Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-23T06:05:31.407Z Has data issue: false hasContentIssue false
  • English
  • Français

Serotonergic axons in the monkey's lateral geniculate nucleus

Published online by Cambridge University Press:  02 June 2009

James R. Wilson  and
Anita E. Hendrickson
James R. Wilson
Affiliation:
Yerkes Regional Primate Research Center and Department of Anatomy and Cell Biology, Emory University, Atlanta
Anita E. Hendrickson
Affiliation:
Departments of Biological Structure and Ophthalmology, University of Washington, Seattle
Get access Rights & Permissions [Opens in a new window]

Abstract

Axons containing serotonin (5-hydroxytryptamine, 5-HT) in the lateral geniculate nucleus of Macaca monkeys were stained using light or electron microscopic (EM) immunocytochemical labeling techniques. 5-HT labeled axons were sparsely and homogeneously distributed throughout the entire nucleus. Small varicosities were located irregularly along each axon giving them a beaded appearance. Examination of these axons at the EM level revealed that the varicosities contained synaptic vesicles that were variable in size and shape. Nearly all of the varicosities lacked synaptic contacts; only two out of over two hundred labeled varicosities appeared to form a synaptic contact, and serial sections through ten varicosities showed no discernible pre- or postsynaptic membrane specializations. 5-HT labeled axon varicosities were not observed to be preferentially located in proximity to any specific neuronal structures at either the light or EM level. 5-HT varicosities were estimated to form about 1% of the profiles containing synaptic vesicles in the neuropil of the lateral geniculate nucleus.

We conclude that axons containing serotonin in the lateral geniculate nucleus release this neurotransmitter to act in a neuromodulatory manner throughout the neuropil, probably to set a general level of neuronal excitability.

Keywords

SerotoninLateral geniculate nucleusPrimateElectron microscopy
Type
Research Articles
Information
Visual Neuroscience , Volume 1 , Issue 1 , January 1988 , pp. 125 - 133
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

