Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-24T01:40:40.893Z Has data issue: false hasContentIssue false
  • English
  • Français

Quantitative analyses of synaptic contacts of interneurons in the dorsal lateral geniculate nucleus of the squirrel monkey

Published online by Cambridge University Press:  02 June 2009

James R. Wilson ,
Donna M. Forestner  and
Ryan P. Cramer
James R. Wilson
Affiliation:
Yerkes Regional Primate Research Center, and Departments of Anatomy and Cell Biology, and Ophthalmology, Emory University, Atlanta
Donna M. Forestner
Affiliation:
Yerkes Regional Primate Research Center, and Departments of Anatomy and Cell Biology, and Ophthalmology, Emory University, Atlanta
Ryan P. Cramer
Affiliation:
Yerkes Regional Primate Research Center, and Departments of Anatomy and Cell Biology, and Ophthalmology, Emory University, Atlanta
Get access Rights & Permissions [Opens in a new window]

Abstract

Three interneurons were recorded from and then injected with horseradish peroxidase in the parvocellular laminae of the squirrel monkey's (Saimiri sciureus) dorsal lateral geniculate nucleus. They were then examined using the electron microscope for their synaptic contacts, both the afferent contacts onto their dendrites and their presynaptic dendritic contacts onto presumptive projection (relay) neuron dendrites. The somata of these interneurons were small (mean = 178 μm2), but the dendritic trees were large compared with those of projection neurons. All three interneurons had similar synaptic patterns onto their dendrites with about equal numbers of retinal, cortical, and GABAergic contacts. The distribution of these contacts was more uniform compared with the same types of contacts made onto projection neurons. The presynaptic dendrites were observed to contact only the dendrites of presumptive projection neurons, and these contacts were nearly all in the form of geniculate triads. None of the three interneurons displayed an axon. The receptive fields of these interneurons were similar to those of projection cells, but were larger and had center-response signs that were the opposite of the projection neurons around them (e.g. OFF center for the dorsal part of the parvocellular mass where ON-center projection neurons reside). The squirrel monkey data provides additional evidence that one aspect of the laminar pattern observed in the parvocellular pathway of the primate's dLGN might be related to a segregation of projection neurons of one center-response sign with interneurons of the opposite center-response sign.

Keywords

PrimateVisual pathwaysHorseradish peroxidaseThalamus
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 6 , November 1996 , pp. 1129 - 1142
Copyright
Copyright © Cambridge University Press 1996

