Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-27T06:07:55.616Z Has data issue: false hasContentIssue false
  • English
  • Français

Connections of contralaterally projecting isthmotectal axons and GABA-immunoreactive neurons in Xenopus tectum: An ultrastructural study

Published online by Cambridge University Press:  02 August 2005

KRYSTYNA KIELAN RYBICKA  and
SUSAN B. UDIN
KRYSTYNA KIELAN RYBICKA
Affiliation:
Department of Physiology and Biophysics, State University of New York, Buffalo
SUSAN B. UDIN
Affiliation:
Department of Physiology and Biophysics and Neuroscience Program, State University of New York, Buffalo
Get access Rights & Permissions [Opens in a new window]

Abstract

To investigate the circuitry that mediates binocular interactions in the tectum of Xenopus frogs, we have begun to identify the tectal cells that receive ipsilateral eye input relayed via the nucleus isthmi. Isthmotectal axons were labeled with horseradish peroxidase, and thin sections were labeled by postembedding immunogold reaction with antibodies to γ-aminobutyric acid (GABA). Ultrastructural examination reveals that many isthmotectal axons terminate on GABA-immunoreactive dendrites. Other isthmotectal axons contact postsynaptic structures that are unlabeled but have an appearance consistent with previously described GABA-poor zones of GABA-immunoreactive dendrites. We also examined the unlabeled inputs to the dendrites that were postsynaptic to filled isthmotectal axons. The most common nonisthmic inputs to those dendrites were GABA-immunoreactive processes with symmetric morphology. Surprisingly, we found only one input with the retinotectal characteristics of densely packed round, clear vesicles and minimal GABA immunoreactivity. These results indicate that isthmotectal axons synapse onto inhibitory interneurons, that retinotectal and isthmotectal axons do not synapse close to each other on the same dendrites, and that inhibitory connections are the closest neighbors to isthmotectal synapses.

Keywords

BinocularIsthmiVisionInhibitionTectum
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 3 , May 2005 , pp. 305 - 315
Copyright
2005 Cambridge University Press

