Summary
GABA-immunoreactive neuronal elements were detected in the stratum griseum superficiale or superficial gray layer of the rat superior colliculus in an electron microscopic study, using postembedding immunocytochemistry with protein A-gold as a marker. In addition to neuronal somata, two types of GABA-immunoreactive neuronal processes were observed. Numerous profiles of axon terminals (1 μm in diameter) with clear round or pleomorphic synaptic vesicles and mitochondria were found to establish mostly symmetrical synaptic contacts with GABA-immunonegative dendrites of various diameters. Some axosomatic synapses could also be observed. The gold particle density in this axon terminal compartment was between seven and 13 times the background level. The stratum griseum superficiale also included GABA-immunoreactive dendrites, some of which contained clear synaptic vesicles. These dendritic profiles always formed the presynaptic component of dendrodendritic synaptic contacts. The density of the gold particles in the dendritic compartment, taken as a whole, was between three and 13 times the background level. Furthermore, the relationship between the GABA-immunoreactive neuronal elements and degenerating retinal nerve endings identified in the left stratum griseum superficiale following enucleation of the right eye was investigated after a 7-day survival period. The profiles of degenerating retinal nerve endings (0.7 μm in diameter) were found to be devoid of any specific labelling. Most of the retinal boutons established axodendritic synapses of the asymmetrical type with an immunonegative dendrite, which was also contacted in some cases by a GABA-immunopositive axon terminal. Other retinal endings were presynaptic to GABA-immunopositive dendritic profiles with synaptic vesicles, some of which were found to contact in turn an unlabelled dendrite, thereby completing serial synaptic relationships. More rarely, retinal endings formed the presynaptic component of possible axoaxonic synapses with GABA-positive terminals presumed to be axonic in nature. It can be concluded that the retinal input to the superficial gray layer often converges with a GABAergic axonal input on a dendritic target, the neurotransmitter specificity of which is unknown. In other cases, retinal terminals synaptically contact GABA-immunolabelled conventional and presynaptic dendrites and probably also some axon terminals; this might provide an anatomical substrate for the control of GABA release from these GABAergic processes. These results indicate that transmitter GABA plays an important role in retinocollicular transmission.
Similar content being viewed by others
References
Albers, F. J., Meek, J. &Hafmans, T. G. M. (1990) Synaptic morphometry and synapse-to-neuron ratios in the superior colliculus of albino rats.Journal of Comparative Neurology 291, 220–30.
André, D., Vuillon-Cacciutolo, G. &Bosler, O. (1987) GABA nerve endings in the rat red nucleus: combined detection with serotonin terminals using dual immunocytochemistry.Neuroscience 23, 1095–102.
Angaut, P. &Sotelo, C. (1987) The dentato-olivary projection in the rat as a presumptive GABAergic link in the olivo-cerebello-olivary loop. An ultrastructural study.Neuroscience Letters 83, 227–31.
Angaut, P. &Sotelo, C. (1989) Synaptology of the cerebello-olivary pathway. Double labelling with anterograde axonal tracing and GABA immunocytochemistry in the rat.Brain Research 479, 361–5.
Arakawa, T. &Okada, Y. (1988) Excitatory and inhibitory action of GABA on synaptic transmission in slices of guinea pig superior colliculus.European Journal of Pharmacology 158, 217–24.
Biasi, S. de, Frassoni, C. &Spreafico, R. (1986) GABA immunoreactivity in the thalamic reticular nucleus of the rat. A light and electron microscopical study.Brain Research 399, 143–7.
Bosler, O. (1989) Ultrastructural relationships of serotonin and GABA terminals in the rat suprachiasmatic nucleus. Evidence for a close interconnection between the two afferent systems.Journal of Neurocytology 18, 105–13.
Behan, M. (1981) Identification and distribution of retinocollicular terminals in the cat: an electron microscopic autoradiographic analysis.Journal of Comparative Neurology 199, 1–15.
Bowery, N. G., Hudson, A. L. &Price, G. W. (1987) GABAA and GABAB receptor site distribution in the rat central nervous system.Neuroscience 20, 365–83.
Bowery, N. G., Price, G. W., Hudson, A. L., Hill, D. R., Wilkin, G. P. &Trunbull, M. J. (1984) GABA receptor multiplicity. Visualization of different receptor types in the mammalian CNS.Neuropharmacology 23, 219–31.
