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Laminar organization and ultrastructure of GABA-immunoreactive neurons and processes in the dorsal lateral geniculate nucleus of the tree shrew (Tupaia belangeri)

Published online by Cambridge University Press:  02 June 2009

Robert N. Holdefer ,
Thomas T. Norton  and
Ranney Mize R.
Robert N. Holdefer
Affiliation:
Department of Physiological Optics, School of Optometry/The Medical Center, The University of Alabama at Birmingham, Birmingham
Thomas T. Norton
Affiliation:
Department of Physiological Optics, School of Optometry/The Medical Center, The University of Alabama at Birmingham, Birmingham
Ranney Mize R.
Affiliation:
Department of Anatomy and Neurobiology, University of Tennessee, Memphis, The Health Sciences Center, Memphis
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Abstract

The distribution and ultrastructure of neurons and neuropil labeled by an antiserum to gamma-aminobutyric acid (GABA) were examined in the lateral geniculate nucleus (LGN) of the tree shrew (Tupaia belangeri). The LGN of this species segregates center type and cell class into three distinct pairs of laminae: a medial pair (laminae 1 and 2) containing ON-center cells, a more lateral pair (4, 5) containing OFF-center cells, and 2 laminae (3, 6) containing W-like cells. The relationship between this laminar segregation and the distribution of GABA immunoreactivity was investigated in the present study. GABA-immunoreactive neurons and neuropil were present in all six of the laminae. However, both the density of labeled cells (adjusted for neuronal density across laminae) and the density of labeled neuropil showed a medial-to-lateral gradient. The adjusted density of labeled cells was higher laterally than medially, and the density of labeled neuropil was significantly greater in the more lateral OFF-center laminae and W-like laminae than in the medial two ON-center laminae. Thus, inhibitory, GABAergic influences may modulate to different degrees the visual signals in the ON, OFF, and W pathways. Labeled cells had a mean cross-sectional area (107 μm2) approximately one-half that of unlabeled cells (216 μm2). They constitute 16–34% of the neurons in the LGN. At the electron microscope level, three different kinds of labeled profile were observed. Vesicle containing profiles like the F2 profiles of cat were postsynaptic to retinal terminals and presynaptic to conventional dendrites. Fl axon terminals with dense clusters of vesicles were also labeled as were some myelinated axons. Another labeled profile, which we suggest should be called an F3 process, was a large dendrite of irregular caliber with punctate groups of vesicles near the synapse. Our results suggest that GABAergic circuitry is an important part of the functional organization in the LGN of the tree shrew.

Keywords

Dorsal lateral geniculate nucleusGABA immunocytochemistryTree shrewVentral lateral geniculate nucleusThalamic reticular nucleus
Type
Research Article
Information
Visual Neuroscience , Volume 1 , Issue 2 , March 1988 , pp. 189 - 204
Copyright
Copyright © Cambridge University Press 1988

