Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-17T06:03:30.130Z Has data issue: false hasContentIssue false

Pattern-reversal electroretinogram in response to chromatic stimuli: II Monkey

Published online by Cambridge University Press:  02 June 2009

Concetta Morrone
Affiliation:
Istituto di Neurofisiologia del CNR, via S. Zeno 51, Pisa, Italy
Adriana Fiorentini
Affiliation:
Istituto di Neurofisiologia del CNR, via S. Zeno 51, Pisa, Italy
Silvia Bisti
Affiliation:
Istituto di Neurofisiologia del CNR, via S. Zeno 51, Pisa, Italy
Vittorio Porciatti
Affiliation:
Istituto di Neurofisiologia del CNR, via S. Zeno 51, Pisa, Italy
David C. Burr
Affiliation:
Istituto di Neurofisiologia del CNR, via S. Zeno 51, Pisa, Italy

Abstract

We have recorded steady-state PERGs from five macaque monkeys in response to red-green plaid patterns reversed sinusoidally in contrast. The patterns had either a pure luminance contrast (red-black, green-black, yellow-black), pure red-green color contrast, or a variable amount of luminance and color contrast. By varying the relative luminance of the red-to-total luminance (color ratio) of red-green patterns, a value could be obtained at which the PERG amplitude was either minimum or locally maximum, and the phase was most lagged. This value was very similar to that producing equiluminance in human observers, and was considered to be equiluminance for the monkey. The phase of the PERG to chromatic stimulus was systematically lagged compared with that to luminance stimuli, by an amount corresponding to about 10–20 ms under our experimental conditions. The variation of phase with temporal frequency suggested an apparent latency of about 80 ms for color contrast compared with 63 ms for luminance. These estimates were confirmed with separate measurements of transient PERGs to abrupt contrast reversal. As a function of temporal frequency, the chromatic PERG function was clearly low-pass with a cutoff around 15 Hz, whereas that to luminance was double-peaked and extended to higher temporal frequencies, around 30 Hz. For both luminance and chromatic stimuli, the amplitude of PERGs increases with increasing stimulus contrast. By summing vectorially the luminance and chromatic responses of appropriate contrasts, we were able to predict with accuracy the response as a function of color ratio. In two monkeys, the optic chiasm was sectioned sagittally causing total degeneration of ganglion cells in the nasal retina, without affecting the temporal retina (verified by histology). In these animals, there was a strong response to both luminance and chromatic patterns in the temporal retinae, but none to either type of pattern in the nasal retinae, suggesting that the PERG to both luminance and chromatic stimuli arises from the inner-retinal layers. Electrophysiological studies suggest that the PERG to chromatic stimuli is probably associated with the activity of P-cells. P-cells may also make a major contribution to the PERG of luminance stimuli, although M-cells may also participate. The above findings on normal monkeys all agree with those reported in the accompanying paper for humans (Morrone et al., 1994), so similar conclusions can probably be extended to human PERG.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Benardete, E.A. & Kaplan, E. (1993). Spatiotemporal dynamics of P-cells and their cone inputs. Society for Neuroscience Abstracts 19, 15.Google Scholar
Benardete, E.A., Kaplan, E. & Knight, B.W. (1992). Contrast gain control in the primate retina: P cells are not X-like, some M cells are. Visual Neuroscience 8, 483486.CrossRefGoogle ScholarPubMed
Dacey, D.M. & Lee, B.B. (1994). The ‘blue-on’ opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731735.CrossRefGoogle ScholarPubMed
Dacey, D.M. (1993 a). Morphology of a small-field bistratified ganglion cell type in the macaque and human retina. Visual Neuroscience 10, 10811098.CrossRefGoogle ScholarPubMed
Dacey, D.M. (1993 b). The mosaic of midget ganglion cells in the human retina. Journal of Neuroscience 13, 53345355.CrossRefGoogle ScholarPubMed
De Monasterio, F.M. (1978). Properties of concentrically organized X and Y ganglion cells of Macaque retina. Journal of Neurophysiology 41, 13941417.CrossRefGoogle ScholarPubMed
