Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-22T23:34:08.680Z Has data issue: false hasContentIssue false
  • English
  • Français

Quantitative light- and electron-microscopic analysis of cytochrome-oxidase distribution in neurons of the lateral geniculate nucleus of the adult monkey

Published online by Cambridge University Press:  02 June 2009

Suyan Liu  and
Margaret Wong-Riley
Suyan Liu
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee
Margaret Wong-Riley
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee
Get access Rights & Permissions [Opens in a new window]

Abstract

The distribution of cytochrome oxidase (CO) in the lateral geniculate nucleus (LGN) of normal adult macaque monkeys was analyzed in quantitative light- and electron-microscope (EM) studies. Both reactive and nonreactive neurons were found throughout laminae 1–6. Darkly reactive neurons were more numerous in laminae 1, 2, and 6. Within each lamina, there was a positive correlation between cell size and level of CO activity in neurons. The cell density was greater in laminae 1, 4, and 6, which received input from the contralateral eye, than in corresponding laminae representing the ipsilateral eye (2, 3, and 5). The cell density in each of the magnocellular laminae was less than that in each of the parvicellular laminae.

Three types of neurons could be distinguished within magnocellular laminae at the EM level. Types I and II were interpreted to be relay neurons, while the small size of type III qualified them to be interneurons. Two populations were found within parvicellular laminae, corresponding to relay neurons and interneurons, respectively. EM quantitative analyses revealed that the darkly reactive neurons contained a high proportion of moderate to darkly reactive mitochondria, which comprised 44.2%, 42.5%, and 39.2% of the mitochondrial population within neurons of laminae 1, 2, and 6 respectively. In contrast, a relatively low proportion of reactive mitochondria were found in neurons within laminae 3 (22.8%), 4 (26.4%), and 5 (32.4%). Moreover, magnocellular laminae contained a higher density of synapses on cell bodies than parvicellular laminae. All laminae, except layer 5, contained predominantly symmetric synapses on cell bodies. However, the proportion of symmetrical synapses in the magnocellular laminae (65.6%) was greater than that in the parvicellular laminae (59%).

Our quantitative light and EM results indicate that the level of metabolic activity in neurons of the monkey LGN is higher in magnocellular, ON-center, and contralateral than in parvicellular, OFF-center, and ipsilateral visual pathways, respectively. The metabolic activity of neurons is likely to reflect the chronic level of spontaneous and synaptically evoked discharges of these cells.

Keywords

Oxidative metabolismMitochondrial enzymeVisual pathwayON-centerOFF-center
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 3 , March 1990 , pp. 269 - 287
Copyright
Copyright © Cambridge University Press 1990