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References

Ahlsen, G., Lindstrom, S. & Lo, F.S. (1985). Interaction between inhibitory pathways to principal cells in the lateral geniculate nucleus of the cat. Experimental Brain Research 58, 134–143.CrossRefGoogle ScholarPubMed
Berardi, N. & Morrone, M.C. (1984). The role of γ-aminobutyric acid mediated inhibition in the response properties of cat lateral geniculate nucleus neurones. Journal of Physiology 357, 505–523.CrossRefGoogle ScholarPubMed
Brunso-Bechtold, J.K. & Casagrande, V.A. (1985). Ultrastructure of the developing tree shrew lateral geniculate nucleus. Brain Research 355, 310–314.CrossRefGoogle ScholarPubMed
Bullier, J. & Norton, T.T. (1979 a). X and Y relay cells in the cat lateral geniculate nucleus: quantitative analysis of receptive-field properties and classification. Journal of Neurophysiology 42, 244–273.CrossRefGoogle ScholarPubMed
Bullier, J. & Norton, T.T. (1979 b). Comparison of the receptive-field properties of X and Y ganglion cells with X and Y geniculate cells in the cat. Journal of Neurophysiology 42, 274–291.CrossRefGoogle ScholarPubMed
Casagrande, V.A. (1974). The laminar organization and connections of the lateral geniculate nucleus in the tree shrew (Tupaia glis). Anatomical Record 178, 323.Google Scholar
Casagrande, V.A., Guillery, R.W. & Harting, J.K. (1978). Differential effects of monocular deprivation seen in different layers of the lateral geniculate nucleus. Journal of Comparative Neurology 179, 469–486.CrossRefGoogle ScholarPubMed
Cleland, B.G. & Lee, B.B. (1985). A comparison of visual responses of cat lateral geniculate neurons with those of ganglion cells afferent to them. Journal of Physiology 369, 249–268.CrossRefGoogle Scholar
Conley, M., Fitzpatrick, D. & Diamond, I.T. (1984). The laminar organization of the lateral geniculate body and striate cortex in the tree shrew (Tupaia glis). Journal of Neuroscience 4, 171–197.CrossRefGoogle ScholarPubMed
Conway, J.L. & Schiller, P.H. (1983). Laminar organization of tree shrew dorsal lateral geniculate nucleus. Journal of Neurophysiol-ogy 50, 1330–1342.CrossRefGoogle ScholarPubMed
Curtis, D.R. & Tebecis, A.K. (1972). Bicuculline and thalamic inhibition. Experimental Brain Research 16, 210–218.CrossRefGoogle ScholarPubMed
Dreher, B., Fukuda, Y. & Rodieck, R.W. (1976). Identification, classification and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of old-world primates. Journal of Physiology 258, 433–452.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1970). Dendro-dendritic synapses in the lateral geniculate nucleus of the cat. Brain Research 20, 181–191.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Peters, A. (1972). The synaptic glomerulus and the intrinsic neuron in the dorsal lateral geniculate nucleus of the cat. Journal of Comparative Neurology 144, 285–334.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Luppino, G., Schmechel, D. & Diamond, I.T. (1985). Subcortical projections to the lateral geniculate nucleus in galago and tree shrew. Society for Neuroscience Abstracts 11, 230.Google Scholar
Fitzpatrick, D., Penny, G.R. & Schmechel, D.E. (1984). Glutamic acid decarboxylase-immunoreactive neurons and terminals in the lateral geniculate nucleus of the cat. Journal of Neuroscience 4, 1809–1829.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Penny, G.R., Schmechel, D.E. & Diamond, I.T. (1982). GAD immunoreactive neurons in the lateral geniculate nucleus of the cat and Galago. Society for Neuroscience Abstracts 8, 261.Google Scholar
Fukuda, Y. & Stone, J. (1976). Evidence of differential inhibitory influences on X- and Y-type relay cells in the cat's lateral geniculate nucleus. Brain Research 113, 188–196.CrossRefGoogle ScholarPubMed
Glickstein, M. (1967). Laminar structure of the dorsal lateral geniculate nucleus in the tree shrew (Tupaia glis). Journal of Comparative Neurology 131, 93–102.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1969). The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Zeitschrift für Zellforschung und Mikroskopische Anatomie 96, 1–38.CrossRefGoogle ScholarPubMed
