Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-23T00:21:51.313Z Has data issue: false hasContentIssue false
  • English
  • Français

Prenatal disruption of binocular interactions creates novel lamination in the cat's lateral geniculate nucleus

Published online by Cambridge University Press:  02 June 2009

Preston E. Garraghty ,
Carla J. Shatz  and
Mriganka Sur
Preston E. Garraghty
Affiliation:
1Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge
Carla J. Shatz
Affiliation:
2 Department of Neurobiology, Stanford University School of Medicine, Stanford
Mriganka Sur
Affiliation:
1Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge
Get access Rights & Permissions [Opens in a new window]

Abstract

The elimination of retinogeniculate afferents from one eye on embryonic day 44 (E44) has pronounced effects on the formation of the cellular laminae in the cat lateral geniculate nucleus (LGN). Only two laminae form: a dorsal, “magnocellular” layer, and a ventral, “parvocellular” layer. Soma size measurements and previously reported patterns of termination of retinogeniculate axons suggest that the dorsal lamina is a coalescence of the normal A-laminae and the dorsal, magnocellular division of layer C, while the ventral layer is a composite of the parvocellular sublamina of layer C and the remaining C-laminae. This is a novel pattern of lamination in the LGN that differs from that found in the normal nucleus, not only in that there are now only two cell layers rather than the normal five, but also in that the interlaminar zone occurs in an abnormal location. This result is markedly different from that observed in other species where interlaminar zones present after early monocular enucleation are a subset of the ones which would normally be present. We suggest that, in the absence of ongoing binocular interactions, interactions between functionally distinct retinal ganglion cell classes from the remaining eye may direct the formation of cell laminae in the LGN, even when such interactions are not normally operative.

Keywords

CatLateral geniculate nucleusVisual developmentLaminationBinocular interactions
Type
Research Articles
Information
Visual Neuroscience , Volume 1 , Issue 1 , January 1988 , pp. 93 - 102
Copyright
Copyright © Cambridge University Press 1988

