Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-26T03:12:53.108Z Has data issue: false hasContentIssue false
  • English
  • Français

Postsynaptic potentials and morphology of tectal cells responding to electrical stimulation of the bullfrog nucleus isthmi

Published online by Cambridge University Press:  02 June 2009

S.R. Wang  and
N. Matsumoto
S.R. Wang
Affiliation:
Department of Visual Information Processing, Institute of Biophysics, Academia Sinica, 100080 Beijing, China
N. Matsumoto
Affiliation:
Department of Biophysical Engineering, Faculty of Engineering Science, Osaka University, Osaka 560, Japan
Get access Rights & Permissions [Opens in a new window]

Abstract

Postsynaptic responses of tectal cells in the bullfrog (Rana catesbeiana) were intracellularly recorded following electrical stimulation of the optic tract and the nucleus isthmi, and fluorescent dye, Lucifer yellow, was injected into some of the impaled cells to show their morphologies. Two main response types were found: The first type was an EPSP followed by an IPSP, and the second type was single IPSP. The first type predominates in cells responding to the optic tract stimulation and the second type prevails in cells responding to the isthmic stimulation. Fifteen cells stained with Lucifer yellow were localized in layer 6 (11 cells), layer 7 (1 cell), and layer 8 (3 cells). They were mainly identified as pear-shaped cells, large ganglionic cells, and stellate cells. Three injections demonstrated “dye-coupling,” which labeled up to six cells following one injection. Comparisons of postsynaptic potentials with cellular morphologies suggested that the nucleus isthmi could directly excite large ganglionic neurons in layer 6. Synaptic mechanisms for strong isthmic inhibition on the tectal neurons remain unknown.

Keywords

Electrical stimulationIntracellular stainingPostsynaptic potentialTectal neuronNucleus isthmiBullfrog
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 5 , November 1990 , pp. 479 - 488
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

