Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-26T00:41:32.815Z Has data issue: false hasContentIssue false
  • English
  • Français

Organization of neurons labeled by antibodies to gamma-aminobutyric acid (GABA) in the superior colliculus of the Rhesus monkey

Published online by Cambridge University Press:  02 June 2009

R. Ranney Mize ,
Chang-Jin Jeon ,
Omar L. Hamada  and
Robert F. Spencer
R. Ranney Mize
Affiliation:
Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee Health Science Center, Memphis
Chang-Jin Jeon
Affiliation:
Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee Health Science Center, Memphis
Omar L. Hamada
Affiliation:
Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee Health Science Center, Memphis
Robert F. Spencer
Affiliation:
Department of Anatomy, Medical College of Virginia, Richmond
Get access Rights & Permissions [Opens in a new window]

Abstract

The inhibitory neurotransmitter gamma-aminobutyric acid (GABA) is found in the superior colliculus (SC) of many mammalian species. In cat, several distinct classes of putative GABAergic neuron have been identified using antibodies directed against the neurotransmitter. It is not known whether these classes are found in other species. To study this, we examined the distribution, morphology, ultrastructure, and synaptic organization of GABA immunoreactive neurons in the SC of the Rhesus monkey (Macaca mulatta). Antibody-labeled neurons were distributed throughout the monkey SC, but were most densely concentrated within the zonal and superficial gray layers (32.5% of the total). These neurons were all small cells ranging from 6.6–16.3 μm in average diameter, and had granule, pyriform, and horizontal morphologies. Four types of labeled profile were identified in single ultrathin sections with the electron microscope. Presynaptic dendrites (PSDs) contained pleomorphic vesicles, received synaptic input from unlabeled axon terminals, and sometimes formed symmeytric synaptic contacts with postsynaptic profiles. Two subtypes were found. One type contained loose accumulations of synaptic vesicles throughout the profile and had a distinctive varicose shape. The other type contained small discrete clusters of synaptic vesicles near the site of synaptic apposition. The former were much more common. Profiles with typical axon terminal morphology were also found. These profiles usually contained numerous flattened vesicles and formed symmetric synapses with postsynaptic profiles, both dendrites and cell bodies. Some conventional dendrites and myelinated axons were also labeled. Serial ultrathin section reconstructions revealed that PSDs formed complex synaptic relationships with other elements. Retinal terminals, identified by their characteristic pale mitochondria, established synaptic contacts with both types of PSD. These PSDs also established contact with each other, providing a possible anatomical substrate for disinhibition. We conclude that the monkey SC has multiple GABAergic cell types, similar to those found in cat may represent an organization common to both mammals and some other vertebrate species. The circuitry established by these cell types may provide a mechanism for disinhibition as well as inhibition in the mammalian SC.

Keywords

UltrastructureInhibitionDisinhibitionAntibody immuocytochemistryPresynaptic dendritesNeural circuitryVisual system
Type
Research Article
Information
Visual Neuroscience , Volume 6 , Issue 1 , January 1991 , pp. 75 - 92
Copyright
Copyright © Cambridge University Press 1991

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

Andersen, P., Dingledine, R., Gjerstad, L., Langmoen, I.A. & Mosfeldt, Laursen A. (1980). Two different responses of hippocampal pyramidal cells to application of gamma-aminobutyric acid. Journal of Physiology 305, 279–296.CrossRefGoogle Scholar
