi: 10.1113/jphysiol.1981.sp013875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dinse H. R., von Seelen W. On the function of cell systems in area 18. Part II. Biol Cybern. 1981;41(1):59–69. doi: 10.1007/BF01836127. [DOI] [PubMed] [Google Scholar]
  16. HUBEL D. H., WIESEL T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol. 1962 Jan;160:106–154. doi: 10.1113/jphysiol.1962.sp006837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kulikowski J. J., Tolhurst D. J. Psychophysical evidence for sustained and transient detectors in human vision. J Physiol. 1973 Jul;232(1):149–162. doi: 10.1113/jphysiol.1973.sp010261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Maffei L., Fiorentini A., Bisti S. Neural correlate of perceptual adaptation to gratings. Science. 1973 Dec 7;182(4116):1036–1038. doi: 10.1126/science.182.4116.1036. [DOI] [PubMed] [Google Scholar]
  19. Maffei L., Fiorentini A. The visual cortex as a spatial frequency analyser. Vision Res. 1973 Jul;13(7):1255–1267. doi: 10.1016/0042-6989(73)90201-0. [DOI] [PubMed] [Google Scholar]
  20. Morrone M. C., Burr D. C. Evidence for the existence and development of visual inhibition in humans. Nature. 1986 May 15;321(6067):235–237. doi: 10.1038/321235a0. [DOI] [PubMed] [Google Scholar]
  21. Morrone M. C., Burr D. C., Maffei L. Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence. Proc R Soc Lond B Biol Sci. 1982 Oct 22;216(1204):335–354. doi: 10.1098/rspb.1982.0078. [DOI] [PubMed] [Google Scholar]
  22. Movshon J. A., Lennie P. Pattern-selective adaptation in visual cortical neurones. Nature. 1979 Apr 26;278(5707):850–852. doi: 10.1038/278850a0. [DOI] [PubMed] [Google Scholar]
  23. Murray I. J., Kulikowski J. J. VEPs and contrast. Vision Res. 1983;23(12):1741–1743. doi: 10.1016/0042-6989(83)90193-1. [DOI] [PubMed] [Google Scholar]
  24. Nakayama K., Mackeben M. Steady state visual evoked potentials in the alert primate. Vision Res. 1982;22(10):1261–1271. doi: 10.1016/0042-6989(82)90138-9. [DOI] [PubMed] [Google Scholar]
  25. Ramoa A. S., Shadlen M., Skottun B. C., Freeman R. D. A comparison of inhibition in orientation and spatial frequency selectivity of cat visual cortex. Nature. 1986 May 15;321(6067):237–239. doi: 10.1038/321237a0. [DOI] [PubMed] [Google Scholar]
  26. Ratliff F., Zemon V. Some new methods for the analysis of lateral interactions that influence the visual evoked potential. Ann N Y Acad Sci. 1982;388:113–124. doi: 10.1111/j.1749-6632.1982.tb50787.x. [DOI] [PubMed] [Google Scholar]
  27. Regan D. Spatial frequency mechanisms in human vision investigated by evoked potential recording. Vision Res. 1983;23(12):1401–1407. doi: 10.1016/0042-6989(83)90151-7. [DOI] [PubMed] [Google Scholar]
  28. Shapley R. M., Victor J. D. How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. J Physiol. 1981 Sep;318:161–179. doi: 10.1113/jphysiol.1981.sp013856. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shapley R. M., Victor J. D. The effect of contrast on the non-linear response of the Y cell. J Physiol. 1980 May;302:535–547. doi: 10.1113/jphysiol.1980.sp013259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sillito A. M. Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. J Physiol. 1979 Apr;289:33–53. doi: 10.1113/jphysiol.1979.sp012723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sillito A. M., Kemp J. A., Milson J. A., Berardi N. A re-evaluation of the mechanisms underlying simple cell orientation selectivity. Brain Res. 1980 Aug 4;194(2):517–520. doi: 10.1016/0006-8993(80)91234-2. [DOI] [PubMed] [Google Scholar]
  32. Spekreijse H., Oosting H. Linearizing: a method for analysing and synthesizing nonlinear systems. Kybernetik. 1970 Apr;7(1):22–31. doi: 10.1007/BF00270331. [DOI] [PubMed] [Google Scholar]
  33. Tolhurst D. J. Separate channels for the analysis of the shape and the movement of moving visual stimulus. J Physiol. 1973 Jun;231(3):385–402. doi: 10.1113/jphysiol.1973.sp010239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tyler C. W., Apkarian P. A. Effects of contrast, orientation and binocularity in the pattern evoked potential. Vision Res. 1985;25(6):755–766. doi: 10.1016/0042-6989(85)90183-x. [DOI] [PubMed] [Google Scholar]
  35. Vidyasagar T. R., Heide W. The role of GABAergic inhibition in the response properties of neurones in cat visual area 18. Neuroscience. 1986;17(1):49–55. doi: 10.1016/0306-4522(86)90224-1. [DOI] [PubMed] [Google Scholar]
  36. Zemon V., Ratliff F. Intermodulation components of the visual evoked potential: responses to lateral and superimposed stimuli. Biol Cybern. 1984;50(6):401–408. doi: 10.1007/BF00335197. [DOI] [PubMed] [Google Scholar]

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

RESOURCES