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. & Levick, W.R. (1969). Changes in maintained discharge with adaptation level in the cat retina. Journal of Physiology (London) 202, 699–718CrossRefGoogle ScholarPubMed
Burke, W. & Sefton, A.J. (1966). Inhibitory mechanisms in lateral geniculate nucleus of rats. Journal of Physiology (London) 187, 231–246.CrossRefGoogle Scholar
Carroll, E.W. & Wong-Riley, M.T.T. (1984). Quantitative light- and electron-microscopic analysis of cytochrome oxidase-rich zones in the striate cortex of the squirrel monkey. Journal of Comparative Neurology 222, 1–17.CrossRefGoogle ScholarPubMed
Connolly, M. & Van Essen, D.C. (1984). The representation of the visual field in parvicellular and magnocellular layers of the lateral geniculate nucleus in the macaque monkey. Journal of Comparative Neurology 226, 544–564.CrossRefGoogle ScholarPubMed
Connolly, M., Le, Vay S., & Van, Essen D.C., (1982). The complete pattern of ocular dominance stripes in macaque striate cortex. Society for Neuroscience Abstracts 8, 676.Google Scholar
Creutzfeldt, O.D., Lee, B.B & Elepfandt, A. (1979). A quantitative study of chromatic organization and receptive fields of cells of the lateral geniculate body of the rhesus monkey. Experimental Brain Research 35, 527–545.CrossRefGoogle ScholarPubMed
Derrington, A.M. & Lennie, P. (1984). The influence of temporal frequency and adaption level of receptive-field organization of retinal ganglion cell in cat. Journal of Physiology (London) 333, 343–366.CrossRefGoogle Scholar
Difiglia, M., Graveland, G.A. & Schiff, L., (1987). Cytochrome oxidase activity in the rat caudate nucleus: light- and electron- microscopic observations. Journal of Comparative Neurology 255, 137–145.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 (London) 258, 433–452.CrossRefGoogle ScholarPubMed
Friedlander, M.J., Lin, C.-S., Stanford, L.R. & Sherman, S.M. (1981). Morphology of functionally identified neurons in the lateral geniculate nucleus of the cat. Journal of Neurophysiology 46, 80–129.CrossRefGoogle ScholarPubMed
Friedlander, M.J., Lin, C.-S. & Sherman, S.M., (1979). Structure of physiologically identified X and Y cells in the cat&s lateral geniculate nucleus. Science 204, 1114–1117.CrossRefGoogle ScholarPubMed
Frishman, L.J. & Levine, M.W., (1983). Statistics of the maintained discharge of cat retinal ganglion cells. Journal of Physiology (London) 339, 475–494.CrossRefGoogle ScholarPubMed
Garey, L.J. & Saini, K.D., (1981). Golgi studies of the normal development of neurons in the lateral geniculate nucleus of the monkey. Experimental Brain Research 44, 117–128.CrossRefGoogle ScholarPubMed
Hamori, J., Pasik, T., Pasik, P. & Szentagothai, (1974). Triadic synaptic arrangements and their possible significance in the lateral geniculate nucleus of the monkey. Brain Research 80, 379–393.CrossRefGoogle 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
Hamori, J., Pasik, P. & Pasik, T., (1983). Differential frequency of P cells and I cells in magnocellular and parvicellular laminae of monkey lateral geniculate nucleus. An ultrastructural study. Experimental Brain Research 52, 57–66.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
Hubel, D.H. & Wiesel, T.N. (1972). Laminar and columnar distribution of geniculocortical fibers in the macaque monkey. Journal of Comparative Neurology 146, 421–450.CrossRefGoogle ScholarPubMed
Kageyama, G.H. & Wong-Riley, M.T.T. (1982). Histochemical localization of cytochrome oxidase in the hippocampus: correlation with specific neuronal types and afferent pathways. Neuroscience 7, 2337–2361.CrossRefGoogle ScholarPubMed
Kageyama, G.H. & Wong-Riley, M.T.T. (1984). The histochemical localization 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, 2445–2459.CrossRefGoogle Scholar
Kageyama, G.H. & Wong-Riley, M. (1985). An analysis of the cellular localization of cytochrome oxidase in the lateral geniculate nucleus of the adult cat. Journal of Comparative Neurology 242, 338–357.CrossRefGoogle ScholarPubMed
Kaplan, E. & Shapley, R.M. (1982). X and Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology 330, 125–143.CrossRefGoogle ScholarPubMed
Kennedy, H., Bullier, J. & Dehay, C.. (1985). Cytochrome-oxidase activity in the striate cortex and lateral geniculate nucleus of the new born and adult macaque monkey. Experimental Brain Research 61, 204–209.CrossRefGoogle Scholar
Knapp, A.G. & Schiller, P.H. (1984). The contribution of ON-bipolar cells to the electroretinogram of rabbits and monkeys. Vision Research 24, 1841–1846.CrossRefGoogle Scholar
Le, Gros Clark W.E. (1941). The laminar organization and cell content of the lateral geniculate body in the monkey. Journal of Anatomy 75, 419–433.Google Scholar
Lehninger, A.L. (1975). The Molecular Basis of Cell Structure and Function. New York: Worth.Google Scholar
LeVay, S., Connolly, M., Houde, J. & Van, Essen D.C. (1985). The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey. Journal of Neuroscience 5, 486–501.CrossRefGoogle ScholarPubMed
Liu, S. & Wong-Riley, M. (1986). An electron-microscopic analysis of the localization of cytochrome oxidase in the lateral geniculate nucleus of macaque monkeys. Society for Neuroscience Abstracts 12, 1039.Google Scholar
Lo, F.-S. & Sherman, S.M. (1988). The retinal EPSP is voltage dependent in geniculate Y (but not X) cells of cats. Society for Neuroscience Abstracts 14, 39.Google Scholar