Hajdu, F., Hassler, R. & Somogyi, Gy. (1982). Neuronal and synaptic organization of the lateral geniculate nucleus of the tree shrew (Tupaia glis). Cell Tissue Research 224, 207–223.CrossRefGoogle ScholarPubMed
Hamori, J., Pasik, T., Pasik, P. & Szentagothai, J. (1974). Triadic synaptic arrangements and their possible significance in the lateral geniculate nucleus of the monkey. Brain Research 80, 379–393.CrossRefGoogle ScholarPubMed
Hamos, J.E., Van Horn, S.C., Raczkowski, D., Uhlrich, D.J. & Sherman, S.M. (1985). Synaptic connectivity of a local circuit neurone in lateral geniculate nucleus of the cat. Nature 317, 618–621.CrossRefGoogle ScholarPubMed
Harting, J.K., Diamond, I.T. & Hall, W.C. (1973). Anterograde degeneration study of the cortical projections of the lateral geniculate and pulvinar nuclei in the tree shrew (Tupaia glis). Journal of Comparative Neurology 146, 393–440.CrossRefGoogle Scholar
Hendrickson, A.E., Ogren, M.P., Vaughn, J.E., Barber, R.P. & Wu, J.Y. (1983). Light and electron microscopic immunocytochemical localization of glutamic acid decarboxylase in monkey geniculate complex: evidence for GABAergic neurons and synapses. Journal of Neuroscience 3, 1245–1262.CrossRefGoogle ScholarPubMed
Hendrickson, A., Ryan, M., Noble, B. & Wu, J.-Y. (1985). Colocalization of [3H]muscimol and antisera to GABA and glutamic acid decarboxylase within the same neurons in monkey retina. Brain Research 348, 391–396.CrossRefGoogle ScholarPubMed
Hickey, T.L. & Hitchcock, P.F. (1984). Genesis of neurons in the dorsal lateral geniculate nucleus of the cat. Journal of Comparative Neurology 228, 186–199.CrossRefGoogle ScholarPubMed
Holdefer, R.N. & Norton, T.T. (1986). Laminar organization of receptive-field properties in the lateral geniculate nucleus of the tree shrew (Tupaia belangeri). Society for Neuroscience Abstracts 12, 8.Google Scholar
Holdefer, R.N., Godwin, D.W., Zhang, Y. & Norton, T.T. (1987). Functional role of GABAergic circuitry in the LGN. Society for Neuroscience Abstracts 13, 203.Google Scholar
Houser, C.R., Vaughn, J.E., Barber, R.P. & Roberts, E. (1980). GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Research 200, 341–354.CrossRefGoogle ScholarPubMed
Hsu, S.M., Ratne, L. & Granger, H. (1981). The use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. Journal of Histochemistry and Cytochemistry 29, 577–580.CrossRefGoogle ScholarPubMed
Irvin, G.E., Norton, T.T., Sesma, M.A. & Casagrande, V.A. (1986). W-like receptive-field properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Research 362, 254–270.CrossRefGoogle ScholarPubMed
Jones, E.G. (1975). Some aspects of the organization of the thalamic reticular complex. Journal of Comparative Neurology 162, 285–308.CrossRefGoogle ScholarPubMed
Kaplan, E., Purpura, K. & Shapley, R.M. (1987). Contrast affects the transmission of visual information through the mammalian lateral geniculate nucleus. Journal of Physiology 391, 267–288.CrossRefGoogle ScholarPubMed
Kayama, Y., Hsiao, C.-F., Fukuda, Y. & Iwama, K. (1981). Sensitivity to GABA of neurons of the dorsal and ventral lateral geniculate nuclei in the rat. Brain Research 211, 202–205.CrossRefGoogle ScholarPubMed
Keppel, G. (1973). Design and Analysis: A Researcher's Handbook. Englewood Cliffs, New Jersey: Prentice-Hall.Google Scholar
Kretz, R., Rager, G. & Norton, T.T. (1986). Laminar organization of ON and OFF regions and ocular dominance in the striate cortex of the tree shrew (Tupaia belangeri). Journal of Comparative Neurology 251, 135–145.CrossRefGoogle Scholar
Lennie, P. (1980). Parallel visual pathways: a review. Vision Research 20, 561–594.CrossRefGoogle ScholarPubMed
Lindstrom, S. (1982). Synaptic organization of inhibitory pathways to principal cells in the lateral geniculate nucleus of the cat. Brain Research 234, 447–453.CrossRefGoogle ScholarPubMed
Madarasz, M., Somogyi, G., Somogyi, J. & Hamori, J. (1985). Numerical estimation of γ-aminobutyric acid (GABA)-containing neurons in three thalamic nuclei of the cat: direct GABA immunocytochemistry. Neuroscience Letters 61, 73–78.CrossRefGoogle ScholarPubMed