Appell, P.P. & Behan, M. (1990). Sources of subcortical GABAergic projections to the superior colliculus in the cat. Journal of Comparative Neurology (in press).CrossRefGoogle Scholar
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, 217–224.CrossRefGoogle ScholarPubMed
Arakawa, T. & Okada, Y. (1989). The effect of GABA on neurotransmission in frog tectal slices. Neuroscience Research 6, 363–368.CrossRefGoogle ScholarPubMed
Araki, M., McGeer, P.L. & McGeer, E.G. (1984). Presumptive gamma-aminobutyric acid pathways from the midbrain to the superior colliculus studied by a combined horseradish peroxidase-gamma-aminobutyric acid transaminase pharmacohistochemical method. Neuroscience 13, 433–439.CrossRefGoogle Scholar
Behan, M. (1981). Identification and distribution of retinocollicular terminals in the cat: An electron-microscopic autoradiographic analysis. Journal of Comparative Neurology 199, 1–16.CrossRefGoogle Scholar
Behan, M., Lin, C.-S. & Hall, W.C. (1987). The nigrotectal projection in the cat: An electron microscope autoradiographic study. Neuroscience 21, 529–539.CrossRefGoogle Scholar
Beninato, M. & Spencer, R.F. (1987). A cholinergic projection to the rat superior colliculus demonstrated by retrograde transport of horseradish peroxidase and choline acetyltransferase immunohistochemistry. Journal of Comparative Neurology 253, 525–538.CrossRefGoogle Scholar
Berman, N. (1977). Connections of the pretectum in the cat. Journal of Comparative Neurology 174, 227–254.CrossRefGoogle ScholarPubMed
Bowery, N.G., Hudson, A.L. & Price, G.W. (1987). GABAa and GABAb receptor site distribution in the cat central nervous system. Neuroscience 20, 365–383.CrossRefGoogle Scholar
Brecha, N. (1983). Retinal neurotransmitters: Histochemical and bio-chemical studies. In Chemical Neuroanatomy, ed. Emson, P.C., pp. 85–129. New York: Raven Press.Google Scholar
Capowski, J.J. (1989). Semiautomatic entry of neuron trees from the microscope. In Computer Techniques in Neuroanatomy, ed. Capowski, J.J., pp. 87–107. New York: Plenum Press.CrossRefGoogle Scholar
Chevalier, G., Thierry, A.M., Shibazaki, T. & Feger, J. (1981). Evidence for GABAergic inhibitory nigrotectal pathway in the rat. Neuroscience Letters 21, 67–70.CrossRefGoogle ScholarPubMed
Cynader, M. & Berman, N. (1972). Receptive-field organization of monkey superior colliculus. Journal of Neurophysiology 35, 187–201.CrossRefGoogle ScholarPubMed
Edwards, S.B., Ginsburgh, C.L., Henkel, C.K. & Stein, B.E. (1979). Sources of subcortical projections to the superior colliculus in the cat. Journal of Comparative Neurology 184, 309–330.CrossRefGoogle Scholar
Famiglitti, 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 Scholar
Ficalora, A.S. & Mize, R.R. (1989). The neurons of the substantia nigra and zona incerta which project to the cat superior colliculus are GABA immunoreactive: A double-label study using GABA immunocytochemistry and lectin retrograde transport. Neuroscience 29, 567–581.CrossRefGoogle 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
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, 167–191.CrossRefGoogle ScholarPubMed
Fosse, V.M., Heggelund, P. & Fonnum, P. (1989). Postnatal development of glutamatergic, GABAergic, and cholinergic neurotransmitter phenotypes in the visual cortex, lateral geniculate nucleus, pulvinar, and superior colliculus in cats. Journal of Neuroscience 9, 426–435.CrossRefGoogle ScholarPubMed
Gehlert, D.R., Yamamura, H.I. & Wamsley, J.K. (1985). Gammaaminobutyric acidB receptors in the rat brain: Quantitative autoradiographic localization using [3H]-baclofen. Neuroscience Letters 56, 183–188.CrossRefGoogle ScholarPubMed
