Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T15:48:49.444Z Has data issue: false hasContentIssue false
  • English
  • Français

The segregation of ON- and OFF-center responses in the lateral geniculate nucleus of normal and monocularly enucleated ferrets

Published online by Cambridge University Press:  02 June 2009

James Morgan  and
Ian D. Thompson
James Morgan
Affiliation:
University Laboratory of Physiology, Parks Road, Oxford, OX1 3PT, UK
Ian D. Thompson
Affiliation:
University Laboratory of Physiology, Parks Road, Oxford, OX1 3PT, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

We have investigated the distribution of ON- and OFF-center responses in the lateral geniculate nucleus of ferrets with normal and abnormal retinal projections. Electrophysiological recordings in normal pigmented animals confirm previous studies on mustelids showing that ON-center responses are found in the anterior, inner parts of laminae A and AI and OFF-center responses in posterior, outer leaflets. In albino animals, lamina A displays normal patterns of ON/OFF segregation but in lamina AI, which receives an abnormal crossed retinal projection, no consistent patterns of segregation are found. Following monocular enucleation on the day of birth, the uncrossed projection in pigmented ferrets remains expanded across the LGN. Anatomically and physiologically, this projection is segregated into two leaflets: an anterior, inner ON-center leaflet and a posterior outer OFF-center leaflet. We conclude that the persistence of ON/OFF segregation, independent of geniculate location, suggests that self-sorting of retinal input is an important factor in generating the segregation.

Keywords

AlbinismLaminationCompetitionRetinal ganglion cellsDevelopment
Type
Research Article
Information
Visual Neuroscience , Volume 10 , Issue 2 , March 1993 , pp. 303 - 311
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