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., Blakemore, C. & Pettigrew, J.D. (1967). The neural mechanism of binocular depth discrimination. Journal of Physiology (London) 193, 327–342.CrossRefGoogle ScholarPubMed
Bickford, M.E., Günlïk, A.E., Godwin, D.W., Gnadt, J.W. & Sherman, S.M. (1995). Subcortical extraretinal projections to the monkey LGN. Society for Neuroscience Abstracts 21, 658.Google Scholar
Conley, M., Birecree, F. & Casagrande, V.A. (1985). Neuronal classes and their relation to functional and laminar organization of the lateral geniculate nucleus: A Golgi study of the prosimian primate, Galago crassicaudatus. Journal of Comparative Neurology 242, 561–583.CrossRefGoogle ScholarPubMed
Conley, M. & Wilson, K.F. (1992). Dendritic organization of class II (inter)neurons in the dorsal lateral geniculate nucleus of the tree shrew: Observation based on Golgi, immunocytochemical, and biocytin methods. Journal of Comparative Neurology 319, 51–65.CrossRefGoogle ScholarPubMed
Cucchiaro, J.B., Bickford, M.E. & Sherman, S.M. (1991 a). A GABAergic projection from the pretectum to the dorsal lateral geniculate nucleus in the cat. Neuroscience 41, 213–226.CrossRefGoogle Scholar
Cucchiaro, J.B., Uhlrich, D.J. & Sherman, S.M. (1991 b). Electronmicroscopic analysis of synaptic input from the perigeniculate nucleus to the A-laminae of the lateral geniculate nucleus in cats. Journal of Comparative Neurology 310, 316–336.CrossRefGoogle Scholar
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology (London) 357, 219–240.CrossRefGoogle ScholarPubMed
Feig, S. & Harting, J.K. (1994). Ultrastructural studies of the primate lateral geniculate nucleus: Morphology and spatial relationships of axon terminals arising from the retina, visual cortex (area 17), superior colliculus, parabigeminal nucleus, and pretectum of Galago crassicaudatus. Journal of Comparative Neurology 343, 17–34.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Usrey, W.M., Schofield, B.R. & Einstein, G. (1994). The sublaminar organization of corticogeniculate neurons in layer 6 of macaque striate cortex. Visual Neuroscience 11, 307–315.CrossRefGoogle ScholarPubMed
Gabbott, P.L.A. & Bacon, S.J. (1994). Two types of interneurons in the dorsal lateral geniculate nucleus of the rat: A combined NADPH diaphorase histochemical and GABA immunocytochemical study. Journal of Comparative Neurology 350, 281–301.CrossRefGoogle Scholar
Guillery, R.W. (1971). Patterns of synaptic interconnections in the dorsal lateral geniculate nucleus of cat and monkey: A brief review. Vision Research 3, 211–227.CrossRefGoogle Scholar
Hamori, J., Pasik, P. & Pasik, T. (1991). Different types of synaptic triads in the monkey dorsal lateral geniculate nucleus. Journal für Hirnforschung 32, 369–379.Google ScholarPubMed
Hamori, J., Pasik, T. & Pasik, P. (1978). Electron-microscopic identification of axonal initial segments belonging to interneurons in the dorsal lateral geniculate nucleus of the monkey. Neuroscience 3, 403–412.CrossRefGoogle ScholarPubMed
Hamos, J.F., 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
Hanker, J.S., Yates, P.E., Metz, C.B. & Rustoni, A. (1977). A new specific sensitive and non-carcinogenic agent for the demonstration of horseradish peroxidase. Histochemical Journal 9, 789–792.CrossRefGoogle Scholar
Harting, J.K., Van Lieshout, D.P. & Feig, S. (1991). Connectional studies of the primate lateral geniculate nucleus: Distribution of axons arising from the thalamic reticular nucleus of Galago crassicaudatus. Journal of Comparative Neurology 310, 411–427.CrossRefGoogle ScholarPubMed
Hendrickson, A.B., 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
Holdefer, R.N., Norton, T.T. & Godwin, D.W. (1989). Effects of bicuculline on signal detectability in lateral geniculate nucleus relay cells. Brain Research 488, 341–347.CrossRefGoogle ScholarPubMed
Kaas, J.H., Huerta, M.F., Weber, J.T. & Harting, J.K. (1978). Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus of primates. Journal of Comparative Neurology 182, 517–554.CrossRefGoogle ScholarPubMed
Labos, E., Pasik, P., Hamori, J. & Nogradi, E. (1990). On the dynamics of triad synaptic arrangements: Computer experiments with formal neural nets of chaotic units. Journal für Hirnforschung 6, 715–722.Google Scholar
Lennie, P. (1980). Parallel visual pathways: A review. Vision Research 20, 561–594.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
Lieberman, A.R. & Webster, K.E. (1974). Aspects of the synaptic organization of intrinsic neurons in the dorsal lateral geniculate nucleus. Journal of Neurocytology 3, 677–710.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1981). Effects of sleep and arousal in the processing of visual information in the cat. Nature 291, 554–561.CrossRefGoogle ScholarPubMed
Malpeli, J.G., Schiller, P.H. & Colby, C.L. (1981). Response properties of single cells in monkey striate cortex during reversible inactivation of individual lateral geniculate laminae. Journal of Physiology 46, 1102–1119.Google ScholarPubMed
McCormick, D.A. & Pape, H.-C. (1988). Acetylcholine inhibits identified interneurons in the cat lateral geniculate nucleus. Nature 334, 246–248.CrossRefGoogle ScholarPubMed
Michael, C.R. (1988). Retinal afferent arborization patterns, dendritic field orientations, and the segregation of function in the lateral geniculate nucleus of the monkey. Proceedings of the National Academy of Sciences of the U.S.A. 85, 4914–4918.CrossRefGoogle ScholarPubMed