Graham, J.& Casagrande, V.A. (1980). A light-microscopic and electron-microscopic study of the superficial layers of the superior colliculus of the tree shrew (Tupaia glis). Journal of Comparative Neurology 191, 133–151.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1969). The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus ofthe cat. Zeitschrift für Zellforschung und Mikroskopische Anatomie 96, 1–38.CrossRefGoogle Scholar
Hall, W.C., Fitzpatrick, D., Klatt, L.L. & Raczkowski, D. (1989). Cholinergic innervation of the superior colliculus in the cat. Journal of Comparative Neurology 287, 495–514.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 neuron in lateral geniculate nucleus of the cat. Nature 317, 618–621.CrossRefGoogle ScholarPubMed
Harting, J.K., Huerta, M.F., Hashikawa, T., Weber, J.T. & Van Lieshout, D.P. (1988). Neuroanatomical studies of the nigrotectal projection in the cat. Journal of Comparative Neurology 278, 615–631.CrossRefGoogle ScholarPubMed
Hartman, M.G., Beitz, A.J., Madl, J.E. & Mize, R.R. (1988). Glutamate-like antibody staining in the cat superior colliculus is reduced by visual decortication. Investigative Ophthalmology and Visual Science (Suppl.) 29, 32.Google Scholar
Houser, C.R., Lee, M. & Vaughn, J.E. (1983). Immunocytochemical localization of glutamic acid decarboxylase in normal and deafferented superior colliculus: Evidence for reorganization of gammaaminobutyric acid synapses. Journal of Neuroscience 3, 2030–2042.CrossRefGoogle ScholarPubMed
Hunt, S.P. & Kunzle, H. (1976). Selective uptake and transport of label within three identified neuronal systems after injection of 3H-GABA into the pigeon optic tectum: An autoradiographic and Golgi study. Journal of Comparative Neurology 170, 173–190.CrossRefGoogle ScholarPubMed
Kanno, S. & Okáda, Y. (1988). Laminar distribution of GABA (gamma-aminobutyric acid) in the dorsal lateral geniculate nucleus, Area 17 and area 18 of the visual cortex, and the superior colliculus of the cat. Brain Research 451, 172–178.CrossRefGoogle ScholarPubMed
Kaufman, D.L., Houser, C.R. & Tobin, A.J. (1989). Two forms of glutamate decarboxylase (GAD), with different N-terminal sequences, have distinct intraneuronal distribution. Society for Neuroscience Abstracts 15, 487.Google Scholar
Kawai, N. & Yamamoto, C. (1967). Effects of gamma-aminobutyric acid on the potentials evoked in vitro in the superior colliculus. Experientia (Basel) 23, 822–823.CrossRefGoogle ScholarPubMed
Kawamura, S., Fukushima, N., Hattori, S. & Tashiro, T. (1978). A ventral lateral geniculate projection to the dorsal thalamus and the midbrain in the cat. Experimental Brain Research 31, 95–106.CrossRefGoogle Scholar
Kayama, Y., Fukuda, Y. & Iwama, K. (1980). GABA sensitivity of neurons of the visual layer in the rat superior colliculus. Brain Research 192, 121–131.CrossRefGoogle ScholarPubMed
Kvale, I. & Fonnum, F. (1983). The effects of unilateral neonatal removal of visual cortex on transmitter parameters in the adult superior colliculus and lateral geniculate body. Developmental Brain Research 11, 261–266.CrossRefGoogle Scholar
Laemle, L.K. (1981). A Golgy study of cellular morphology in the superficial layers of superior colliculus of man, Saimiri, and Macaca. Journal für Hirnforschung 22, 243–253.Google ScholarPubMed
Langer, T.P. (1976). Cellular and fiber patterns in the superior colliculus of the cat. Ph.D. Dissertation, University of Washington, Seattle, WA.Google Scholar
Lu, S.M., Lin, C.-S., Behan, M., Cant, N.B. & Hall, W.C. (1985). Glutamate decarboxylase immunoreactivity in the intermediate gray layer of the superior colliculus in the cat. Neuroscience 16, 123–131.CrossRefGoogle ScholarPubMed