Archer, S.M., Dubin, M.W. & Stark, L.A. (1982). Abnormal development of kitten retino-geniculate connectivity in the absence of action potentials. Science 217, 743–745CrossRefGoogle ScholarPubMed
Bowling, D.B. & Wieniawa-Narkiewicz, E. (1986). The distribution of ON- and OFF-centre X- and Y-like cells in the A layers of the cat’s lateral geniculate nucleus. Journal of Physiology 375, 561–572CrossRefGoogle Scholar
Brunso-Bechtold, J.K. & Casagrande, V.A. (1982). Early postnatal development of laminar characteristics in the dorsal lateral geniculate nucleus of the tree shrew. Journal of Neuroscience 2, 589–597CrossRefGoogle ScholarPubMed
Casagrande, V.A. & Condo, G.J. (1988). The effects of altered neu-ronal activity of the development of layers in the lateral geniculate. Journal of Neuroscience 8, 395–416CrossRefGoogle Scholar
Chalupa, L.M. & Williams, R.W. (1984). Organization of the cat’s lateral geniculate nucleus following interruption of prenatal binocular competition. Human Neurobiology 3, 103–107Google ScholarPubMed
Coleman, L.-A. & Beazley, L.D. (1989). Expanded retinofugal projections to the dorsal lateral geniculate nucleus and superior colliculus after unilateral enucleation in the wallaby Setonix brachyurus, quokka. Developmental Brain Research 48, 273–291CrossRefGoogle Scholar
Constantine-Paton, M., Cline, H.T. & Debski, E. (1990). Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annual Review of Neuroscience 13, 129–154CrossRefGoogle ScholarPubMed
Conway, J.L. & Schiller, P.H. (1983). Laminar organisation of tree shrew dorsal lateral geniculate nucleus. Journal of Neurophysiology 50, 1330–1342CrossRefGoogle ScholarPubMed
Cucchiaro, J. & Guillery, R.W. (1984). The development of the retinogeniculate pathways in normal and albino ferrets. Proceedings of Royal Society B (London) 223, 141–164Google ScholarPubMed
Dubin, M.W., Stark, L.A. & Archer, S.M. (1986). A role for action potential activity in the development of neuronal connections in the kitten retinogeniculate pathway. Journal of Neuroscience 6, 1021–1036CrossRefGoogle ScholarPubMed
Galli, L. & Maffei, L. (1988). Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science 242, 90–91CrossRefGoogle ScholarPubMed
Garraghty, P.E., Shatz, C.J., Sretavan, D.W. & Sur, M. (1988 a). Axon arbors of X and Y retinal axons are differentially affected by prenatal disruption of binocular inputs. Proceedings of the National Academy of Sciences of the U.S.A. 85, 7361–7365CrossRefGoogle ScholarPubMed
Garraghty, P.E., Shatz, C.J. & Sur, M. (1988 b). Prenatal disruption of binocular interactions creates novel lamination in the cat’s lateral geniculate nucleus. Visual Neuroscience 1, 93–102CrossRefGoogle ScholarPubMed
Glickstein, M. & Millodot, M. (1970). Retinoscopy and eye size. Science 168, 605–606CrossRefGoogle ScholarPubMed
Guillery, R.W. (1971). An abnormal retinogeniculate projection in the albino ferret (Mustela furo). Brain Research 33, 482–485CrossRefGoogle ScholarPubMed
Guillery, R.W. (1979). A speculative essay on geniculate lamination and its development. Progress in Brain Research 51, 403–418CrossRefGoogle ScholarPubMed
Guillery, R.W. (1989). Early monocular enucleations in fetal ferrets produce a decrease of uncrossed and an increase of crossed retinofugal components: A possible model for the albino abnormality. Journal of Anatomy 164, 73–84Google 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, 1370–1379CrossRefGoogle ScholarPubMed
Guillery, R.W., Polley, E.H. & Torrealba, F. (1982). The arrangement of axons according to fibre diameter in the optic tract of the cat. Journal of Neuroscience 2, 714–721CrossRefGoogle ScholarPubMed
Hahm, J.-O., Langdon, R.B. & Sur, M. (1991). Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors. Nature 351, 568–570CrossRefGoogle ScholarPubMed
Henderson, Z. (1987). Cholinergic innervation of the ferret visual system. Neuroscience 20, 503–518CrossRefGoogle ScholarPubMed
Heumann, D. & Rabinowicz, T.H. (1980). Postnatal development of the dorsal lateral geniculate nucleus in the normal and enucleated albino mouse. Experimental Brain Research 38, 75–85CrossRefGoogle ScholarPubMed
Kageyama, G.H. & Wong-Riley, M.T.T. (1984). The histochemical localisation of cytochrome oxidase in the retina and lateral geniculate nucleus of the ferret, cat, and monkey with particular reference to retinal mosaics and ON/OFF-center visual channels. Journal of Neuroscience 4, 2445–2459CrossRefGoogle Scholar
Kaas, J.H., Guillery, R.W. & Allman, J.M. (1972). Some principles of organization in the dorsal lateral geniculate nucleus. Brain, Behaviour, and Evolution 6, 253–299CrossRefGoogle ScholarPubMed
Jenkins, E.C. (1972). Wire loop application of liquid emulsion to slides for autoradiography in light microscopy. Stain Technology 47, 23–26CrossRefGoogle ScholarPubMed
LeVay, S. & McConnell, S.K. (1982). ON and OFF layers in the lateral geniculate nucleus of the mink. Nature 300, 350–351CrossRefGoogle ScholarPubMed
LeVay, S., McConnell, S.K. & Luskin, M.B. (1987). Functional organisation of primary visual cortex in the Mink (Mustela vison) and a comparison with the cat. Journal of Comparative Neurology 257, 422–441CrossRefGoogle Scholar