Montero, V.M. (1986). The interneuronal nature of GABAergic neurons in the lateral geniculate nucleus of the rhesus monkey: A combined HRP and GABA-immunocytochemical study. Experimental Brain Research 64, 615–622.CrossRefGoogle ScholarPubMed
Montero, V.M. (1987). Ultrastructural identification of synaptic terminals from the axons of type 3 interneurons in the cat lateral geniculate nucleus. Journal of Comparative Neurology 264, 268–283.CrossRefGoogle ScholarPubMed
Montero, V.M. (1991). A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus. Experimental Brain Research 86, 257–270.CrossRefGoogle ScholarPubMed
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. (1985). Ultrastructural identification of somata and neural processes immunoreactive to antibodies against glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the cat. Experimental Brain Research 59, 151–165.CrossRefGoogle ScholarPubMed
Montero, V.M. & Zempel, J. (1986). The proportion and size of GABA-immunoreactive neurons in the magnocellular and parvocellular layers of the lateral geniculate nucleus of rhesus monkey. Experimental Brain Research 62, 215–223.CrossRefGoogle ScholarPubMed
Norton, T.T. & Godwin, D.W. (1992). Inhibitory GABAergic control of visual signals at the lateral geniculate nucleus. Progress in Brain Research 90, 193–217.CrossRefGoogle ScholarPubMed
Ohara, P.T., Sefton, A.J. & Lieberman, A.R. (1980). Mode of termination of afferents from the thalamic reticular nucleus in the dorsal lateral geniculate nucleus of the rat. Brain Research 197, 503–506.CrossRefGoogle ScholarPubMed
Pasik, P., Pasik, T., Hámori, J. & Szentágothai, P. (1973 a). Golgi type II interneurons in the neuronal circuit of the monkey lateral geniculate nucleus. Experimental Brain Research 17, 18–34.CrossRefGoogle ScholarPubMed
Pasik, P., Pasik, T., Hámori, J. & Szentágothai, P. (1973 b). “Triadic” synapses and other articulations of interneurons in the lateral geniculate of rhesus monkeys. Transactions of the American Neurological Association 98, 293–295.Google ScholarPubMed
Rapisardi, S. (1981). Serial thin section analysis of retino-geniculate afferents in the dorsal lateral geniculate nucleus of the monkey. Neuroscience Letters (Suppl.) 7, 51–52.Google Scholar
Saini, K.D. & Garey, L. (1981). Morphology of neurons in the lateral geniculate nucleus of the monkey. A Golgi study. Experimental Brain Research 42, 235–248.Google ScholarPubMed
Schiller, P.H. & Malpeli, J.G. (1978). Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. Journal of Neurophysiology 41, 788–794.CrossRefGoogle ScholarPubMed
Somogyi, P. (1988). Immunochemical demonstration of GABA in physiologically characterized HRP-filled neurons and their postsynaptic targets. In Techniques in the Behavioral and Neural Sciences, ed. van Leeuwen, F.W., Buijs, R.M., Pool, C.W. & Poch, O.L., pp. 339–359. Amsterdam: Elsevier Science Publishers.Google Scholar
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
Thurlow, G.A., Bowling, D.B. & Cooper, R.M. (1993). ON and OFF activity gradients in the lateral geniculate nucleus of the cat: A combined 14C 2-deoxyglucose and D, L-2-amino-4-phosphonobutyric acid study. Visual Neuroscience 10, 1027–1033.CrossRefGoogle Scholar
Uhlrich, D.J. & Cucchiaro, J.B. (1992). GABAergic circuits in the lateral geniculate nucleus of the cat. Progress in Brain Research 90, 171–192.CrossRefGoogle ScholarPubMed
Weber, A.J., Kalil, R.E. & Behan, M. (1989). Synaptic connections between corticogeniculate axons and interneurons in the dorsal lateral geniculate nucleus of the cat. Journal of Comparative Neurology 289, 156–164.CrossRefGoogle 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, 1115–1156.CrossRefGoogle ScholarPubMed
Wilson, J.R. (1989). Synaptic organization of individual neurons in the macaque lateral geniculate nucleus. Journal of Neuroscience 9, 2931–2953.CrossRefGoogle ScholarPubMed
Wilson, J.R. (1993). Circuitry of the dorsal lateral geniculate nucleus in the cat and monkey. Acia Anatomica 147, 1–13.CrossRefGoogle Scholar
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 70, 399–405.CrossRefGoogle ScholarPubMed
Wilson, J.R., Cowey, A. & Somogyi, P. (1995). GABA immunopositive axons in the optic nerve and optic tract of macaque monkeys. Vision Research 36, 1357–1363.CrossRefGoogle Scholar
Wilson, J.R. & Forestner, D.M. (1995). Synaptic inputs to single neurons in the lateral geniculate nuclei of normal and monocularly deprived squirrel monkeys. Journal of Comparative Neurology 362, 468–488.CrossRefGoogle ScholarPubMed
Wilson, J.R., Forestner, D.M., Counts, S., Uhlrich, D. & Manning, K. (1996). Histaminergic and cholinergic terminals in the lateral geniculate nucleus of macaque monkeys (submitted).Google Scholar
Wilson, J.R., Friedlander, M.J. & Sherman, S.M. (1984). Fine structural morphology of identified X- and Y-cells in the cat's lateral geniculate nucleus. Proceedings of the Royal Society B (London) 221, 411–436.Google ScholarPubMed
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
Wilson, J.R. & Hendrickson, A.E. (1988). Serotonergic axons in the monkey's lateral geniculate nucleus. Visual Neuroscience 1, 125–133.CrossRefGoogle ScholarPubMed
Winfield, D.A. (1980). The synaptic organization of glomeruli in the magnocellular and parvocellular laminae of the lateral geniculate nucleus in the monkey. Brain Research 198, 55–62.CrossRefGoogle ScholarPubMed
Wiser, A.K. & Callaway, E.M. (1996). Contributions of individual layer 6 pyramidal neurons to local circuitry in macaque primary visual cortex. Journal of Neuroscience 16, 2724–2739.CrossRefGoogle ScholarPubMed