Lund, R.D. (1972). Synaptic patterns in the superficial layers of the superior colliculus of the monkey, (Macaca mulatta). Experimental Brain Research 15, 194–211.CrossRefGoogle ScholarPubMed
Lund, R.D. (1969). Synaptic patterns of the superficial layers of the superior colliculus of the rat. Journal of Comparative Neurology 135, 179–208.CrossRefGoogle ScholarPubMed
Ma, T.P., Cheng, H.-W., Czech, J.A. & Rafols, J.A. (1990). Intermediate and deep layers of the macaque superior colliculus: A golgi study. Journal of Comparative Neurology 295, 92–110.CrossRefGoogle ScholarPubMed
Marrocco, R.T. & Li, R.H. (1977). Monkey superior colliculus: Properties of single cells and their afferent inputs. Journal of Neurophysiology 40, 844–860.CrossRefGoogle ScholarPubMed
Mize, R.R. (1983). Variations in the retinal synapses of the cat superior colliculus revealed using quantitative electron microscope auto-radiography. Brain Research 269, 211–221.CrossRefGoogle Scholar
Mize, R.R. (1988). Immunocytochemical localization of gamma-aminobutyric acid (GABA) in the cat superior colliculus. Journal of Comparative Neurology 276, 169–187.CrossRefGoogle ScholarPubMed
Mize, R.R. (1989). Enkephalin-like immunoreactivity in the cat superior colliculus: Distribution, ultrastructure, and colocalization with GABA. Journal of Comparative Neurology 285, 133–155.CrossRefGoogle ScholarPubMed
Mize, R.R. & Horner, L.H. (1989). Origin, distribution, and morphology of serotonergic afferents to the cat superior colliculus: A light and electron microscope immunocytochemistry study. Experimental Brain Research 75, 83–98.CrossRefGoogle Scholar
Mize, R.R. & Murphy, E.H. (1976). Alterations in receptive field properties of superior colliculus cells produced by visual cortex ablation in infant and adult cats. Journal of Comparative Neurology 168, 393–424.CrossRefGoogle ScholarPubMed
Mize, R.R. & Norton, T.T. (1985). GABA antiserum reactivity in the superior colliculus of the tree shrew (Tupaia Belangeri). Investigative Ophthalmology and Visual Science (Suppl.) 26, 163.Google Scholar
Mize, R.R. & Sterling, P. (1976). Synaptic organization of the superficial gray layer of cat superior colliculus analyzed by serial section cinematography. Investigative Ophthalmology and Visual Science (Suppl.) 15, 47.Google Scholar
Mize, R.R. & Vana, B.A. (1989). Origin and distribution of norepinephrine in the cat superior colliculus studied with an antibody to dopamine-beta-hydroxylase and horseradish peroxidase retrograde transport. Investigative Ophthalmology and Visual Science (Suppl.) 30, 300.Google Scholar
Mize, R.R. & White, D.A. (1989). [3H]muscimol labels neurons in both the superficial and deep layers of cat superior colliculus. Neuroscience Letters 104, 31–37.CrossRefGoogle Scholar
Mize, R.R., Beitz, A.J., Madl., J.E. & Gurski, M.R. (1987). Corticotectal cells in cat are glutamate immunoreactive: a double label study using WGA retrograde transport and transmitter immunocytochemistry. Society for Neuroscience Abstracts 13, 1435.Google Scholar
Mize, R.R., Jeon, C.-J., Butler, G.D. & Emson, P.C. (1990). Antibodies to calbindin label discrete subpopulations of interneurons in the cat superior colliculus. Society for Neuroscience Abstracts 16, 108.Google Scholar
Mize, R.R., Spencer, R.F. & Sterling, p. (1981). Neurons and glia in cat superior colliculus accumulate [3H]-gamma-aminobutyric acid (GABA). Journal of Comparative Neurology 202, 385–396.CrossRefGoogle ScholarPubMed
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, 180–192.CrossRefGoogle ScholarPubMed
Montero, V.M. (1986). Localization of aminobutyric acid (GABA) in type 3 cells and demonstration of their source to F2 terminals in the cat lateral geniculate nucleus: A Golgi-electron-microscopic GABAimmunocytochemical study. Journal of Comparative Neurology 254, 228–245.CrossRefGoogle ScholarPubMed