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

Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 29, 775.CrossRefGoogle Scholar
Antal, M. (1991). Distribution of GABA immunoreactivity in the optic tectum of the frog: A light and electron microscopic study. Neuroscience 42, 879–891.CrossRefGoogle Scholar
Crooks, J. & Kolb, H. (1992). Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina. Journal of Comparative Neurology 315, 287–302.CrossRefGoogle Scholar
Da Costa, B.L.S.A., Hokoc, J.N., Pinaud, R.R., & Gattass, R. (1997). GABAergic retinocollicular projection in the new world monkey Cebus apella. Neuroreport 8, 1797–1802.CrossRefGoogle Scholar
Ewert, J.-P. (1984). Tectal mechanisms that underlie prey-catching and avoidance behaviors in toads. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 247–416. New York: Plenum.CrossRef
Finch, D.J. & Collett, T.S. (1983). Small-field, binocular neurones in the superficial layers of the frog optic tectum. Proceedings of the Royal Society B (London) 217, 491–497.CrossRefGoogle Scholar
Fite, K.V. (1969). Single-unit analysis of binocular neurons in the frog optic tectum. Experimental Neurology 24, 475–486.CrossRefGoogle Scholar
Gábriel, R. & Straznicky, C. (1995). Synapses of optic axons with GABA- and glutamate-containing elements in the optic tectum of Bufo marinus. Journal für Hirnforschung 36, 329–340.Google Scholar
Gaillard, F. (1985). Binocularly driven neurons in the rostral part of the frog optic tectum. Journal of Comparative Physiology A 157, 47–55.CrossRefGoogle Scholar
Gaze, R.M. & Keating, M.J. (1970). Receptive field properties of single units from the visual projection to the ipsilateral tectum in the frog. Quarterly Journal of Experimental Physiology 55, 143–152.CrossRefGoogle Scholar
Gernert, M. & Ewert, J.-P. (1995). Cholinergic, GABAergic, and dopaminergic influences on visually evoked field potentials in the superficial optic tectum of Bufo marinus. Comparative Biochemistry and Physiology A—Comparative Physiology 112, 387–401.CrossRefGoogle Scholar
Grant, A.S. & Lettvin, J.Y. (1991). Sources of electrical transients in tectal neuropil of the frog, Rana pipiens. Brain Research 560, 106–121.CrossRefGoogle Scholar
Grant, S., Dawes, E.A., & Keating, M.J. (1992). The critical period for experience-dependent plasticity in a system of binocular visual connection in Xenopus laevis: Its extension by dark-rearing. European Journal of Neuroscience 4, 37–45.CrossRefGoogle Scholar
Gray, E.G. (1959). Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscopic study. Journal of Anatomy 93, 420–433.Google 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
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 Scholar
Gruberg, E.R. & Udin, S.B. (1978). Topographic projections between the nucleus isthmi and the tectum of the frog Rana pipiens. Journal of Comparative Neurology 179, 487–500.CrossRefGoogle Scholar
Hamassaki-Britto, D.E., Brzozowska-Prechtl, A., Karten, H.J., Lindstrom, J.M., & Keyser, K.T. (1991). GABA-like immunoreactive cells containing nicotinic acetylcholine receptors in the chick retina. Journal of Comparative Neurology 313, 394–408.CrossRefGoogle Scholar
Hearl, W.G. & Churchich, J.E. (1985). A mitochondrial NADP+-dependent reductase related to the 4–aminobutyrate shunt. Purification, characterization, and mechanism. Journal of Biological Chemistry 260, 16361–16366.Google Scholar
Hickmott, P.W. & Constantine-Paton, M. (1993). The contributions of NMDA, non-NMDA, and GABA receptors to postsynaptic responses in neurons of the optic tectum. Journal of Neuroscience 13, 4339–4353.Google Scholar
Hughes, T.E. (1990). A light- and electron-microscopic investigation of the optic tectum of the frog, Rana pipiens, I: The retinal axons. Visual Neuroscience 4, 499–518.CrossRefGoogle Scholar
Kozicz, T. & Lázár, G. (2001). Colocalization of GABA, enkephalin and neuropeptide Y in the tectum of the green frog Rana esculenta. Peptides 22, 1071–1077.CrossRefGoogle Scholar
Lettvin, J.Y., Maturana, H.R., McCulloch, W.S., & Pitts, W.H. (1959). What the frog's eye tells the frog's brain. Proceedings of the Institute of Radio Engineers N.Y. 47, 1940–1951.CrossRefGoogle Scholar
Li, Z. & Fite, K.V. (2001). GABAergic visual pathways in the frog Rana pipiens. Visual Neuroscience 18, 457–464.CrossRefGoogle Scholar
Mahendrasingam, S., Wallam, C.A., Polwart, A., & Hackney, C.M. (2004). An immunogold investigation of the distribution of GABA and glycine in nerve terminals on the somata of spherical bushy cells in the anteroventral cochlear nucleus of guinea pig. European Journal of Neuroscience 19, 993–1004.CrossRefGoogle Scholar
Mize, R.R. (1992). The organisation of GABAergic neurons in the mammalian superior colliculus. In The Organization of GABAergic Neurons in the Mammalian Superior Colliculus, Vol. 90, ed. Mize, R.R., Marc, R.E. & Sillito, A.M., pp. 219–248. Amsterdam: Elsevier Science Publishers.