Estevez, O. & Spekreuse, H. (1982). The “silent substitution” method in visual research. Vision Research 22, 681691.CrossRefGoogle Scholar
Gouras, P. (1968). Identification of cone mechanisms in monkey ganglion cells. Journal of Physiology 199, 533547.CrossRefGoogle ScholarPubMed
Hess, R.F., Baker, C.L., Zrenner, E. & Schwarzer, J. (1986). Differences between electroretinograms of cat and primate. Journal of Neurophysiology 56, 747768.CrossRefGoogle Scholar
Holländer, H., Bisti, S., Maffel, L. & Hebel, R. (1984). Electroret-inographic responses and retrograde changes of retinal morphology after intracranial optic nerve section: A quantitative analysis in the cat. Experimental Brain Research 55, 483493.CrossRefGoogle ScholarPubMed
Kaplan, E., Lee, B.B. & Shapley, R.M. (1990). New views of primate retinal function In Progress in Retinal Research, ed. Osborn, N. & Chader, G., pp. 273336. Oxford: Pergamon Press.Google Scholar
Kaplan, E. & Shapley, R.M. (1982). X and Y cells in the lateral genic-ulate nucleus of macaque monkeys. Journal of Physiology (London) 330, 125143.CrossRefGoogle ScholarPubMed
Kaplan, E. & Shapley, R.M. (1986). The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proceedings of the National Academy of Sciences of the U.S.A. 83, 27552757.CrossRefGoogle ScholarPubMed
Kremers, J., Lee, B.B., Pokorny, J. & Smith, V.S. (1993). Responses of ganglion cells and human observers to compound periodic waveforms. Vision Research 33, 19972011.CrossRefGoogle ScholarPubMed
Lee, B.B., Martin, P.R. & Valberg, A. (1989). Nonlinear summation of M- and L-cone inputs to phasic retinal ganglion cells of the macaque. Journal of Neuroscience 9, 14331442.CrossRefGoogle ScholarPubMed
Lee, B.B., Pokorny, J., Smith, V.C., Martin, P.R. & Valberg, A. (1990). Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers Journal of the Optical Society of America A 7, 22232236.Google ScholarPubMed
Maffel, L. & Fiorentini, A. (1981). Electroretinographic responses to alternating gratings before and after section of the optic nerve. Science 211, 953955.Google Scholar
Maffel, L. & Fiorentini, A. (1982). Electroretinographic response to alternating gratings in the cat. Experimental Brain Research 48, 327334.Google Scholar
Maffel, L., Fiorentini, A., Bisti, S. & Holländer, H. (1985). Pattern ERG in the monkey after section of the optic nerve. Experimental Brain Research 59, 423425.Google Scholar
Martin, P.R. & Gruenert, U. (1992). Spatial density and immuno-reactivity of bipolar cells in the Macaque Monkey. Journal of Comparative Neurology 323, 269287.CrossRefGoogle Scholar
Mills, S.L. & Sperling, H.G. (1990). Red/green opponency in the rhesus macaque ERG spectral sensitivity is reduced by bicuculline. Visual Neuroscience 5, 217221.CrossRefGoogle ScholarPubMed
Morrone, M.C., Porciatti, V., Fiorentini, A., Burr, D.C. & Bisti, S. (1993). PERG response to chromatic patterns in normal and ganglion-cell-depleted monkey retina. Investigative Ophthalmology and Visual Science 34, 1274.Google Scholar
Morrone, M.C., Porciatti, V., Burr, D.C. & Fiorentini, A. (1994). Pattern-reversal electroretinogram in response to chromatic stimuli: I Humans. Visual Neuroscience 11, 861871.CrossRefGoogle ScholarPubMed
Perry, V.H. & Cowey, A. (1984). Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience 12, 11251137.CrossRefGoogle Scholar
Perry, V.H., Oehler, R. & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 11011123.CrossRefGoogle Scholar
Purpura, K., Kaplan, E. & Shapley, R.M. (1988). Background light and the contrast gain control of primate P and M retinal ganglion cells. Proceedings of the National Academy of Sciences of the U.S.A. 85, 45344537.CrossRefGoogle Scholar
Rodieck, R.W., Binmoeller, K.F. & Dineen, J. (1985). Parasol and midget ganglion cells of the human retina. Journal of Comparative Neurology 233, 115132.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Watanabe, M. (1988). Morphology of ganglion cell types thai project to the parvocellular laminae of the lateral geniculate nucleus, pretectum and superior colliculus of primates. Society for Neuroscience Abstracts 14, 1120.Google Scholar
Sperling, H.J. & Mills, S.L. (1991). Red-green interactions in the spectral sensitivity of primates as derived from ERG and behavioral data. Visual Neuroscience 7, 7586.CrossRefGoogle ScholarPubMed