Caruso, D. M., Owczarzak, M. T., Goebel, D. J., Hazlett, J. C. &Pourcho, R. G. (1989) GABA-immunoreactivity in ganglion cells of the retina.Brain Research 476, 129–34.
Chalupa, L. M. (1984) Visual physiology of the mammalian superior colliculus. InComparative Neurology of the Optic Tectum, Ch. 19 (edited byVanegas, H.) pp. 775–818. New York: Plenum Press.
Chazal, G. &Ohara, P. T. (1986) Vesicle-containing dendrites in the nucleus raphe dorsalis of the cat. A serial section electron microscopic analysis.Journal of Neurocytology 15, 777–87.
Chazal, G. &Ohara, P. T. (1987) Synaptic organization of the nucleus raphe dorsalis of the cat.Journal of Neurocytology 16, 667–79.
Cuenod, M. &Streit, P. (1979) Amino-acid transmitters and local circuitry in optic tectum. InThe Neurosciences: Fourth Study Program (edited bySchmitt, F. O. &Worden, F. G.) pp. 989–1004. Cambridge, MA & London: MIT Press.
Decavel, C., Dubourg, P., Leon-Henri, B., Geffard, M. &Calas, A. (1989) Simultaneous immunogold labeling of GABAergic terminals and vasopressin-containing neurons in the rat paraventricular nucleus.Cell and Tissue Research 255, 77–80.
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.
Fonnum, F., Lund Karlsen, R., Malthe-Sorenssen, D., Skrede, K. K. &Walaas, I. (1979) Localization of neurotransmitters, particularly glutamate, in hippocampus, septum, nucleus accumbens and superior colliculus.Progress in Brain Research 51, 167–91.
Fox, G. Q. (1988) A morphometric analysis of synaptic vesicle distributions.Brain Research 475, 103–17.
Geffard, M., Henrich-Rock, A. M., Dulluc, J. &Seguela, P. (1985) Antisera against small neurotransmitter-like molecules.Neurochemistry International 7, 403–13.
Grofova, I., Ottersen, O. P. &Rinvik, E. (1978) Mesencephalic and diencephalic afferents to the superior colliculus and periaqueductal gray substance demonstrated by retrograde axonal transport of horseradish peroxidase in cat.Brain Research 146, 205–20.
Hamori, J. &Takacs, J. (1989) Two types of GABA-containing axon terminals in cerebellar glomeruli of cat: an immunogold-em study.Experimental Brain Research 74, 471–9.
Hayhow, W. R., Sefton, A. &Webb, C. (1962) Primary optic centers of the rat in relation to the terminal distribution of the crossed and uncrossed optic nerve fibers.Journal of Comparative Neurology 118, 295–321.
Henderson, Z. (1987) Cholinergic innervation of ferret visual system.Neuroscience 20, 503–18.
Henderson, Z. (1989) The cholinergic input to the superficial layers of the superior colliculus: an ultrastructural immunocytochemical study in the ferret.Brain Research 476, 149–53.
Hofbauer, A. &Holländer, H. (1986) Synaptic connections of cortical and retinal terminals in the superior colliculus of the rabbit: an electron double labelling study.Experimental Brain Research 65, 145–55.
Houser, C. R., Lee, M. &Vaughn, J. E. (1983) Immunocyto-chemical localization of glutamic acid decarboxylase in normal and deafferented superior colliculus. Evidence for reorganization of γ-aminobutyric acid synapses.Journal of Neuroscience 3, 2030–40.
Huerta, M. F. &Harting, J. K. (1984a) Connectional organization of the superior colliculus.Trends in Neurosciences 7, 286–9.
Huerta, M. F. &Harting, J. K. (1984b) The mammalian superior colliculus: studies of its morphology and connections. InComparative Neurology of the Optic Tectum (edited byVanegas, H.) pp. 687–773. New York and London: Plenum Press.
Kayama, Y., Fukuda, Y. &Iwama, K. (1980) GABA sensitivity of neurons of the visual layer in the rat superior colliculus.Brain Research 192, 121–31.
Levitt, P. &Moore, R. Y. (1979) Origin and organization of brainstem catecholamine innervation in the rat.Journal of Comparative Neurology 186, 505–28.
Lieberman, A. R. &Webster, K. E. (1974) Aspects of the synaptic organization of intrinsic neurons in the dorsal lateral geniculate nucleus. An ultrastructural study of the normal and of the experimentally deafferrented nucleus in the rat.Journal of Neurocytology 3, 677–710.