Antal, M., Matsumoto, N., & Székely, G. (1986). Tectal neurons of the frog: intracellular recording and labeling with cobalt electrodes. Journal of Comparative Neurology 246, 238–253.CrossRefGoogle ScholarPubMed
Arbib, M.A. (1987). Levels of modeling of mechanisms of visually guided behavior. Behavioral and Brain Sciences 10, 407–436.CrossRefGoogle Scholar
Baleydier, C. & Magnin, M. (1979). Afferent and efferent connections of the parabigeminal nucleus in cat revealed by retrograde axonal transport of horseradish peroxidase. Brain Research 161, 187–198.CrossRefGoogle ScholarPubMed
Caine, H.S. & Gruberg, E.R. (1985). Ablation of nucleus isthmi leads to loss of specific visually elicited behaviors in the frog (Rana pipiens). Neuroscience Letters 54, 307–312.CrossRefGoogle ScholarPubMed
Collett, T.S. & Udin, S.B. (1983). The role of the toad's nucleus isthmi in prey-catching behavior. In Proceedings of the Second Workshop on Visuomotor Coordination in Frog and Toad: Models and Experiments, ed. Lara, R. & Arbib, M.A., pp. 117–135. Coins Technical Report 83–19.Google Scholar
Felix, D., Wang, S.R., Yan, K. & Wang, Y.T. (1985). The effect of acetylcholine on neurons of the amphibian nucleus isthmi. Brain Research 326, 313–316.CrossRefGoogle ScholarPubMed
Fite, K.V. & Wang, S.R. (1986). Microiontophoresis and single-unit analysis of cholinergic drugs in the optic tectum of frog. Brain, Behavior, and Evolution 28, 198–206.CrossRefGoogle Scholar
Freeman, J.A. & Norden, J.J. (1984). Neurotransmitters in the optic tectum nmammalians. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 469–546. New York: Plenum Press.CrossRefGoogle Scholar
Glasser, S. & Ingle, D.J. (1978). The role of the nucleus isthmi in the ipsilateral visual projection of the frogapos;s optic tectum. Society for Neuroscience Abstracts 4, 630.Google Scholar
Grace, A.A. & Bunney, B.S. (1983). Intracellular and extracellular electrophysiology of nigral dopaminergic neurons, III: Evidence for electrotonic coupling. Neuroscience 10, 333–348.CrossRefGoogle Scholar
Graybiel, A.M. (1978). A satellite system of the superior colliculus: the parabigeminal nucleus and its projections to the superficial collicular layers. Brain Research 145, 365–374.CrossRefGoogle Scholar
Grobstein, P., Comer, C., Hollyday, M. & Archer, S.M. (1978). A crossed isthmo-tectal projection in Rana pipiens and its involvement in the ipsilateral visuotectal projection. Brain Research 156, 117–123.CrossRefGoogle ScholarPubMed
Gruberg, E.R. (1983). Recent work on the nucleus isthmi and its niche in the visual system. In Progress in Nonmammalian Brain Research, Vol. I, ed. Nistico, & Bolis, L., pp. 159–174. Boca Raton: CRC Press.Google Scholar
Gruberg, E.R. & Udin, S. (1978). Topographic projections between the nucleus isthmi and the tectum of the frog (Rana pipiens). Journal of Comparative Neurology 179, 487–500.CrossRefGoogle ScholarPubMed
Gruberg, E.R. & Lettvin, J.Y. (1980). Anatomy and physiology of a binocular system in the frog (Rana pipiens). Brain Research 192, 313–325.CrossRefGoogle ScholarPubMed
Hardy, O., Leresche, N. & Jassik-Gerschenfeld, D. (1985). Morphology and laminar distribution of electrophysiologically identified cells in the pigeon's optic tectum: an intracellular study. Journal of Comparative Neurology 233, 390–404.CrossRefGoogle ScholarPubMed
Harting, J.K., Hashikawa, T. & Van Lieshout, D. (1986). Laminar distribution of tectal, parabigeminal, and pretectal inputs to the primate dorsal lateral geniculate nucleus: connectional studies in Galago crassicaudatus. Brain Research 366, 358–363.CrossRefGoogle Scholar
Hashikawa, T., Van Lieshout, D. & Harting, J.K. (1986). Projections from the parabigeminal nucleus to the dorsal lateral geniculate nucleus in the tree shrew (Tupaia glis). Journal of Comparative Neurology 246, 382–394.CrossRefGoogle Scholar
Hock, F.J. (1983). Cholinergic system in the toad's (Bufo bufo L.) visual system. Behavioral and Neural Biology 38, 313–316.CrossRefGoogle ScholarPubMed
Hunt, S.P., Heneke, H., Reubi, J.C., Schenker, T., Sterit, P., Felix, D. & Cuenod, M. (1976). Afferent and intrinsic organization of laminated structures in the brain. Experimental Brain Research (Suppl.) 1, 521–525.Google Scholar
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
Hunt, S.P., Streit, P., Kunzle, H. & Cuenod, M. (1977). Characterization of the pigeon isthmo-tectal pathway by selective uptake and retrograde movement of radioactive compounds and by Golgi-like horseradish peroxidase labeling. Brain Research 129, 197–212.CrossRefGoogle ScholarPubMed
Ito, H., Tanaka, H., Sakamoto, N. & Morita, Y. (1981). Isthmic afferent neurons identified by the retrograde HRP method in a teleost (Novodon modestus). Brain Research 207, 163–169.CrossRefGoogle Scholar