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, 189–211CrossRefGoogle ScholarPubMed
Lund, R.D., Cunningham, T.J. & Lund, J.S. (1973). Modified optic projections after unilateral eye removal in young rats. Brain, Behaviour, and Evolution 8, 51–72CrossRefGoogle ScholarPubMed
Maffei, L. & Galli-Resta, L. (1990). Correlations in the discharges of neighbouring rat retinal ganglion cells during prenatal life. Proceedings of the National Academy of Sciences of the U.S.A. 87, 2861–2864CrossRefGoogle ScholarPubMed
Mastronarde, D.N. (1989). Correlated firing of retinal ganglion cells. Trends in Neuroscience 12, 75–80CrossRefGoogle ScholarPubMed
Meister, M., Wong, R.O.L., Baylor, D.A. & Shatz, C.J. (1991). Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939–943CrossRefGoogle ScholarPubMed
Merrill, E.G. & Ainsworth, A. (1972). Glass-coated platinum-plated tungsten microelectrodes. Medical and Biological Engineering 10, 662–672CrossRefGoogle ScholarPubMed
Morgan, J.E. (1986). The organization of the retinogeniculate pathways in normal and neonatally enucleated pigmented and albino ferrets. D.Phil. Thesis, University of Oxford.Google Scholar
Morgan, J.E., Henderson, Z. & Thompson, I.D. (1987). Retinal decussation patterns in pigmented and albino ferrets. Neuroscience 20, 519–535CrossRefGoogle ScholarPubMed
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, 1101–1123CrossRefGoogle Scholar
Price, D.J. & Morgan, J.E. (1987). Spatial properties of neurones in the lateral geniculate nucleus of the pigmented ferret. Experimental Brain Research 68, 28–36CrossRefGoogle ScholarPubMed
Rakic, P. (1981). Development of visual centres in the primate brain depends on binocular competition before birth. Science 214, 928–931CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1979). Visual pathways. Annual Review of Neuroscience 2, 193–225CrossRefGoogle ScholarPubMed
Roe, A.W., Garraghty, P.E. & Sur, M. (1989). Terminal arbors of single ON-centre and OFF-centre X and Y retinal ganglion cell axons within the ferret’s lateral geniculate nucleus. Journal of Comparative Neurology 288, 208–242CrossRefGoogle Scholar
Sanderson, K.J. (1974). Lamination of the dorsal lateral geniculate of the weasel (Mustelidae), raccoon (Procyonidae), and fox (Canidae) families. Journal of Comparative Neurology 153, 239–266CrossRefGoogle ScholarPubMed
Sanderson, K.J., Guillery, R.W. & Shackelford, R.M. (1974). Congenitally abnormal visual pathways in mink (Mustela vison) with reduced retinal pigment. Journal of Comparative Neurology 154, 225–248CrossRefGoogle ScholarPubMed
Shapley, R. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neuroscience 9, 229–235CrossRefGoogle Scholar
Shatz, C.J. (1990). Impulse activity and the patterning of connections during CNS development. Neuron 5, 745–756CrossRefGoogle ScholarPubMed
Shatz, C.J. & Stryker, M.P. (1988). Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242, 87–89CrossRefGoogle ScholarPubMed
Sherman, S.M. & Spear, P.D. (1982). Organisation of visual pathways in normal and visually deprived cats. Physiological Reviews 62, 738–855CrossRefGoogle ScholarPubMed
Shook, B.L. & Chalupa, L.M. (1986). Organization of geniculo-cortical connections following prenatal disruption of binocular interactions. Developmental Brain Research 28, 47–62CrossRefGoogle Scholar
So, K.-F., Woo, H.H. & Jen, L.S. (1984). The normal and abnormal postnatal development of retinogeniculate projections in golden hamsters: An anterograde horseradish peroxidase tracing study. Developmental Brain Research 12, 191–205CrossRefGoogle Scholar
Sretavan, D.W. & Shatz, C.J. (1986). Prenatal development of cat retinogeniculate axon arbors in the absence of binocular interactions. Journal of Neuroscience 6, 990–1003CrossRefGoogle ScholarPubMed
Stryker, M.P. & Zahs, K. (1983). ON and OFF sublaminae in the lateral geniculate nucleus of the ferret. Journal of Neuroscience 3, 1943–1951CrossRefGoogle ScholarPubMed
Thompson, I.D., Jeffery, G., Morgan, J.E. & Baker, G. (1991). Albino gene dosage and retinal decussation patterns in the pigmented ferret. Visual Neuroscience 6, 393–398CrossRefGoogle ScholarPubMed
Thompson, I.D., Morgan, J.E. & Henderson, Z. (1992). The effects of monocular enucleation on ganglion cell number and terminal distribution in the ferret’s uncrossed retinal pathway (submitted for publication).Google Scholar
Walsh, C. & Guillery, R.W. (1985). Age-related fibre order in the optic tract of the ferret. Journal of Neuroscience 5, 3061–3070CrossRefGoogle ScholarPubMed
White, C.A., Chalupa, L.M., Maffei, L., Kirby, M.A. & Lia, B. (1989). Response properties in the dorsal lateral geniculate nucleus of the adult cat after interruption of prenatal binocular interactions. Journal of Neurophysiology 62, 1039–1051CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Hubei, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiology 29, 1115–1156CrossRefGoogle ScholarPubMed
Williams, R.W. & Rakic, P. (1988). Elimination of neurons from the rhesus monkey’s lateral geniculate nucleus during development. Journal of Comparative Neurology 272, 424–436CrossRefGoogle ScholarPubMed