Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-26T20:13:42.469Z Has data issue: false hasContentIssue false
  • English
  • Français

Glutamate containing neurons in the cat superior colliculus revealed by immunocytochemistry

Published online by Cambridge University Press:  02 June 2009

Chang-Jin Jeon ,
Michael R. Gurski  and
R. Ranney Mize
Chang-Jin Jeon
Affiliation:
Department of Anatomy and Neurobiology, University of Tennessee, Memphis, and Department of Anatomy and the Neuroscience Center, Louisiana State University Medical Center, New Orleans
Michael R. Gurski
Affiliation:
Department of Anatomy and Neurobiology, University of Tennessee, Memphis, and Department of Anatomy and the Neuroscience Center, Louisiana State University Medical Center, New Orleans
R. Ranney Mize
Affiliation:
Department of Anatomy and Neurobiology, University of Tennessee, Memphis, and Department of Anatomy and the Neuroscience Center, Louisiana State University Medical Center, New Orleans
Get access Rights & Permissions [Opens in a new window]

Abstract

Glutamate is the probable neurotransmitter of both retinal and cortical afferents to the cat superior colliculus (SC). The present study shows that glutamate is also contained in many postsynaptic neurons in SC. The distribution, morphology, and ultrastructure of neurons in SC were examined using glutamate antibody immunocytochemistry. Labeled cells were widely distributed throughout, but a specific laminar pattern was evident. Relatively few cells were found in the zonal and upper superficial gray layers (SGL). A dense band of intensely labeled neurons was found within the deep superficial gray and upper optic layers. Many cells were also labeled in the deeper layers. Labeled cells had varied sizes and morphologies. Soma diameters ranged from 9–67 μm, with a mean of 22 μm. Cells with stellate, vertical fusiform, and multipolar morphologies were labeled. Cells in the deep subdivision all had morphologies and sizes typical of projection neurons. To determine if labeled cells in the dense band were also projection neurons, WGA-HRP was injected into the lateral posterior nucleus and these sections were double-labeled with the glutamate antibody. Over one-half of cells in the dense band that were labeled by HRP were also obviously labeled by antibody. At the electron-microscope level, both medium- and large-sized neurons were also labeled by glutamate antibodies. These cells had different but characteristic morphologies.

Keywords

Projection neuronsRetrograde tracingGamma-L-glutamyl-L-glutamic acidUltrastructureAmino acid neurotransmitters
Type
Short Communication
Information
Visual Neuroscience , Volume 14 , Issue 2 , March 1997 , pp. 387 - 393
Copyright
Copyright © Cambridge University Press 1997