Aghajanian, G.K. & McCall, R.B. (1980). Serotonergic synaptic input to facial motoneurons: localization by electron microscopy autoradiography. Neuroscience 5, 2155–2162.CrossRefGoogle Scholar
Ajika, K. & Ochi, J. (1978). Serotonergic projections to the suprachiasmatic nucleus and the median eminence of the rat: identification by fluorescence and electron microscope. Journal of Anatomy 127, 563–576.Google Scholar
Beaudet, A. & Descarries, L. (1976). Quantitative data on serotonin nerve terminals in adult rat neocortex. Brain Research 111, 301–309.CrossRefGoogle ScholarPubMed
Beaudet, A. & Descarries, L. (1978). The monoamine innervation of rat cerebral cortex: synaptic and nonsynaptic axon terminals. Neuroscience 3, 851–860.CrossRefGoogle ScholarPubMed
Beaudet, A. & Descarries, L. (1981). The fine structure of central serotonin neurons. Journal of Physiology (Paris) 77, 193–203.Google ScholarPubMed
Calas, A., Besson, M.J., Gaughy, C, Alonso, G., Glowinski, J. & Cheramy, A. (1976). Radioautographic study of in vivo incorporation of 3H-monoamines in the cat caudate nucleus: identification of serotoninergic fibers. Brain Research 118, 1–13.CrossRefGoogle ScholarPubMed
Campos-Ortega, J.A., Glees, P. & Neuhoff, V. (1968). Ultrastructural analysis of individual layers in the lateral geniculate body of the monkey. Zeitschrift fur Zellforschung 87, 82–100.CrossRefGoogle ScholarPubMed
Chan-Palay, V. (1975). Fine structure of labeled axon in the cerebellar cortex and nuclei of rodents and primates after intraventricular infusions with tritiated serotonin. Anatomy and Embryology 148, 235–265.CrossRefGoogle ScholarPubMed
Chan-Palay, V. (1978). The paratrigeminal nucleus. III. Identification and interrelations of catecholamine axons, indoleamine axons, and substance P immunoreactive cells in the neuropil. Journal of Neurocytology 7, 419–422.CrossRefGoogle Scholar
Cropper, E.C., Eisenman, J.S. & Azmitia, E.C. (1984). An immunocytochemical study of the serotonergic innervation of the thalamus of the rat. Journal of Comparative Neurology 224, 38–50.CrossRefGoogle ScholarPubMed
Curtis, D.R. & Davis, R. (1962). Pharmacological studies upon neurones of the lateral geniculate nucleus of the cat. British Journal of Pharmacology 18, 217–246.Google ScholarPubMed
DeHoff, R.T. & Rhines, F.N. (1961). Determination of the number of particles per unit volume from measurements on random plane sections: the general cylinder and the ellipsoid. Transactions of Aime 221, 975–982.Google Scholar
De Lima, A.D. & Singer, W. (1987). The serotonergic fibers in the dorsal lateral geniculate nucleus of the cat: distribution and synaptic connections demonstrated with immunocytochemistry. Journal of Comparative Neurology 258, 339–351.CrossRefGoogle Scholar
Descarries, L., Beaudet, A. & Watkins, K.C. (1975). Serotonin nerve terminals in adult rat neocortex. Brain Research 100, 563–568.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1967). Pattern 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. & Colonnier, M. (1970). Synaptic patterns in the dorsal lateral geniculate nucleus of the monkey. Zeitschrift fur Zellforschung 103, 90–108.CrossRefGoogle ScholarPubMed
Hendrickson, A.E. (1972). Electron microscopic distribution of axoplasmic transport. Journal Comparative Neurology 144, 381–398.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Hunt, S.P. & Wu, J.-Y. (1981). Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex. Nature 292, 605–607.CrossRefGoogle ScholarPubMed
Jacobs, B.L., Heym, J. & Thrulson, M.E. (1981). Behavioral and physiological correlates of brain serotonergic unit activity. Journal of Physiology (Paris) 77, 431–436.Google Scholar
Jones, E.G. & Powell, T.P.S. (1969). Electron microscopy of synaptic glomeruli in the thalamic relay nuclei of the cat. Proceedings of the Royal Society (London) 172, 153–171.Google ScholarPubMed
Kupferman, I. (1979). Modulatory actions of neurotransmitters. Annual Review of Neuroscience 2, 447–465.CrossRefGoogle Scholar
Maley, B. & Elde, R. (1982). The ultrastructural localization of serotonin immunoreactivity within the nucleus of the solitary tract of the cat. Journal of Neuroscience 2, 1499–1506.CrossRefGoogle ScholarPubMed
Marks, G.A., Speciale, S.G., Cobbey, K. & Roffwary, H.P. (1987). Serotonergic inhibition of the dorsal lateral geniculate nucleus. Brain Research 418, 76–84.CrossRefGoogle ScholarPubMed
Mize, R.R., Faulkner, L.E. & Horner, L.H. (1984). Immunocytochemical localization of serotonergic fibers in the lateral geniculate complex of the cat. Neuroscience Abstracts 10, 298.Google Scholar
Molliver, M.E., Grzanna, R., Lidov, H.G.W., Morrison, J.H. & Oeschowska, J.A. (1982). Monoamine systems in the cerebral cortex. In Cytochemical Methods in Neuroanatomy, ed. Chan-Palay, V. & Palay, S.L., pp. 255–277. New York: A.R. Liss, Inc.Google Scholar
Morrison, J.H. & Foote, S.L. (1986). Noradrenergic and serotonergic innervation of cortical, thalamic, and tectal visual structures in Old and New World monkeys. Journal of Comparative Neurology 243, 117–138.CrossRefGoogle Scholar