Lund, R. D. (1964) Terminal distribution in the superior colliculus of fibers originating in the visual cortex.Nature 204, 1283–5.
Lund, R. D. (1969) Synaptic patterns of the superficial layers of the superior colliculus of the rat.Journal of Comparative Neurology 135, 179–208.
Lund, R. D. &Lund, J. S. (1971a) Modifications of synaptic patterns in the superior colliculus of the rat during development and following deafferentation.Vision Research 11, 281–98.
Lund, R. D. &Lund, J. S. (1971b) Synaptic adjustment after deafferentation of the superior colliculus of the rat.Science 171, 804–7.
Mize, R. R. (1983) Variations in the retinal synapses of the cat superior colliculus revealed using quantitative electron microscope autoradiography.Brain Research 269, 211–21.
Mize, R. R. (1988) Immunocytochemical localization of γ-aminobutyric acid (GABA) in the cat superior colliculus.Journal of Comparative Neurology 276, 169–87.
Mize, R. R. &Horner, L. H. (1989) Origin, distribution, and morphology of serotoninergic afferents to the cat superior colliculus: a light and electron immunocytochemistry study.Experimental Brain Research 75, 83–98.
Mize, R. R., Spencer, R. F. &Sterling, P. (1981) Neurons and glia in the cat superior colliculus accumulate [3H]γ-aminobutyric acid (GABA).Journal of Comparative Neurology 202, 385–96.
Mize, R. R., Spencer, R. F. &Sterling, P. (1982) Two types of GABA accumulating neurons in the superficial gray layer of the cat superior colliculus.Journal of Comparative Neurology 206, 180–92.
Mooney, R. D., Bradley, G. K., Jacquin, M. F. &Rhoades, R. W. (1984) Dendrites of deep layer, somatosensory superior collicular neurons extend into the superficial laminae.Brain Research 324, 361–5.
Mooney, R. D., Bradley, G. K. &Rhoades, R. W. (1985) Correlations between the structural and functional characteristics of neurons in the superficial laminae and the hamster's superior colliculus.Journal of Neuroscience 5, 2989–3009.
Mooney, R. D., Nikoletseas, M. M., Hess, P. R., Allen, Z., Lewin, A. C. &Rhoades, R. W. (1988) The projection from the superficial to the deep layers of the superior colliculus: an intracellular horseradish peroxidase injection study in the hamster.Journal of Neuroscience 8, 1384–99.
Mufson, E. J., Martin, T. L., Mash, D. C., Wainer, B. H. &Mesulam, M-M. (1986) Cholinergic projection from the parabigeminal nucleus (Ch8) to the superior colliculus in mouse: a combined analysis of horseradish peroxidase transport and choline acetyltransferase immunohistochemistry.Brain Research 370, 144–8.
Nistri, A. &Sivilotti, L. (1985) An unusual effect of γ-aminobutyric acid on synaptic transmission on frog tectal neuronesin vitro.British Journal of Pharmacology 85, 917–21.
Ohara, P. T., Lieberman, A. R., Hunt, S. P. &Wu, J-Y. (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.
Okada, Y. (1974) Distribution of γ-aminobutyric acid (GABA) in the layers of the superior colliculus of the rabbit.Brain Research 75, 362–5.
Okada, Y. (1976) Distribution of GABA and GAD activity in the layers of the superior colliculus of the rabbit. InGABA in Nervous System Fuction (edited byRoberts, E., Chase, T. N. &Tower, D. B.) pp. 229–33. New York: Raven Press.
Ottersen, O. P. &Storm-Mathisen, J. (1984) Neurons containing or accumulating transmitter aminoacids. InHandbook of Chemical Neuroanatomy, Vol. 3 (edited byBjörklund, A., Hökfelt, T. &Kuhar, M. J.) pp. 141–246. Amsterdam: Elsevier.
Palacios, J. M., Wamsley, J. K. &Kuhar, M. J. (1981) High affinity GABA receptors. Autoradiographic localization.Brain Research 222, 285–307.
Parent, A., Descarries, L. &Beaudet, A. (1981) Organization of ascending serotonin system in the adult rat brain. A radioautographic study after intraventricular administration of [3H]5-hydroxytryptamine.Neuroscience 6, 115–38.