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

REFERENCES

Baughman, R.W. & Gilbert, C.D. (1981). Aspartate and glutamate as possible neurotransmitters in the visual cortex. Journal of Neuroscience 1, 427–439.CrossRefGoogle ScholarPubMed
Beitz, A.J. (1989). Possible origin of glutamatergic projections to the midbrain periaquaductal gray and deep layer of the superior colliculus of the rat. Brain Research Bulletin 23, 25–35.CrossRefGoogle Scholar
Bennett-Clarke, C., Mooney, R.D., Chiaia, N.L. & Rhoades, R.W. (1989). A substance P projection from the superior colliculus to the parabigeminal nucleus in the rat and hamster. Brain Research 500, 1–11.CrossRefGoogle Scholar
Caldwell, R.B. & Mize, R.R. (1981). Superior colliculus neurons which project to the cat lateral posterior nucleus have varying morphologies. Journal of Comparative Neurology 203, 53–66.CrossRefGoogle Scholar
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., Iversen, E. & Fonnum, F. (1984). Effects of area 17 ablation on neurotransmitter parameters in efferents to area 18, the lateral geniculate body, pulvinar and superior colliculus in the cat. Neuroscience Letters 52, 323–328.CrossRefGoogle ScholarPubMed
Fosse, V.M., Kolstad, J. & Fonnum, F. (1986). A bioluminescence method for the measurements of L-glutamate: Application to the study of changes in the release of L-glutamate from lateral geniculate nucleus and superior colliculus after visual cortex ablation in rats. Journal of Neurochemistry 47, 340–349.CrossRefGoogle Scholar
Harrel, J.V., Caldwell, R.B. & Mize, R.R. (1982). The superior colliculus neurons which project to the dorsal and ventral lateral geniculate nuclei in the cat. Experimental Brain Research 46, 234–242.CrossRefGoogle Scholar
Jeon, C.-J., Hartman, M. & Mize, R.R. (1997). Glutamate-like immunoreactivity in the cat superior colliculus and visual cortex: Further evidence that glutamate is the neurotransmitter of the corticocollicular pathway. Visual Neuroscience 14, 27–38.CrossRefGoogle ScholarPubMed
Kanaseki, T. & Sprague, J.M. (1974). Anatomical organization of pretectal nuclei and tectal laminae in the cat. Journal of Comparative Neurology 158, 319–338.CrossRefGoogle ScholarPubMed
Kawamura, S., Fukushima, N., Hattori, S. & Kudo, M. (1980). Laminar segregation of cells of origin of ascending projections from the superficial layers of the superior colliculus in the cat. Brain Research 184, 486–490.CrossRefGoogle ScholarPubMed
Madl, J.E., Larson, A.A. & Beitz, A.J. (1986). Monoclonal antibody specific for carbodiimide-fixed glutamate: Immunocytochemical localization in the rat CNS. Journal of Histochemistry and Cytochemistry 34, 317–326.CrossRefGoogle ScholarPubMed
Mize, R.R. (1985 a). A microcomputer plotter for use with light and electron microscopes. In The Microcomputer in Cell and Neurobiology Research, ed. Mize, R.R., pp. 111–133. New York: Elsevier Science Publishers.Google Scholar
Mize, R.R. (1985 b). Morphometric measurement using a computerized digitizing system. In The Microcomputer in Cell and Neurobiology Research, ed. Mize, R.R., pp. 177–215. New York: Elsevier Science Publishers.Google Scholar
Mize, R.R. (1988). Immunocytochemical localization of gamma-amino-butyric acid (GABA) in the cat superior colliculus. Journal of Comparative Neurology 276, 169–187.CrossRefGoogle Scholar
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. (1992). The organization of GABAergic neurons in the mammalian superior colliculus. In Progress in Brain Research, Vol. 90. ed. Mize, R.R., Marc, R.E. & Sillito, A.M. pp. 219–248. Amsterdam: Elsevier.Google Scholar
Mize, R.R. (1994). Conservation of basic synaptic circuits that mediate GABA inhibition in the subcortical visual system. In Neuroscience: From the Molecular to the Cognitive. Progress in Brain Research, Vol. 100, ed. Bloom, F.E., pp. 123–132. Amsterdam: Elsevier.CrossRefGoogle Scholar
Mize, R.R. & Butler, G.D. (1996). Postembedding immunocytochemistry demonstrates directly that both retinal and cortical terminals in the cat superior colliculus are glutamate immunoreactive. Journal of Comparative Neurology 371, 633–648.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Mize, R.R., Spencer, R.F. & Sterling, P. (1982). Two types of GABA-accumulating neuron in the superficial gray layer of the cat superior colliculus. Journal of Comparative Neurology 206, 180–192.CrossRefGoogle ScholarPubMed
Mize, R.R., Jeon, C.-J., Butler, G.D., Luo, Q. & Emson, P.C. (1991). The calcium binding protein calbindin-D 28K reveals subpopulation of projection and interneurons in the cat superior colliculus. Journal of Comparative Neurology 307, 417–436.CrossRefGoogle ScholarPubMed
Mize, R.R., Luo, Q., Butler, G., Jeon, C.-J. & Nabors, B. (1992). The calcium binding proteins parvalbumin and calbindin-D 28K form complementary patterns in the cat superior colliculus. Journal of Comparative Neurology 320, 243–256.CrossRefGoogle ScholarPubMed
Mooney, R.D., Bennett-Clarke, C.A., King, T.D. & Rhoades, R.W. (1990). Tectospinal neurons in hamster contain glutamate-like immunoreactivity. Brain Research 537, 375–380.CrossRefGoogle ScholarPubMed
Moschovakis, A.K. & Karabelas, A.B. (1985). Observations on the somatodendritic morphology and axonal trajectory of intracellularly HRP-labeled efferent neurons located in the deeper layers of the superior colliculus of the cat. Journal of Comparative Neurology 239, 276–308.CrossRefGoogle ScholarPubMed
Moschovakis, A.K., Karabelas, A.B. & Highstein, S.M. (1988). Structure-function relationships in the primate superior colliculus: I. Morphological classification of efferent neurons. Journal of Neurophysiology 60, 232–262.CrossRefGoogle ScholarPubMed
Nabors, L.B. & Mize, R.R. (1991). A unique neuronal organization in the cat pretectum revealed by antibodies to the calcium binding protein calbindin-D 28K. Journal of Neuroscience 11, 2460–2476.CrossRefGoogle Scholar
Ottersen, O.P. & Storm-Mathisen, J. (1984). Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. Journal of Comparative Neurology 229, 374–393.CrossRefGoogle ScholarPubMed
Sakurai, T. & Okada, Y. (1992). Selective reduction of glutamate in the rat superior colliculus and dorsal lateral geniculate nucleus after contralateral enucleation. Brain Research 573, 197–203.CrossRefGoogle ScholarPubMed
Sakurai, T., Miyamoto, T. & Okada, Y. (1990). Reduction of glutamate content in rat superior colliculus after retino-tectal denervation. Neuroscience Utters 109, 299–303.CrossRefGoogle ScholarPubMed
Spangler, K.M. & Morley, B.J. (1987). Somatostatin-like immunoreactivity in the midbrain of the cat. Journal of Comparative Neurology 260, 87–97.CrossRefGoogle ScholarPubMed
Vincent, S.R., McIntosh, C.H.S., Buchanan, A.M.J. & Brown, J.C. (1985). Central somatostatin systems revealed with monoclonal antibodies. Journal of Comparative Neurology 238, 169–186.CrossRefGoogle ScholarPubMed