Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-23T15:35:00.361Z Has data issue: false hasContentIssue false
  • English
  • Français

Visual effects of damage to P ganglion cells in macaques

Published online by Cambridge University Press:  02 June 2009

James J. Lynch ,
Luiz C. L. Silveira ,
V. Hugh Perry  and
William H. Merigan
James J. Lynch
Affiliation:
Department of Biophysics, University of Rochester Medical Center, Rochester
Luiz C. L. Silveira
Affiliation:
Departmento de Fisiologia, Centro de Ciencias Biologicas, Universidade Federal do Para, 66059 Belem, Para, Brasil
V. Hugh Perry
Affiliation:
Department of Experimental Psychology, University of Oxford, Oxford, U.K.
William H. Merigan
Affiliation:
Department of Ophthalmology and Center for Visual Science, University of Rochester Medical Center, Rochester
Get access Rights & Permissions [Opens in a new window]

Abstract

Four indices of visual performance were measured in control macaques and in macaques that had been exposed to monomeric acrylamide, a neurotoxicant that preferentially damages P retinal ganglion cells. Morphological examination of the retina and visual pathways of these monkeys showed virtually complete loss of P ganglion cells over a region extending to at least 40 deg from the fovea, and relative sparing of M ganglion cells. The four tests examined visual functions for which the visual pathway from P ganglion cells might be of great importance: visual acuity, contrast discrimination, hyperacuity, and shape discrimination.

In the acrylamide-dosed monkeys, visual acuity was reduced slightly more than fourfold, a somewhat larger reduction than that seen previously after ibotenic-acid lesions of the P pathway in the geniculate. The residual acuity was in good agreement with the Nyquist frequency calculated from the density of ON or OFF M ganglion cells. Contrast increment thresholds were elevated for the dosed monkeys only in one of the two conditions tested. The elevation was found only under those spatiotemporal conditions for which we have previously shown that contrast thresholds are increased by acrylamide exposure, and was most marked at low background contrasts. Vernier acuity was elevated in one dosed monkey, but not affected in a second monkey that also had severe loss of P ganglion cells. Finally, we found no effect of acrylamide exposure on the number of training trials required to learn simple or complex shape discriminations. These results support previous findings in showing that the P pathway mediates visual acuity, and they show that several other important aspects of visual perception are not exclusively dependent on the P pathway.

Keywords

Parallel pathwaysSampling densityMacaque monkey acuityShape discrimination
Type
Research Articles
Information
Visual Neuroscience , Volume 8 , Issue 6 , June 1992 , pp. 575 - 583
Copyright
Copyright © Cambridge University Press 1992