Morrison, J.R. & Foote, S.L. (1986). Noradrenergic and serotoninergic innervation of cortical, thalamic, and tectal visual structures in old and new world monkeys. Journal of Comparative Neurology 243, 117–138.CrossRefGoogle ScholarPubMed
Mugnaini, E. & Oertel, W.H. (1985). An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunohistochemistry. In Handbook of Chemical Neuroanatomy. Vol. 4: GABA and Neuropeprides in the CNS, Part 1, ed. Bjorklund, A. & Hokfelt, T., pp. 436–608. New York: Elsevier.Google Scholar
Nabors, L.B. & Mize, R.R. (1990). Antibodies to calbindin delineate retinal projection zones within the pretectum. Society for Neuroscience Abstracts 16, 109.Google Scholar
Norita, M. (1980). Neurons and synaptic patterns in the deep layers of the superior colliculus of the cat. A Golgi and electron microscopic study. Journal of Comparative Neurology 190, 29–48.CrossRefGoogle Scholar
Norita, M. & Sugiyama, M. (1979). Presynaptic dendrites and serial synapses in the intermediate and deep layers of the cat superior colliculus. Neuroscience Letters 11, 161–164.CrossRefGoogle Scholar
Okada, Y. (1974). Distribution of gamma-aminobutyric acid (GABA) in the layers of superior colliculus of the rabbit. Brain Research 75, 362–365.CrossRefGoogle ScholarPubMed
Okada, Y. (1976). Distribution of GABA and GAD activity in the layers of superior colliculus of the rabbit. In GABA in Nervous System Function, ed. Roberts, E., Chase, T.N. & Tower, D.B., pp. 229–233. New York: Raven Press.Google Scholar
Okada, Y.& Saito, M. (1979). Inhibitory action of adenosine, 5-HT (serotonin) and GABA (γ-aminobutyric acid) on the postsynaptic potential (PSP) of slices from olfactory cortex and superior colliculus in correlation to the level of cyclic AMP. Brain Research 160, 368–371.CrossRefGoogle Scholar
Ottersen, O.P. & Storm-Mathisen, J. (1984 a). Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. Journal of Comparative Neurology 229, 374–392.CrossRefGoogle ScholarPubMed
Ottersen, O.P. & Storm-mathisen, J. (1984 b). Neurons containing or accumulating transmitter amino acids. In Handbook of Chemical Neuroanatomy, Vol 3: Classical Transmitters and Transmitter Receptors in the CNS, Part II, ed. Bjorklund, A., Hokfelt, T. & Kuhar, M.J., pp. 141–246. New York: Elsevier.Google Scholar
Palacios, J.M., Wamsley, J.K. & Kuhar, M.J. (1981). High-affinity GABA receptors—autoradiographic localization. Brain Research 222, 285–307.CrossRefGoogle ScholarPubMed
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.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
Ribak, C.E., Vaughn, J.E. & Satto, K. (1978). Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following coichicine inhibition of axonal transport. Brain Research 140, 315–332.CrossRefGoogle ScholarPubMed
Rosenquist, A.C. & Palmer, L.A. (1971). Visual rcceptive field properties of cells of the superior colliculus after cortical lesions in the cat. Experimental Neurology 33, 629–652.CrossRefGoogle ScholarPubMed
Rothe, T., Schliebs, R. & Bigl, V. (1985). Benzodiazepine receptors in the visual structures of monocularly deprived rats. Effects of light and dark adaptation. Brain Research 329, 143–150.CrossRefGoogle ScholarPubMed
Sandberg, M., Jacobson, I. & Hamberger, A. (1982). Release of endogenous amino acids in vitro from the superior colliculus and the hippocampus. Progress in Brain Research 55, 157–166.CrossRefGoogle ScholarPubMed
Schiller, P.H., Stryker, M., Cynader, M. & Berman, N. (1974). Response characteristics of single cells in the monkey superior colliculus following ablation or cooling of visual cortex. Journal of Neurophysiology 37, 181–194.CrossRefGoogle ScholarPubMed