Perez de la Mora, M., Possani, L. D., Tapia, R., Teran, L., Palacios, R., Fuxe, K., Hökfelt, T. &Ljungdahl, A. (1981) Demonstration of central γ-aminobutyrate nerve terminals by means of antibodies against glutamate decarboxylase.Neuroscience 6, 875–95.
Pinard, R., Segu, L., Cau, P. &Lanoir, J. (1988) Distribution of benzodiazepine receptors in the rat superior colliculus: a light and electron microscope quantitative autoradiographic study.Brain Research 474, 48–65.
Richards, J. G., Schoch, P., Häring, P., Takacs, B. &Möhler, H. (1987) Resolving GABAA/benzodiazepine receptors: cellular and subcellular localization in the CNS with monoclonal antibodies.Journal of Neuroscience 7, 1866–86.
Seguela, P., Geffard, M., Buijs, R. M. &Le Moal, M. (1984) Antibodies against γ-aminobutyric acid: specificity studies and immunocytochemical results.Proceedings of the National Academy of Sciences (USA) 81, 3888–92.
Seitanidou, T., Triller, A. &Korn, H. (1988) Distribution of glycine receptors on the membrane of a central neuron: an immunoelectron microscopy study.Journal of Neuroscience 8, 4319–33.
Sequier, J. M., Richards, J. G., Malherbe, P., Price, G. W., Mathews, S. &Möhler, H. (1988) Mapping of brain areas containing RNA homologous to cDNAs encoding the α and β subunits of the rat GABAA γ-aminobutyrate receptor.Proceedings of the National Academy of Sciences (USA) 85, 7815–19.
Soghomonian, J. J., Pinard, R. &Lanoir, J. (1989) GABA innervation in adult rat oculomotor nucleus: a radioautographic and immunocytochemical study.Journal of Neurocytology 18, 319–31.
Sterling, P. (1971) Receptive fields and synaptic organization of the superficial gray layer of the cat superior colliculus.Vision Research 11, 309–28.
Sterling, P. (1973) Quantitative mapping with the electron microscope: retinal terminals in the superior colliculus.Brain Research 54, 347–54.
Straschill, M. &Perwein, J. (1971) Effect of iontophoretically applied biogenic amines and of cholinomimetic substances upon the activity of neurons in the superior colliculus and mesencephalic reticular formation of the cat.Pflügers Archives 324, 43–55.
Tappaz, M. L., Wassef, M., Oertel, W. H., Paut, L. &Pujol, J. F. (1983) Light and electron microscopic immunocytochemistry of glutamic acid decarboxylase (GAD) in the basal hypothalamus: morphological evidence for neuroendocrine γ-aminobutyrate (GABA).Neuroscience 9, 271–87.
Theodosis, D. T., Paut, L. &Tappaz, M. L. (1986) Immunocytochemical analysis of the GABAergic innervation of oxytocin- and vasopressin-secreting neurons in the rat supraoptic nucleus.Neuroscience 19, 207–22.
Tigges, M. &Tigges, J. (1975) Presynaptic dendrite cells and two other classes of neurons in the superficial layers of the superior colliculus of the chimpanzee.Cell and Tissue Research 162, 279–95.
Triller, A., Cluzeaud, F. &Korn, H. (1987) Gammaaminobutyric acid-containing terminals can be apposed to glycine receptors at central synapses.Journal of Cell Biology 104, 947–56.
Valdivia, O. (1971) Methods of fixation and the morphology of synaptic vesicles.Journal of Comparative Neurology 142, 257–74.
Vanegas, H. (1984)Comparative Neurology of the Optic Tectum. New York & London: Plenum Press.
Villar, M. J., Vitale, M. L., Hökfelt, T. &Verhofstad, A. A. J. (1988) Dorsal raphe serotoninergic branching neurons projecting both to the lateral geniculate body and superior colliculus: a combined retrograde tracingimmunohistochemical study in the rat.Journal of Comparative Neurology 277, 126–40.
Zhu, C. G., Sandri, C. &Akert, K. (1981) Morphological identification of axo-axonic and dendro-dendritic synapses in the rat substantia gelatinosa.Brain Research 230, 25–40.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Pinard, R., Benfares, J. & Lanoir, J. Electron microscopic study of GABA-immunoreactive neuronal processes in the superficial gray layer of the rat superior colliculus: their relationships with degenerating retinal nerve endings. J Neurocytol 20, 262–276 (1991). https://doi.org/10.1007/BF01235544
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01235544