Parnavelas, J.G., Moises, H.C. & Speciale, S.G. (1985). The monoaminergic innervation of the rat visual cortex. Proceedings of the Royal Society (London) 223, 319–329.Google ScholarPubMed
Pasik, P., Pasik, T., & Hamori, J. (1976). Synapses between interneurons in the lateral geniculate nucleus. Experimental Brain Research 17, 18–34.Google Scholar
Pasik, T., Pasik, P. & Holstein, G.R. (1983). Serotonin immunoreactivity in the monkey dorsal lateral geniculate nucleus. Neuroscience Abstracts 9, 1047.Google Scholar
Phillis, J.W., Tebecis, A.K. & York, D.H. (1967). The inhibitory action of monoamines on lateral geniculate neurones. Journal of Physiology (London) 190, 563–581.CrossRefGoogle ScholarPubMed
Pickel, V.M., Joh, T.J., Chan, J. & Beaudet, A. (1984). Serotonergic terminals: ultrastructure and synaptic interaction with catecholamine-containing neurons in the medial nuclei of the solitary tracts. Journal of Comparative Neurology 225, 291–301.CrossRefGoogle Scholar
Rapisardi, S. & Lipsenthal, L. (1983). Asymmetric and symmetric synaptic junctions in the dorsal lateral geniculate nucleus of cat and monkey. Journal of Comparative Neurology 224, 415–424.CrossRefGoogle Scholar
Rinaldi, P., Sutko, M., Mahnke, J.H. & Verzeano, M. (1975). Serotonin in the lateral geniculate. Physiological Behavior 14, 95–102.CrossRefGoogle ScholarPubMed
Rogawski, M.A. & Aghajanian, G.K. (1980). Norepinephrine and serotonin: opposite effects on the activity of lateral geniculate neurons evoked by optic pathway stimulation. Experimental Neurology 67, 678–694.CrossRefGoogle Scholar
Ruda, M.A., Coffield, J. & Steinbusch, H.W.M. (1982). Immunocytochemical analysis of serotonergic axons in laminae I and II of the lumbar spinal cord of the cat. Journal of Neuroscience 2, 1660–1671.CrossRefGoogle ScholarPubMed
Saavedra, J.P., Pasik, T. & Pasik, P. (1983). Immunocytochemistry of serotonergic neurons in the central nervous system of monkeys. In Neural Transmission, Learning and Memory, ed. Caputo, R. & Marson, C.A., pp. 81–96. New York: Raven Press.Google Scholar
Satinsky, D. (1967). Pharmacological responsiveness of lateral geniculate nucleus neurons. International Journal of Neuropharmacology 6, 387–397.CrossRefGoogle ScholarPubMed
Schaffar, N., Jean, A. & Calas, A. (1984). Radioautographic study of serotonergic axon terminals in the rat trigeminal motor nucleus. Neuroscience Letters 44, 31–36.CrossRefGoogle Scholar
Somogyi, P. & Takagi, H. (1982). A note on the use of picric acid, paraformaldehyde, and glutaraldehyde fixative for correlative light and EM immunohistochemistry. Neuroscience 7, 1779–1783.CrossRefGoogle Scholar
Steinbusch, H.W.M. (1981). Distribution of serotonin immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6, 557–618.CrossRefGoogle ScholarPubMed
Steinbusch, H.W.M., Verhofstad, A.A.J. & Joosten, H.W.J. (1983). Antibodies to serotonin for neuroimmunocytochemistry studies: methodological aspects and applications. In Immunohistochemistry, ed. Zuello, A.C., EBRO Handbook Series: Methods in the Neurosciences, Vol. 3, 3: pp. 193–214. New York: Wiley and Sons.Google Scholar
Takeuchi, Y. & Sano, Y. (1984). Serotonin nerve fibers in the primary visual cortex of the monkey. Anatomy and Embryology 169, 1–8.CrossRefGoogle ScholarPubMed
Tebecis, A.K. & Dimoria, A. (1972). A reevaluation of the mode of action of 5-hydroxytryptamine on lateral geniculate neurones: comparison with catecholamines and LSD. Experimental Brain Research 14, 480–493.CrossRefGoogle ScholarPubMed
Ueda, S. & Sano, Y. (1986). Distributional pattern of serotoninimmunoreactive fibers in the lateral geniculate nucleus of the rat, cat and monkey (Macaca fuscata). Cell and Tissue Research 243, 249–253.CrossRefGoogle Scholar
Wiklund, L., Descarries, L. & Molligard, K. (1981). Serotonergic axon terminals in the rat dorsal accessory olive: normal ultrastructure and light microscopic demonstration of regeneration after 5,6-dihydroxytryptamine lesioning. Journal of Neurocytology 10, 1009–1027.CrossRefGoogle Scholar
Wilson, J.R. (1986). Synaptic connections of relay and local circuit neurons in the monkey's dorsal lateral geniculate nucleus. Neuroscience Letters 66, 79–84.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
Winfield, D.A., Gatter, K.C. & Powell, T.P.S. (1975). Certain connections of the visual cortex of the monkey shown by the use of horseradish peroxidase. Brain Research 92, 456–461.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, 25–60.CrossRefGoogle ScholarPubMed
Woodward, D.J., Moiser, H.C., Waterhouse, B.D., Hoffer, B.J. & Freedman, R. (1979). Modulatory actions of norepinephrine in the central nervous system. Federation Proceedings 38, 2109–2116.Google ScholarPubMed
Yoshida, M., Masashi, S. & Takaori, S. (1984). Serotonin-mediated inhibition from dorsal raphe nucleus of neurons in dorsal lateral geniculate and thalamic reticular nuclei. Brain Research 290, 95–105.CrossRefGoogle ScholarPubMed