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

Banks, M.S., Geisler, W.S. & Bennett, P.J. (1987). The physical limits of grating visibility. Vision Research 11, 1915–1924.CrossRefGoogle Scholar
Crook, J.M., Lange-Malecki, B., Lee, B.B. & Valberg, A. (1988). Visual resolution of macaque retinal ganglion cells. Journal of Physiology 396, 205–224.Google Scholar
Demonasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. Journal of Physiology 251, 167–195.CrossRefGoogle Scholar
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurons in lateral geniculate nucleus of macaque. Journal of Physiology 357, 219–240.Google Scholar
Deyoe, E.A. & Vanessen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11, 219–226.CrossRefGoogle ScholarPubMed
Ferrera, V.P., Nealey, T.A. & Maunsell, J.H.R. (1991). Magnocellular and parvocellular inputs to macaque area V4. Investigative Ophthalmology and Visual Science (Suppl.) 32, 1117.Google Scholar
Gross, C.G. (1972). Visual functions of inferotemporal cortex. Handbook of Sensory Physiology, 7/3b, Central Visual Information, pp 451–481. Berlin: Springer.Google Scholar
Heywood, C.A. & Cowey, A. (1987). On the role of cortical area V4 in the discrimination of hue and pattern in macaque monkeys. Journal of Neuroscience 7, 2601–2617.CrossRefGoogle ScholarPubMed
Judge, S.J., Richmond, B.J. & Chu, F.C. (1980). Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Research 20, 535–538.Google Scholar
Krauskopf, J. & Farell, B. (1991). Vernier acuity: effects of chromatic content, blur and contrast. Vision Research 31, 735–749.Google Scholar
Leooe, G.E. & Kersten, D. (1987). Contrast discrimination in peripheral vision. Journal of the Optical Society of America 4, 1594–1598.Google Scholar
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in the Old World monkey: morphology and central projections. Science 213, 1139–1142.Google Scholar
Levi, D.M., Klein, S.A. & Aitsebaomo, A.P. (1985). Vernier acuity, crowding and cortical magnification. Vision Research 25, 963–977.CrossRefGoogle ScholarPubMed
Lynch, J.J. III, Silveira, L.C.L., Perry, V.H. & Merigan, W.H. (in preparation). Mechanisms of differential ganglion cell vulnerability in the primate retina.Google Scholar
Maunsell, J.H.R. & Newsome, W.T. (1987). Visual processing in monkey extrastriate cortex. Annual Review of Neuroscience 10, 363–401.CrossRefGoogle ScholarPubMed
Merigan, W.H. (1989). Chromatic and achromatic vision of macaques: Role of the P pathway. Journal of Neuroscience 9, 776–783.CrossRefGoogle ScholarPubMed
Merigan, W.H. (1991). P and M pathway specialization in the macaque. In From Pigments to Perception: Advances in Understanding Visual Processes, ed Valberg, A. & Lee, B.B., pp. 117–126. New York: Plenum.CrossRefGoogle Scholar
Merigan, W.H., Byrne, C.E. & Maunsell, J. (1989). Role of the magnocellular pathway in primate vision. Society for Neuroscience Abstracts 250, 1256.Google Scholar
Merigan, W.H., Byrne, C. & Maunsell, J.H.R. (1991a). Does primate motion perception depend on the magnocellular pathway? Journal of Neuroscience 11, 3422–3429.CrossRefGoogle ScholarPubMed
Merigan, W.H. & Eskin, T.A. (1986). Spatio-temporal vision of macaques with severe loss of Pb retinal ganglion cells. Vision Research 26, 1751–1761.CrossRefGoogle Scholar
Merigan, W.H. & Katz, L.M. (1990). Spatial resolution across the macaque retina. Vision Research 30, 985–991.CrossRefGoogle ScholarPubMed
Merigan, W.H., Katz, L.M. & Maunsell, J.H.R. (1991b). The effects of parvocellular lateral geniculate lesions on the acuity and contrast sensitivity of macaque monkeys. Journal of Neuroscience 11, 994–1001.CrossRefGoogle ScholarPubMed
Merigan, W.H. & Maunsell, J.H.R. (1990). Macaque vision after magnocellular lateral geniculate lesions. Visual Neuroscience 5, 347–352.CrossRefGoogle ScholarPubMed
Morgan, M.J. & Aiba, T.S. (1985). Positional acuity with chromatic stimuli. Vision Research 25, 689–695.CrossRefGoogle ScholarPubMed
Parker, A. & Hawken, M. (1985). Capabilities of monkey cortical cells in spatial-resolution tasks. Journal of the Optical Society of America 2, 1101–1114.Google Scholar
Perry, V.H. & Cowey, A. (1984). Retinal Ganglion Cells That Project To The Superior Colliculus And Pretectum In The Macaque Monkey. Neuroscience 12, 1125–1137.CrossRefGoogle Scholar
Perry, V.H. & Cowey, A. (1985). The ganglion cell and cone distributions in the monkey's retina: Implications for central magnification factors. Vision Research 25, 1795–1810.Google Scholar
Perry, V.H., Oehler, R. & Cowey, A. (1984). Retinal ganglion cells which project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 1101–1123.Google Scholar
Purpura, K., Kaplan, E. & Shapley, R. (1988). Background light and the contrast gain of primate P and M retinal ganglion cells. Proceedings of the National Academy of Sciences of the U.S.A. 85, 4534–4537.Google Scholar
Schein, S.J. & Demonasterio, F.M. (1987). Mapping of retinal and geniculate neurons onto striate cortex macaque. Journal of Neuroscience 7, 996–1009.Google Scholar
Schiller, P.H., Logothetis, N.K. & Charles, E.R. (1990a). Functions of the colour-opponent and broad-band channels of the visual system. Nature 343, 68–70.CrossRefGoogle ScholarPubMed
Schiller, P.H., Logothetis, N.K. & Charles, E.R. (1990b). Role of the color-opponent and broadband channels in vision. Visual Neuroscience 5, 321–346.Google Scholar
Sclar, G., Maunsell, J.H.R. & Lennie, P. (1990). Coding of image contrast in central visual pathways of the macaque monkey. Vision Research 30, 1–10.Google Scholar
Shapley, R., Kaplan, E. & Soodak, R. (1981). Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque. Nature 292, 543–545.Google Scholar
Shapley, R. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neuroscience 9, 229–235.Google Scholar
Silveira, L.C.L. & Perry, V.H. (1990). A neurofibrillar staining method for retina and skin: a simple modification for improved staining and reliability. Journal of Neuroscience Methods 33, 11–21.CrossRefGoogle ScholarPubMed
Silveira, L.C.L. & Perry, V.H. (1991). The topography of magnocellular projecting ganglion cells (M ganglion cells) in the primate retina. Neuroscience 40, 217–237.Google Scholar
Toet, A. & Koenderink, J.J. (1988). Differential spatial displacement discrimination thresholds for gabor patches. Vision Research 28, 133–143.Google Scholar
WÄSsle, H., Grunert, U., Rohrenbeck, J. & Boycott, B. (1989). Cortical magnification factor and the ganglion cell density of the primate retina. Nature 341, 643–646.Google Scholar
Wehrhahn, C. & Westheimer, G. (1990). How vernier acuity depends on contrast. Experimental Brain Research 80, 618–620.CrossRefGoogle ScholarPubMed
Westheimer, G. (1982). The spatial grain of the perifoveal visual field. Vision Research 22, 157–162.Google Scholar
Williams, D.R. (1985). Aliasing in human foveal vision. Vision Research 25, 195–205.Google Scholar
Williams, D.R. (1990). The invisible cone mosaic. In Advances in Photoreceplion, ed C.V.N.R., Council, pp. 135–148. Washington: National Academy Press.Google Scholar
Williams, R.A., Enoch, J.M. & Essock, E.A. (1984). The resistance of selected hyperacuity configurations to retinal image degradation. Investigative Ophthalmology and Visual Science 25, 389–399.Google Scholar
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome-oxidase histochemistry. Brain Research 171, 11–28.Google Scholar