Ito, H., Sakamoto, N. & Takatsuji, K. (1982). Cytoarchitecture, fiber connections, and ultrastructure of nucleus isthmi in a teleost (Navodon modestus) with a special reference to degenerating isthmic afferents from optic tectum and nucleus pretectalis. Journal of Comparative Neurology 205, 299–311.CrossRefGoogle Scholar
Jen, L.S., Dai, Z.G. & So, K.F. (1984). The connections between the parabigeminal nucleus and the superior colliculus in the golden hamster. Neuroscience Letters 5, 189–194.CrossRefGoogle Scholar
Kunzle, H. & Schnyder, H. (1984). The isthmus-tegmentum complex in the turtle and rat: a comparative analysis of its interconnections with the optic tectum. Experimental Brain Research 56, 509–522.CrossRefGoogle Scholar
Lázár, G., Toth, P., Csank, G. & Kicliter, E. (1983). Morphology and location of tectal projection neurons in frogs: a study with HRP and cobalt-filling. Journal of Comparative Neurology 215, 108–120.CrossRefGoogle ScholarPubMed
Leresche, N., Hardy, O., Audinat, E. & Jassik-Gerschenfeld, D. (1986). Synaptic organization of inhibitory circuits in the pigeon's optic tectum. Brain Research 365, 383–387.CrossRefGoogle ScholarPubMed
Lettvin, J.Y., Maturana, H., McCulloch, W.S. & Pitts, W.H. (1959). What the frog's eye tells the frog's brain. Proceedings of Institute of Radio Engineers 47, 1940–1951.Google Scholar
Li, Z., Wang, S.R., Xu, H.Y. & Yan, K. (1987). Acetylcholinesterase staining patterns of the tectum–nucleus isthmi systems in frogs and pigeons. Acta Anatomica Sinica 18, 42–47.Google Scholar
Linden, R. & Perry, V.H. (1983). Retrograde and anterograde-transneuronal degeneration in the parabigeminal nucleus following tectal lesions in developing rats. Journal of Comparative Neurology 218, 270–281.CrossRefGoogle ScholarPubMed
Matsumoto, N. (1989). Morphological and physiological studies of tectal and pretectal neurons in the frog. In Visuomotor Coordination: Amphibians, Comparisons, Models, and Robots, ed. Ewert, J.P. & Arbib, M.A., pp. 201–222. New York: Plenum Press.CrossRefGoogle Scholar
Matsumoto, N. & Bando, T. (1980). Excitatory synaptic potentials and morphological classification of tectal neurons of the frog. Brain Research 192, 39–48.CrossRefGoogle ScholarPubMed
Matsumoto, N., Schwippert, W.W. & Ewert, J.P. (1986). Intracellular activity of morphologically identified neurons of the grass frog's optic tectum in response to moving configurational visual stimuli. Journal of Comparative Physiology A 159, 721–739.CrossRefGoogle Scholar
Mendez-Otero, R., Rocha-Mirinda, C.E. & Perry, V.H. (1980). The organization of the parabigemino-tectal projections in the opossum. Brain Research 193, 183–189.CrossRefGoogle Scholar
Mufson, E.J., Martin, T.L., Mash, D.C., Wainer, B.H. & Mesulam, M.M. (1986). Cholinergic projections from the parabigeminal nucleus (Ch8) to the superior colliculus in the mouse: a combined analysis of horseradish-peroxidase transport and choline-acetyltransferase immunohistochemistry. Brain Research 370, 144–148.CrossRefGoogle Scholar
Nagano, K., Li, Q.L., Tamada, A. & Matsumoto, N. (1988). An analysis of postsynaptic potentials of tectal neurons of the frog: correlation with impulses recorded from the terminals of retinotectal afferents. Experimental Brain Research 70, 429–432.CrossRefGoogle ScholarPubMed
Potter, H.D. (1969). Structural characteristics of cell and fiber populations in the optic tectum of the frog (Rana catesbeiana). Journal of Comparative Neurology 136, 203–232.CrossRefGoogle ScholarPubMed
Reubi, J.C. & Cuenod, M. (1976). Release of exogenous glycine in the pigeon optic tectum during stimulation of a midbrain nucleus. Brain Research 112, 347–361.CrossRefGoogle ScholarPubMed
Ricciuti, A.J. & Gruberg, E.R. (1985). Nucleus isthmi provides most tectal choline acetyltransferase in the frog (Rana pipiens). Brain Research 341, 399–402.CrossRefGoogle ScholarPubMed
Roberts, P.J. & Yates, R.A. (1976). Tectal deafferentation in the frog: selective loss of L-glutamate and r-aminobutyrate. Neuroscience 1, 371–374.CrossRefGoogle Scholar
Roldman, M., Reinoso-Suarez, F. & Tortelly, A. (1983). Parabigeminal projections to the superior colliculus in the cat. Brain Research 280, 1–13.CrossRefGoogle Scholar
Sas, E. & Maler, L. (1986). Identification of a nucleus isthmi in the weakly electric fish Apteronotus leptorhynchus (Gymnotiformes). Brain, Behavior, and Evolution 28, 170–185.CrossRefGoogle ScholarPubMed
Satou, M. & Ewert, J.P. (1985). The antidromic activation of tectal neurons by electrical stimuli applied to the caudal medulla oblongata in the toad (Bufo bufo L.). Journal of Comparative Neurology 157, 739–748.Google Scholar
