Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-23T04:33:25.988Z Has data issue: false hasContentIssue false

Center/surround relationships of magnocellular, parvocellular, and koniocellular relay cells in primate lateral geniculate nucleus

Published online by Cambridge University Press:  02 June 2009

Gregg E. Irvin
Affiliation:
Department of Physiological Optics, School of Optometry/The Medical Center, The University of Alabama at Birmingham
Vivien A. Casagrande
Affiliation:
Departments of Cell Biology and Psychology, Vanderbilt University, Nashville
Thomas T. Norton
Affiliation:
Department of Physiological Optics, School of Optometry/The Medical Center, The University of Alabama at Birmingham

Abstract

As in other primates, the lateral geniculate nucleus (LGN) of the prosimian primate, bush baby (Galago crassicaudatus), contains three morphologically and physiologically distinct cell classes [magnocellular (M), parvocellular (P), and koniocellular (K)] (Norton & Casagrande, 1982; Casagrande & Norton, 1991). The present study examined quantitatively the center/surround relationships of cells in all three classes. Estimates of receptive-field center size (Rc) and sensitivity (Kc) and of surround size (Rs) and sensitivity (Ks) were obtained from 47 LGN relay cells by fitting a difference of Gaussians function to contrast-sensitivity data. For M and P cells, center size (Rc) increases with eccentricity but is about two times larger for M than for P cells at a given eccentricity. Surround size (Rs) increases with eccentricity for P but not for M or K cells. The center sensitivity (Kc) is inversely related to center size (Rc) and surround sensitivity (Ks) is inversely related to surround size (Rs) for cells in all classes, a result consistent with the sensitivity regulation that is produced by light adaptation. High spatial-frequency cutoff (acuity) is inversely related to center size (Rc). However, the peak contrast sensitivity is relatively independent of Rc. The ratio of the integrated strength (volume) of the surround to the volume of the center remains relatively constant (median, 0.87) across all three cell classes. This ratio is an excellent predictor of a cell’s rolloff in contrast sensitivity at low spatial frequencies: cells with a low surround/center ratio have less low-frequency rolloff. Although M, P, and K cells generally display similar center/surround relationships, differences in center size and the other parameters between the classes distinguish most M, P, and K cells. These findings demonstrate that both similarities and differences in the visual-response properties of primate LGN cells in these three parallel afferent pathways can be explained by basic center/surround relationships.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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