Lowry, O.H. (1975). Energy metabolism in brain and its control. In Brain Work-Alfred Benzon Symposium, Vol. VIII, ed. Ingvar, D.H. & Lassen, N.A., pp.48–64. New York: Academic Press.Google Scholar
Lund, J.S., Lund, R.D., Hendrickson, A.E., Bunt, A.H. & Fuchs, A.F. (1975). The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 164, 287–304.CrossRefGoogle ScholarPubMed
Michael, C.H. (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. & Zempel, J. (1986). The proportion and size of GABA-immunoreactive neurons in the magnocellular and parvicellular layers of the lateral geniculate nucleus of the rhesus monkey. Experimental Brain Research 62, 215–223.CrossRefGoogle Scholar
Pasik, P., Pasik, T., Hamori, J. & Szentagothai, J. (1973). Golgi type II interneurons in the neuronal circuit of the monkey lateral geniculate nucleus. Experimental Brain Research 17, 18–34.CrossRefGoogle ScholarPubMed
Polyak, S. (1957). The Vertebrate Visual System. Illinois: The University of Chicago Press.Google Scholar
Purpura, K., Kaplan, E. & Shapley, R.M. (1986). The effect of mean luminance on the contrast gain of P and M cells in the macaque retina. Society for Neuroscience Abstracts 12, 7.Google Scholar
Purpura, K., Kaplan, E. & Shapley, R.M. (1989). Fluctuations in spontaneous discharge and visual responses in M and P pathways of the macaque monkey. Investigative Ophthalmology and Visual Science (Suppl.) 3, 38.Google Scholar
Saini, K.D. & Garey, L.J. (1981). Morphology of neurons in the lateral geniculate nucleus of the monkey. Experimental Brain Research 42, 235–248.Google ScholarPubMed
Schiller, P.H. (1982). Central connections of the retinal ON and OFF pathways. Nature 297, 580–583.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Malpeli, J.G. (1978). Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. Journal of Neurophysiology 41, 788–797.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Sandell, J.H. (1986). Functions of ON and OFF channels of the visual system. Nature 322, 824–825.CrossRefGoogle Scholar
Shapley, R.M. & Kaplan, E. (1986). What are the P and M cells of the monkey visual system sensitive to? Society for Neuroscience Abstracts 12, 7.Google Scholar
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. Nature (London) 292, 543–545.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neuroscience 9, 229–232.CrossRefGoogle Scholar
Sherman, S.M., Wilson, J.R., Kaas, J.H. & Webb, S.V. (1976). X and Y cells in the dorsal lateral geniculate nucleus of the owl monkey (Aotus trivirgatus). Science 192, 475–477.CrossRefGoogle ScholarPubMed
Sherman, S.M., Schumer, R.A. & Movshon, J.A. (1984). Functional cell classes in the macaque's LGN. Society for Neuroscience Abstracts 10, 297.Google Scholar
Singer, W., Poppel, E. & Creutzfeldt, O. (1972). Inhibitory interaction in the cat's lateral geniculate nucleus. Experimental Brain Research 14, 210–226.CrossRefGoogle ScholarPubMed
Skou, J.C. (1957). The influence of some cations on an adenosine triphosphate from peripheral nerve. Biochimica et Biophysica Acta. 23, 394–401.CrossRefGoogle Scholar
Tootell, R.B.H., Hamilton, S.L. & Silverman, M.S. (1985). Topography of cytochrome-oxidase activity in owl monkey cortex. Journal of Neuroscience 5, 2786–2800.CrossRefGoogle ScholarPubMed
Wiener, S.I., Johnson, J.I. & Ostapoff, E.M. (1987). Demarcations of the mechanosensory projection zones in the racoon thalamus, shown by cytochrome oxidase, actylcholinesterase, and Nissl stains. Journal of Comparative Neurology 258, 509–526.CrossRefGoogle Scholar
Wiesel, T. & 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. & 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
Wong-Riley, M.T.T. (1972). Neuronal and synaptic organization of the normal dorsal lateral geniculate nucleus of the squirrel monkey (Saimiri sciureus). Journal of Comparative Neurology 144, 25–59.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. (1976). Endogenous peroxidatic activity in brain stem neurons as demonstrated by their staining with diaminobenzidine in normal squirrel monkeys. Brain Research 108, 257–277.CrossRefGoogle ScholarPubMed
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome-oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. & Carroll, E.W. (1984 a). Quantitative light- and electron-microscopic analysis of cytochrome oxidase-rich zones in VII prestriate cortex of the squirrel monkey. Journal of Comparative Neurology 222, 18–37.CrossRefGoogle Scholar
Wong-Riley, M. & Carroll, E.W. (1984 b). The effect of impulse blockage on cytochrome-oxidase activity in monkey visual system. Nature 307, 262–264.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. & Kageyama, G.H. (1986). Localization of cytochrome oxidase in the mammalian spinal cord and dorsal root ganglia, with quantitative analysis of ventral horn cells in monkeys. Journal of Comparative Neurology 245, 41–61.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T., Merzenich, M.M. & Leake, P.A. (1978). Changes in endogenous enzymatic reactivity to DAB induced by neuronal inactivity. Brain Research 141, 185–192.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T., Walsh, S.M., Leake-Jones, P.A. & Merzenich, M.M. (1981). Maintenance of neuronal activity by electrical stimulation of unilaterally deafened cats demonstrable with the cytochnome-oxidase technique. Annals of Otology, Rhinology, and Laryngology (Suppl. 82), 90, 30–32.CrossRefGoogle ScholarPubMed