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

Boss, V.C. & Schmidt, J.T. (1984). Activity and the formation of ocular dominance patches in dually innervated tectum of goldfish. Journal of Neuroscience 4, 2891–2905.CrossRefGoogle ScholarPubMed
Bowling, D.B. & Michael, C.R. (1980). Projections of single physiologically characterized optic tract fibres in cat. Nature 286, 899–902.CrossRefGoogle ScholarPubMed
Bowling, D.B. & Michael, C.R. (1984). Terminal patterns of single, physiologically characterized optic tract fibers in the cat's lateral geniculate nucleus. Journal of Neuroscience 4, 198–216.CrossRefGoogle ScholarPubMed
Casagrande, V.A. & Brunso-Bechtold, J.K. (1985). Development of lamination in the lateral geniculate nucleus: critical factors. In Advances in Neural and Behavioral Development, Vol. 1, ed. Aslin, R., pp. 33–78. New York: Ablex.Google Scholar
Casagrande, V.A. & Condo, G.J. (1987). Is binocular competition essential for layer formation in the lateral geniculate nucleus. Brain, Behavior and Evolution (in press).Google Scholar
Casagrande, V.A. & Joseph, R. (1980). Morphological effects of monocular deprivation and recovery on the dorsal lateral geniculate nucleus in galago. Journal of Comparative Neurology 194, 413–426.CrossRefGoogle ScholarPubMed
Chalupa, L.M. & Williams, R.W. (1984). Organization of the cat's lateral geniculate nucleus following interruption of prenatal binocular competition. Human Neurobiology 3, 103–107.Google ScholarPubMed
Cucchiaro, J. & Guillery, R.W. (1984). The development of the retinogeniculate pathways in normal and albino ferrets. Proceedings of the Royal Society of London B 223, 141–164.Google ScholarPubMed
Derrington, A.M., & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology 357, 219–240.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr. (1975). Another look at lateral geniculate lamination in the cat. Neuroscience Abstracts 1, 41.Google Scholar
Friedlander, M.J., Lin, C.-S., Stanford, L.R. & Sherman, S.M. (1981). Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. Journal of Neurophysiology 46, 80–129.CrossRefGoogle ScholarPubMed
Garraghty, P.E., Frost, D.O. & Sur, M. (1987 a). The morphology of retinogeniculate X- and Y -cell axonal arbors in dark-reared cats. Experimental Brain Research 66, 115–127.CrossRefGoogle ScholarPubMed
Garraghty, P.E., Shatz, C.J., Sretavan, D.W. & Sur, M. (1987 b). Prenatal monocular enucleation in the cat: effects on the morphology of retinogeniculate axons and formation of laminae in the lateral geniculate nucleus. Investigative Ophthalmology and Visual Science (Suppl.) 28, 335.Google Scholar
Garraghty, P.E., Sur, M., Weller, R.E. & Sherman, S.M. (1986). Morphology of retinogeniculate X and Y axon arbors in monocularly enucleated cats. Journal of Comparative Neurology 251, 198–215.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1967). Patterns of fiber degeneration in the dorsal lateral geniculate nucleus of the cat following lesions in the visual cortex. Journal of Comparative Neurology 130, 197–222.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1970). The laminar distribution of retinal fibers in the dorsal lateral geniculate nucleus of the cat: a new interpretation. Journal of Comparative Neurology 138, 339–368.CrossRefGoogle Scholar
Guillery, R.W. (1979). A speculative essay on geniculate lamination and its development. Progress in Brain Research 51, 403–418.CrossRefGoogle ScholarPubMed
Guillery, R.W. & Kaas, J.H. (1971). A study of normal and congenially abnormal retinogeniculate projections in cats. Journal of Comparative Neurology 143, 73–100.CrossRefGoogle Scholar
Guillery, R.W., LaMantia, A.S., Robson, J.A. & Huang, K. (1985). The influence of retinal afferents upon the development of layers in the dorsal lateral geniculate nucleus of Mustelids. Journal of Neuroscience 5, 1370–1379.CrossRefGoogle ScholarPubMed
Guillery, R.W. & Oberdorfer, M.D. (1977). A study of fine and coarse retinofugal axons terminating in the geniculate C laminae and in the medial interlaminar nucleus of the mink. Journal of Comparative Neurology 176, 515–526.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Wilson, J.R. & Ogren, M.P. (1978). The neuroanatomical organizations of pathways between dorsal lateral geniculate nucleus and visual cortex in Old and New World primates. Journal of Comparative Neurology 182, 123–136.CrossRefGoogle ScholarPubMed
Hickey, T.L. (1980). Development of the dorsal lateral geniculate nucleus in normal and visually deprived cats. Journal of Comparative Neurology 189, 467–481.CrossRefGoogle ScholarPubMed
Hickey, T.L. & Guillery, R.W. (1974). An autoradiographic study of retino-geniculate pathways in the cat and the fox. Journal of Comparative Neurology 156, 239–254.CrossRefGoogle Scholar
Humphrey, A.L., Sur, M., Uhlrich, D.J. & Sherman, S.M. (1985). Projection patterns of individual X- and Y-cell axons from the lateral geniculate nucleus to cortical area 17 in the cat. Journal of Comparative Neurology 233, 159–189.CrossRefGoogle ScholarPubMed
Irvin, G.E., Norton, T.T., Sesma, M.A. & Casagrande, V.A. (1986). W-like response properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Research 362, 254–274.CrossRefGoogle ScholarPubMed
Kaas, J.H., Guillery, R.W. & Allman, J.M. (1972). Some principles of organization in the dorsal lateral geniculate nucleus. Brain, Behavior and Evolution 6, 253–299.CrossRefGoogle ScholarPubMed
Kaas, J.H., Guillery, R.W. & Allman, J.M. (1973). Discontinuities in the dorsal lateral geniculate nucleus corresponding to the optic disc: a comparative study. Journal of Comparative Neurology 147, 163–180.CrossRefGoogle Scholar
Kaas, J.H., Huerta, M.F., Weber, J.T. & Harting, J.K. (1978). Pattern of retinal terminations and laminar organization of the lateral geniculate nucleus of primates. Journal of Comparative Neurology 182, 517–554.CrossRefGoogle ScholarPubMed