Sherk, H. (1978). Visual-response properties and visual-field topography in the cat's parabigeminal nucleus. Brain Research 145, 375–379.CrossRefGoogle ScholarPubMed
Sherk, H. (1979 a). A comparison of visual-response properties in cat's parabigeminal nucleus and superior colliculus. Journal of Neurophysiology 42, 1640–1655.CrossRefGoogle ScholarPubMed
Sherk, H. (1979 b). Connections and visual-field mapping in cat's tectoparabigeminal circuit. Journal of Neurophysiology 42, 1656–1668.CrossRefGoogle ScholarPubMed
Soltesz, I., Lightowler, S., Leresche, N. & Crunelli, V. (1989). optic tract stimulation evokes GABAa but not GABAb IPSPs in the rat ventral lateral geniculate nucleus. Brain Research 479, 49–55.CrossRefGoogle Scholar
Stevens, R.J. (1973). A cholinergic inhibitory system in the frog optictectum: its role in visual electrical responses and feeding behavior. Brain Research 49, 309–321.CrossRefGoogle Scholar
Stewart, W.W. (1978). Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14, 741–759.CrossRefGoogle ScholarPubMed
Székely, G. (1973). Anatomy and synaptology of the optic tectum. In Handbook of Sensory Physiology, Vll/3: Central Visual Information B, ed. Richard, J., pp. 1–26. 1973. Springer–Verlag.Google Scholar
Székely, G. & Lázár, G. (1976). Cellular and synaptic architecture of the optic tectum. In Frog Neurobiology, ed. Llinas, R. & Precht, W., pp. 407–437. Springer–Verlag.CrossRefGoogle Scholar
Udin, S.B. (1987). A projection from the mesencephalic tegmentum to the nucleus isthmi in the frogs Rana pipiens and Acris crepitans. Neuroscience 21, 631–638.CrossRefGoogle Scholar
Vinogradova, V.M. & Manteifel, Tu.B. (1977). Neuronal responses in the nucleus isthmi area of the frog to optic nerve stimulation. Neurophysiology (in Russian) 9, 33–40.CrossRefGoogle ScholarPubMed
Vinogradova, V.M. & Manteifel, Tu. B. (1979). Neuronal reactions of the isthmal nucleus area of the frog Rana temporaria to visual stimulation. Journal of Evolutionary Biochemistry and Physiology (in Russian) 15, 172–178.Google Scholar
Wang, S.R. (1988). The nucleus isthmus is a visual center: neuroanatomy and electrophysiology. In Vision: Structure and Function, ed. Yew, D.T., So, K.F. & Tsang, D.S.C., pp. 304–364. Singapore: World Scientific Publishing Co., Pte. Ltd.Google Scholar
Wang, S.R., Yan, K. & Wang, Y.T. (1981). Visual-field topography in the frog's nucleus isthmi. Neuroscience Letters 23, 37–41.Google ScholarPubMed
Wang, S.R., Yan, K. & Wang, Y.T. (1982). Nucleus isthmus of toad is secondary visual center. Scientia Sinica (Series B) 25, 1172–1178.Google ScholarPubMed
Wang, S.R., Yan, K., Wang, Y.T., Jiang, S.Y. & Wang, X.S. (1983 a). Neuroanatomy and electrophysiology of the lacertilian nucleus isthmi. Brain Research 275, 355–360.CrossRefGoogle ScholarPubMed
Wang, Y.T., Yan, K. & Wang, S.R. (1983 b). Reciprocal topography between the toad's tectum and nucleus isthmi and cell classification. Kexue Tongbao (Chinese Science Bulletin) 28, 1681–1684.Google Scholar
Wang, S.R., Yan, K. & Xu, H.Y. (1985). Chemosensitivity of the frog isthmic neurons to acetylcholine, glutamate, and glycine. Kexue Tongbao (Chinese Science Bulletin) 30, 1681–1683.Google Scholar
Wang, S.R., Wang, Y.T. & Wang, X.S. (1986 a). The distribution of acetylcholinesterase in the nucleus isthmi of amphibians and reptiles. Kexue Tongbao (Chinese Science Bulletin) 31, 700–702.Google Scholar
Wang, S.R., Li, Z. & Xu, H.Y (1986 b). Muscarinic action of acetylcholine in the pigeon optic tectum. Experimental Neurology 94, 436–440.CrossRefGoogle ScholarPubMed
Watanabe, K. & Kawana, E. (1979). Efferent projections of the parabigeminal nucleus in rats: a horseradish peroxidase (HRP) study. Brain Research 168, 1–11.CrossRefGoogle ScholarPubMed
Weerasuriya, A. & Ewert, J.P. (1981). Prey-selective neurons in the toad's optic tectum and sensori-motor interfacing: HRP studies and recording experiments. Journal of Comparative Physiology 144, 429–434.CrossRefGoogle Scholar
Williams, B. & Vanegas, H. (1982). Tectal projections in teleosts: responses of some target nuclei to direct tectal stimulation. Brain Research 242, 3–9.CrossRefGoogle ScholarPubMed
Williams, B., Hernandez, N. & Vanegas, H. (1983). Electrophysiological analysis of the teleostean nucleus isthmi and its relationships with the optic tectum. Journal of Comparative Physiology 152, 545–554.CrossRefGoogle Scholar
Yan, K. & Wang, S.R. (1986). Visual responses of neurons in the avian nucleus isthmi. Neuroscience Letters 64, 340–344.CrossRefGoogle ScholarPubMed
Zieglgansberger, W. & Reiter, G. (1974). Interneuronal movement of Procion yellow in cat spinal neurons. Experimental Brain Research 20, 527–530.CrossRefGoogle Scholar