Schliebs, R. & Rothe, T. (1988). Development of GABAa receptors in the central visual structures of rat brain. Effects of visual pattern deprivation. General Physiology and Biophysics 7, 281–292.Google ScholarPubMed
Sherman, S.M. & Koch, C. (1986). The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Experimental Brain Research 63, 1–20.CrossRefGoogle ScholarPubMed
Sulrro, A.M. (1977). Inhibitory process underlying the directional specificity of simple, complex, and hypercomplex cells in the cat's visual cortex. Journal of Physiology 271, 699–720.Google Scholar
Sivilotti, L. & Nistri, A. (1989). Pharmacology of a novel effect of gamma-aminobutyric acid on the frog optic tectum in vitro. European Journal of Pharmacology 164, 205–212.CrossRefGoogle ScholarPubMed
Skangiel-Kramska, J., Cymerman, U. & Kossut, M. (1986). Autoradiographic localization of GABAergic and muscarinic cholinergic receptors sites in the visual system of the kitten. Acta Neurobiologae Experimenralis 46, 119–130.Google ScholarPubMed
Spencer, R.F., Wenthold, R.J. & Baker, R. (1989). Evidence of glycine as an inhibitory neurotransmitter of vestibular, reticular, and prepositus hypoglossi neurons that project to the cat abducens nucleus. Journal of Neuroscience 9, 2718–2736.CrossRefGoogle Scholar
Stein, B.E. & Arigbede, M.O. (1972). A parametric study of movement detection properties of neurons in the cat's superior colliculus. Experimental Neurology 36, 179–196.CrossRefGoogle Scholar
Sterling, P. (1971). Receptive fields and synaptic organization of the superficial gray layer of the cat superior colliculus. Vision Research (Suppl.) 3, 309–328.CrossRefGoogle Scholar
Sterling, P. & Davis, T.L. (1980). Neurons in the cat lateral geniculate nucleus that concentrate exogenous [3H]-gamma-aminobutyric acid (GABA). Journal of Comparative Neurology 192, 737–749.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Streit, P., Knecht, E., Reubi, J.C., Hunt, S.P. & Cuenod, M. (1978). GABA-specific presynaptic dendrites in pigeon optic tectum: A high- resolution autoradiographic study. Brain Research 149, 204–210.CrossRefGoogle ScholarPubMed
Swanson, L.W., Cowan, W.M. & Jones, E.G. (1974). An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and the cat. Journal of Comparative Neurology 156, 143–164.CrossRefGoogle ScholarPubMed
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, 279–295.CrossRefGoogle ScholarPubMed
Ueda, S., Ihra, N. & Sano, Y. (1985). The organization of serotonin fibers in the mammalian superior colliculus. An immunohistochemical study. Anatomy and Embryology (Berlin) 173, 13–21.CrossRefGoogle ScholarPubMed
Updyke, B.V. (1974). Characteristic of unit responses in superior colliculus of the monkey. Journal of Neurophysiology 37, 896–909.CrossRefGoogle ScholarPubMed
Valverde, F. (1973). The neuropil in superficial layers of the superior colliculus of the mouse. A correlated Golgi and electron-microscopic study. Zeitschrft für Anatomie und Entwicklungsgeschichte 142, 117–147.CrossRefGoogle Scholar
Vincent, S.R., Hattori, T. & McGeer, E.G. (1978). The nigrotectal projection: A biochemical and ultrastructural characterization. Brain Research 151, 159–164.CrossRefGoogle ScholarPubMed
Wenthold, R.J., Zempel, J.M., Parakkal, M.R., Reeks, K.A. & Altschuler, R.A. (1986). Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig. Brain Research 380, 7–18.CrossRefGoogle ScholarPubMed
Wickelgren, B.G. & Sterling, P. (1969). Influence of visual cortex on receptive fields in the superior colliculus of the cat. Journal of Neurophysiology 32, 16–23.CrossRefGoogle ScholarPubMed
Young, S.J., Royer, S.M., Groves, P.M. & Kinnamon, J.C. (1987). Three-dimensional reconstructions from serial micrographs using the IBM PC. Journal of Electron Microscopy Technique 6, 207–217.CrossRefGoogle Scholar