LeVay, S. & McConnell, S.K. (1982). On and off layers in the lateral geniculate nucleus of the mink. Nature 300, 350–351.CrossRefGoogle ScholarPubMed
LeVay, S., McConnell, S.K. & Luskin, M.B. (1987). Functional organization of primary visual cortex in the mink (Mustela vison), and a comparison with the cat. Journal of Comparative Neurology 257, 422–441.CrossRefGoogle Scholar
Leventhal, A.G. (1979). Evidence that the different classes of relay cells of the cat's lateral geniculate nucleus terminate in different layers of the striate cortex. Experimental Brain Research 37, 349–372.CrossRefGoogle ScholarPubMed
Linden, D.C., Guillery, R.W. & Cucchiaro, J. (1981). The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. Journal of Comparative Neurology 203, 189–211.CrossRefGoogle ScholarPubMed
McConnell, S.K. & LeVay, S. (1984). Segregatio of on- and off-center afferents in mink visual cortex. Proceedings of the National Academy of Science of the U.S.A. 81, 1590–1593.CrossRefGoogle Scholar
Murakami, D.M. & Wilson, P.D. (1987). The development of soma size changes in the C-laminae of the cat lateral geniculate nucleus following monocular deprivation. Developmental Brain Research 35, 215–224.CrossRefGoogle Scholar
Raczkowski, D. & Rosenquist, A.C. (1983). Connections of the multiple visual cortical areas with the lateral posterior-pulvinar complex and adjacent thalamic nuclei in the cat. Journal of Neuroscience 3, 1912–1942.CrossRefGoogle ScholarPubMed
Rakic, P. (1981). Development of visual centers in the primate brain depends on binocular competition before birth. Science 214, 928–931.CrossRefGoogle ScholarPubMed
Rioch, D.M. (1929). Studies on the diencephalon of carnivora. I. The nuclear configuration of the thalamus, epithalamus, and hypothalamus of the dog and cat. Journal of Comparative Neurology 49, 1–119.CrossRefGoogle Scholar
Rodieck, R.W. (1979). Visual pathways. Annual Review of Neuroscience 2, 193–225.CrossRefGoogle ScholarPubMed
Sanderson, K.J. (1971). The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. Journal of Comparative Neurology 143, 101–117.CrossRefGoogle Scholar
Sanderson, K.J. (1974). Lamination of the dorsal lateral geniculate nucleus of carnivores of the weasel (Mustelidae), raccoon (Procyonidae), and fox (Canidae) families. Journal of Comparative Neurology 153, 239–266.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Malpeli, J.G. (1978). Functional specificity of lateral geniculate nucleus laminae of the Rhesus monkey. Journal of Comparative Neurophysiology 41, 788–797.CrossRefGoogle ScholarPubMed
Schmidt, J.T. & Tieman, S.B. (1985). Eye-specific segregation of optic afferents in mammals, fish, and frogs: the role of activity. Cellular and Molecular Neurobiology 5, 5–34.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1983). The prenatal development of the cat's retinogeniculate pathway. Journal of Neuroscience 3, 482–499.CrossRefGoogle ScholarPubMed
Shatz, C.J. & Stryker, M.P. (1986). Tetrodotoxin infusion prevents the formation of eye-specific layers during prenatal development of the cat's retinogeniculate projection. Neuroscience Abstracts 12, 589.Google Scholar
Sherman, S.M. (1985). Functional organization of the W-, X-, and Y-cell pathways in the cat: a review and hypothesis. In Progress in Psychobiology and Physiological Psychology, Vol. II. eds. Sprague, J.M. & Epstein, A.N., pp. 233–314. New York: Academic Press.Google Scholar
Shook, B.L. & Chalupa, L.M. (1986). Organization of geniculocortical connections following prenatal interruption of binocular interactions. Developmental Brain Research 28, 47–62.CrossRefGoogle Scholar
Sretavan, D.W. & Shatz, C.J. (1986). Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers within the cat's lateral geniculate nucleus. Journal of Neuroscience 6, 234–251.CrossRefGoogle ScholarPubMed
Sretavan, D.W., Garraghty, P.E., Sur, M. & Shatz, C.J. (1985). Development of retinogeniculate axon arbors following prenatal unilateral enucleation. Neuroscience Abstracts 11, 805.Google Scholar
Stanford, L.R., Friedlander, M.J. & Sherman, S.M. (1981). Morphology of physiologically identified W-cells in the C laminae of the cat's lateral geniculate nucleus. Journal of Neuroscience 1, 578–584.CrossRefGoogle Scholar
Stanford, L.R., Friedlander, M.J. & Sherman, S.M. (1983). Morphological and physiological properties of geniculate W-cells: a comparison with X- and Y-cells. Journal of Neurophysiology 50, 582–608.CrossRefGoogle ScholarPubMed
Stryker, M.P. & Zahs, K.R. (1983). On and off sublaminae in the lateral geniculate nucleus of the ferret. Journal of Neuroscience 3, 1943–1951.CrossRefGoogle ScholarPubMed
Sur, M., Esguerra, M., Garraghty, P.E., Kritzer, M.F. & Sherman, S.M. (1987). Morphology of physiologically identified retinal X- and Y-cell axons in the cat lateral geniculate nucleus. Journal of Neurophysiology 58, 1–32.CrossRefGoogle Scholar
Sur, M. & Sherman, S.M. (1982 a). Linear and nonlinear W-cells in C-laminae of the cat's lateral geniculate nucleus. Journal of Neurophysiology 47, 869–884.CrossRefGoogle ScholarPubMed
Sur, M. & Sherman, S.M. (1982 b). Retinogeniculate terminations in cats: morphological differences between X and Y cell axons. Science 218, 389–391.CrossRefGoogle ScholarPubMed
Updyke, B.V. (1977). Topographic organization of the projections from cortical areas 17, 18, and 19 onto the thalamus, pretectum, and superior colliculus in the cat. Journal of Comparative Neurology 173, 81–122.CrossRefGoogle Scholar
Wilson, P.D., Rowe, M.H. & Stone, J. (1976). Properties of relay cells in cat's lateral geniculate nucleus: a comparison of W-cells with X- and Y-cells. Journal of Neurophysiology 39, 1193–1209.CrossRefGoogle ScholarPubMed