Barlow, H.B. (1953). Summation and inhibition in the frog’s retina. Journal of Physiology (London) 119, 6988CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1976). Threshold setting by the surround of cat retinal ganglion cells. Journal of Physiology (London) 259, 737757CrossRefGoogle ScholarPubMed
Barlow, H.B., Fitzhugh, R. & Kuffler, S.W. (1957). Change of organization in the receptive fields of the cat’s retina during dark adaptation. Journal of Physiology (London) 137, 338354CrossRefGoogle ScholarPubMed
Casagrande, V.A. & Debruyn, E.J. (1982). The Galago visual system: Aspects of normal organization and developmental plasticity. In The Lesser Bushbaby (Galago) An Animal Model: Selected Topics, ed. Haines, D.E., pp. 138168. Boca Raton, Florida: C.R.C. Press.Google Scholar
Casagrande, V.A. & Norton, T.T. (1991). Lateral geniculate nucleus: A review of its physiology and function. In The Neural Basis of Visual Function: Vision and Visual Dysfunction, ed. Leventhal, A., pp. 4184. London: McMillian Press, Ltd.Google Scholar
Cleland, B.G. & Levick, W.R. (1974). Brisk and sluggish concentrically organized ganglion cells in the cat’s retina. Journal of Physiology (London) 240, 421456CrossRefGoogle ScholarPubMed
Cleland, B.G., Levick, W.R. & Sanderson, K.J. (1973). Properties of sustained and transient ganglion cells in the cat retina. Journal of Physiology (London) 228, 649680CrossRefGoogle ScholarPubMed
Cleland, B.G., Harding, T.H. & Tulunay-Keesey, U. (1979). Visual resolution and receptive field size: Examination of two kinds of cat retinal ganglion cell. Science 205, 10151017CrossRefGoogle ScholarPubMed
Dawis, S., Shapley, E.K., Kaplan, E. & Tranchina, D. (1984). The receptive field organization of X-cells in the cat: Spatiotemporal coupling and asymmetry. Vision Research 24, 549564CrossRefGoogle ScholarPubMed
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivity of neurones in lateral geniculate nucleus of macaque. Journal of Physiology (London) 357, 219240CrossRefGoogle ScholarPubMed
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. Journal of Physiology (London) 357, 241265CrossRefGoogle ScholarPubMed
Diamond, I.T., Conley, M., Itoh, K. & Fitzpatrick, D. (1985). Laminar organization of geniculocortical projections in Galago senegalen-sis and Aotus trivirgatus. Journal of Comparative Neurology 242, 584610CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Freeman, A.W. (1987). The receptive-field spatial structure of cat retinal Y cells. Journal of Physiology (London) 384, 4979CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Lennie, P. (1975). The control of retinal ganglion cell discharge by receptive field surrounds. Journal of Physiology (London) 247, 551578CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Pinto, L. (1972). Properties of the surround response mechanism of cat retinal ganglion cells and center surround interaction. Journal of Physiology (London) 220, 403439CrossRefGoogle Scholar
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology (London) 187, 517552CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Shapley, R.M. (1973). Flux, not retinal illumination, is what cat retinal ganglion cells really care about. Journal of Physiology (London) 233, 311326CrossRefGoogle Scholar
Fisher, B. & May, H.U. (1970). Invarianzen in der Katzenretina: Gesetz-massige Beziehungen zwischen Empfindlichkeit, Grosse und Lage receptiver Felder von Ganlienzellen. Experimental Brain Research 11, 448464Google Scholar
Harding, T.H. & Enroth-Cugell, C. (1978). Absolute dark sensitivity and center size in cat retinal ganglion cells. Brain Research 153, 157162CrossRefGoogle ScholarPubMed
Irvin, G.E., Norton, T.T. & Casagrande, V.A. (1986 a). Receptive-field properties derived from spatial contrast sensitivity measurements of primate LGN cells. Investigative Ophthalmology and Visual Science (Suppl.) 27, 16.Google Scholar
Irvin, G.E., Norton, T.T., Sesma, M.A. & Casagrande, V.A. (1986 b). W-like response properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Research 363, 254274CrossRefGoogle Scholar
Kaas, J.H. (1986). The structural basis for information processing in the primate visual system. In Visual Neurosciences, ed. Pettigrew, J.D., Levick, W.R. & Sanderson, K.J., pp. 315342, Cambridge: Cambridge University Press.Google Scholar
Kaplan, E. & Shapley, R.M. (1982). X- and Y-cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology (London) 330, 125143CrossRefGoogle ScholarPubMed
Kaplan, E., Purpura, K. & Shapley, R.M. (1987). Contrast effects the transmission of visual information through the mammalian lateral geniculate nucleus. Journal of Physiology (London) 391, 267288CrossRefGoogle ScholarPubMed
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 3768CrossRefGoogle ScholarPubMed