Maley, B. & Newton, B.W. (1985). Immunohistochemistry of γ-aminobutyric acid in the cat nucleus tractus solitarius. Brain Research 330, 364–368.CrossRefGoogle ScholarPubMed
Mize, R.R., Spencer, R.F. & Horner, L.H. (1986). Quantitative comparison of retinal synapses in the dorsal and ventral (parvocellular) C laminae of the cat dorsal lateral geniculate nucleus. Journal of Comparative Neurology 248, 57–73.CrossRefGoogle Scholar
Montero, V.M. & Scott, G.L. (1981). Synaptic terminals in the dorsal lateral geniculate nucleus from neurons of the thalamic reticular nucleus: a light and electron microscope autoradiographic study. Neuroscience 6, 2561–2577.CrossRefGoogle ScholarPubMed
Montero, V.M. & Singer, W. (1984). Ultrastructure and synaptic relations of neural elements containing glutamic acid decarboxylase (GAD) in the perigeniculate of the cat: a light and electron microscopic immunocytochemical study. Experimental Brain Research 56, 115–125.CrossRefGoogle Scholar
Norton, T.T. (1982). Geniculate and extrageniculate visual systems in the tree shrew. In Changing Concepts of the Nervous System ed. Morrison, A.R. & Strick, P.L., pp. 377–409. New York: Academic Press.CrossRefGoogle Scholar
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, 715–741.CrossRefGoogle ScholarPubMed
Norton, T.T., Kretz, R. & Rager, G. (1985). ON and OFF regions in layer IV of striate cortex. Brain Research 327, 319–323.CrossRefGoogle ScholarPubMed
Norton, T.T., Holdefer, R.N., Zhang, Y. & Godwin, D.W. (1988). Effects of bicuculline on contrast sensitivity functions of lateral geniculate nucleus (LGN) relay cells. Investigative Ophthalmology and Visual Science (Suppl.) 29, 296.Google Scholar
Ohara, P.T., Lieberman, A.R., Hunt, S.P. & Wu, J.T. (1983). Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat: immunohistochemical studies by light and electron microscopy. Neuroscience 8, 189–211.CrossRefGoogle ScholarPubMed
Ohara, P.T., Sefton, A.J. & Lieberman, A.R. (1980). Mode of termination of afferents from thalamic reticular nucleus in the dorsal lateral geniculate nucleus of the rat. Brain Research 197, 503–506.CrossRefGoogle ScholarPubMed
Rapisardi, S.C. & Miles, T.P. (1984). Synaptology of retinal terminals in the dorsal lateral geniculate nucleus of the cat. Journal of Comparative Neurology 223, 515–534.CrossRefGoogle ScholarPubMed
Reger, J.F., Fitzgerald, M.E. & Mize, R.R. (1986). GABA antiserum reactivity in the lateral geniculate nucleus of the cat. Investigative Ophthalmology and Visual Science (Suppl.) 27, 205.Google Scholar
Schiller, P.H. & Malpeli, J.G. (1978). Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. Journal of Neu-rophysiology 41, 788–797.Google ScholarPubMed
Sillito, A.M. & Kemp, J.A. (1983). The influence of GABAergic inhibitory processes on the receptive-field structure of X- and Y-cells in cat dorsolateral geniculate nucleus (dLGN). Brain Research 277, 63–77.CrossRefGoogle Scholar
Singer, W. (1977). Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. Physiological Reviews 57, 386–420.CrossRefGoogle ScholarPubMed
Sterling, P. & Davis, T.L. (1980). Neurons in cat lateral geniculate nucleus that concentrate exogenous [3H]-γ-aminobutyric acid (GABA). Journal of Comparative Neurology 192, 737–749.CrossRefGoogle ScholarPubMed
Wilson, J.R., Bullier, J. & Norton, T.T. (1988). Signal-to-noise comparisons for X- and Y-cells in the retina and lateral geniculate nucleus of the cat. Experimental Brain Research (in press).CrossRefGoogle Scholar
Wilson, J.R. & Hendrickson, A.E. (1981). Neuronal and synaptic structure of the dorsal lateral geniculate nucleus in normal and monocularly deprived Macaca monkeys. Journal of Comparative Neurology 197, 517–539.CrossRefGoogle ScholarPubMed
Zempel, J. & Montero, V.M. (1985). Two types of GABA-containing interneurons in the A-laminae of the cat LGN: a double-label HRP and GABA-immunocytochemical study. Society for Neuroscience Abstracts 11, 317.Google Scholar