Lachica, E.A. & Casagrande, V.A. (1992). Direct W-like geniculate projections to the cytochrome oxidase (CO) blobs in primate visual cortex: Axon morphology. Journal of Comparative Neurology 319, 141159CrossRefGoogle Scholar
Lachica, E.A., Beck, P.D. & Casagrande, V.A. (1992). Parallel pathways in macaque monkey striate cortex: Anatomically defined columns in layer III. Proceedings of the National Academy of Sciences of the U.S.A. 89, 35663570CrossRefGoogle ScholarPubMed
Lachica, E.A., Beck, P.D. & Casagrande, V.A. (1993). Intrinsic connections of layer III of striate cortex in squirrel monkey and bush baby: Correlations with patterns of cytochrome oxidase. Journal of Comparative Neurology (in press).CrossRefGoogle ScholarPubMed
Linsenmeier, R.A., Frishman, L.J., Jaktela, H.G. & Enroth-Cugell, C. (1982). Receptive field properties of X and Y cells in the cat retina derived from contrast sensitivity measurements. Vision Research 22, 11731183CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1982). Thalmic inputs to the cytochrome oxidase-rich regions in monkey visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 79, 60986101CrossRefGoogle Scholar
Livingstone, M. & Hubel, D. (1988). Segregation of form, color, move-ment, and depth: Anatomy, physiology, and perception. Science 240, 740749CrossRefGoogle Scholar
Merigan, W.H. (1989). Chromatic and achromatic vision of macaques: Role of the P pathway. Journal of Neuroscience 9, 776783CrossRefGoogle ScholarPubMed
Movshon, J.A., Eggers, H.M., Gizzi, M.S., Hendrickson, A.E., Ki-Orpes, L. & Boothe, R.G. (1987). Effects of early unilateral blur on the macaque’s visual system. III. Physiological Observations. Journal of Neuroscience 7, 13401351CrossRefGoogle ScholarPubMed
Norton, T.T. & Casagrande, V.A. (1982). Laminar organization of receptive-field properties in lateral geniculate nucleus of bush baby (Galago crassicaudatus). Journal of Neurophysiology 47, 715741CrossRefGoogle ScholarPubMed
Norton, T.T. & Godwin, D.W. (1992). Inhibitory GABAergic control of visual signals at the lateral geniculate nucleus. In GABA in the Retina and Central Visual System, ed. MIZE, R.R., MARC, R.E. & Sillito, A.M., pp. 193217. Amsterdam: Elsevier.CrossRefGoogle Scholar
Norton, T.T., Casagrande, V.A., Irvin, G.E., Sesma, M.A. & Petry, H.M. (1988). Contrast-sensitivity functions of W-, X-, and Y-like relay cells in the lateral geniculate nucleus of bush baby, Galago crassicaudatus. Journal of Neurophysiology 59, 16391656CrossRefGoogle Scholar
Norton, T.T., Holdefer, R.N. & Godwin, D.W. (1989). Effects of bicuculline on receptive-field center sensitivity of relay cells in the lateral geniculate nucleus. Brain Research 488, 352358CrossRefGoogle ScholarPubMed
Peichl, L. & Wassle, H. (1979). Size, scatter, and coverage of ganglion cell receptive field centers in the cat retina. Journal of Physiology (London) 291, 117141CrossRefGoogle ScholarPubMed
Pettigrew, J.D., Cooper, M.L. & Blasdel, G.G. (1979). Improved use of tapetal reflection for eye-position monitoring. Investigative Ophthalmology and Visual Science 18, 490495Google ScholarPubMed
Rodieck, R.W. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research 5, 583601CrossRefGoogle ScholarPubMed
Schiller, P.H., Logothetis, N.K. & Charles, E.R. (1991). Parallel pathways in the visual system: Their role in perception at iso-luminance. Neuropsychologia 29, 433441CrossRefGoogle Scholar
Shapley, R. (1982). Parallel pathways in the mammalian visual system. Annals of the New York Academy of Sciences 388, 1120CrossRefGoogle ScholarPubMed
Shapley, R.M., Kaplan, E. & Soodak, R. (1981). Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque monkey. Nature 292, 543545CrossRefGoogle Scholar
So, Y.T. & Shapley, R. (1981). Spatial tuning of cells in and around lateral geniculate nucleus of the cat: X and Y relay cells and perige-niculate interneurons. Journal of Neurophysiology 45, 107120CrossRefGoogle Scholar
Soodak, R.E. (1986). Two dimensional modeling of visual receptive fields using gaussian subunits. Proceedings of the National Academy of Sciences of the U.S.A. 83, 92599263CrossRefGoogle ScholarPubMed
Stone, J. & Fukuda, Y. (1974). Properties of cat retinal ganglion cells: A comparison of W-cells with X- and Y-cells. Journal of Neurophysiology 37, 722748CrossRefGoogle ScholarPubMed
Wiesel, T.N. (1960). Receptive fields of ganglion cells in the cat’s retina. Journal of Physiology (London) 153, 583594CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiology 29, 11151156CrossRefGoogle ScholarPubMed
Wolin, L.R. & Massopust, L.C. (1970). Morphology of the primate retina. In The Primate Brain, ed. Noback, C.R. & Montagna, W., pp. 127. New York: Appleton-Century-Crofts.Google Scholar