Mize, R.R. & Butler, G.D. (1997). The distribution of the GABAA β2,β3 subunit receptor in the cat superior colliculus using antibody immunocytochemistry. Neuroscience 79, 1121–1135.CrossRefGoogle Scholar
Östberg, A. & Norden, J. (1979). Ultrastructural study of degeneration and regeneration in the amphibian tectum. Brain Research 168, 441–455.CrossRefGoogle Scholar
Pasternack, M., Boller, M., Pau, B., & Schmidt, M. (1999). GABAA and GABAC receptors have contrasting effects on excitability in superior colliculus. Journal of Neurophysiology 82, 2020–2023.Google Scholar
Phend, K.D., Weinberg, R.J., & Rustioni, A. (1992). Techniques to optimize post-embedding single and double staining for amino acid neurotransmitters. Journal of Histochemistry and Cytochemistry 40, 1011–1020.CrossRefGoogle Scholar
Prada, C., Udin, S.B., Wiechmann, A.F., & Zdanova, I.V. (2005). Stimulation of melatonin receptors decreases calcium levels in Xenopus tectal cells by activating GABAC receptors. Journal of Neurophysiology, Published on-line April 7.Google Scholar
Prada, C., Wiechmann, A., Lima, R., & Udin, S.B. (2004). Melatonin 1b receptor expression and physiology in the tectum of Xenopus. Program No. 647.10. Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience. Online
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 Scholar
Rio, J.P., Vesselkin, N.P., Repérant, J., Kenigfest, N.B., Miceli, D., & Adanina, V. (1996). Retinal and non-retinal inputs upon retinopetal RMA neurons in the lamprey: A light and electron microscopic study combining HRP axonal tracing and GABA immunocytochemistry. Journal of Chemical Neuroanatomy 12, 51–70.CrossRefGoogle Scholar
Roberts, P.J. & Yates, R.A. (1976). Tectal deafferentation in the frog: Selective loss of L-glutamate and γ-aminobutyrate. Neuroscience 1, 371–374.CrossRefGoogle Scholar
Rogers, P.C. & Pow, D.V. (1995). Immunocytochemical evidence for an axonal localization of GABA in the optic nerves of rabbits, rats, and cats. Visual Neuroscience 12, 1143–1149.CrossRefGoogle Scholar
Rybicka, K.K. & Udin, S.B. (1994). Ultrastructure and GABA-immunoreactivity in layers 8 and 9 of the optic tectum of Xenopus laevis. European Journal of Neuroscience 6, 1567–1582.CrossRefGoogle Scholar
Scherer, W.J. & Udin, S.B. (1991). Latency and temporal overlap of visually-elicited contralateral and ipsilateral firing in Xenopus tectum during and after the critical period. Developmental Brain Research 58, 129–132.CrossRefGoogle Scholar
Schmidt, M., Boller, M., Ozen, G., & Hall, W.C. (2001). Disinhibition in rat superior colliculus mediated by GABAc receptors. Journal of Neuroscience 21, 691–699.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 Scholar
Skarf, B. (1973). Development of binocular single units in the optic tectum of frogs raised with disparate stimulation to the eyes. Brain Research 51, 352–357.CrossRefGoogle Scholar
Straznicky, C. & Hiscock, J. (1984). Post-metamorphic retinal growth in Xenopus. Anatomy and Embryology. 169, 103–109.CrossRefGoogle Scholar
Székely, G., Setalo, G., & Lázár, G. (1973). Fine structure of the frog's optic tectum: Optic fibre termination layers. Journal für Hirnforschung 14, 189–225.Google Scholar
Titmus, M.J., Lima, R., Tsai, H.J., & Udin, S.B. (1999). Effects of choline and other nicotinic agonists on the tectum of juvenile and adult Xenopus frogs: A patch-clamp study. Neuroscience 91, 753–769.CrossRefGoogle Scholar
Tyler, C.J., Fite, K.V., & Devries, G.J. (1995). Distribution of GAD-like immunoreactivity in the retina and central visual system of Rana pipiens. Journal of Comparative Neurology 353, 439–450.CrossRefGoogle Scholar
Udin, S.B. (1989). The development of the nucleus isthmi in Xenopus. II. Branching patterns of contralaterally projecting isthmotectal axons during maturation of binocular maps. Visual Neuroscience 2, 153–163.Google Scholar
Udin, S.B. & Fisher, M.D. (1985). The development of the nucleus isthmi in Xenopus laevis: I. Cell genesis and formation of connections with the tecta. Journal of Comparative Neurology 232, 25–35.Google Scholar
Udin, S.B., Fisher, M.D., & Norden, J.J. (1990). Ultrastructure of the crossed isthmotectal projection in Xenopus frogs. Journal of Comparative Neurology 292, 246–254.CrossRefGoogle Scholar
Udin, S.B., Fisher, M.D., & Norden, J.J. (1992). Isthmotectal axons make ectopic synapses in monocular regions of the tectum in developing Xenopus laevis frogs. Journal of Comparative Neurology 322, 461–470.CrossRefGoogle Scholar
Udin, S.B. & Grant, S. (1999). Plasticity in the tectum of Xenopus laevis: Binocular maps. Progress in Neurobiology 59, 81–106.CrossRefGoogle Scholar
Udin, S.B. & Keating, M.J. (1981). Plasticity in a central nervous pathway in Xenopus: Anatomical changes in the isthmotectal projection after larval eye rotation. Journal of Comparative Neurology 203, 575–594.CrossRefGoogle Scholar
Udin, S.B. & Scherer, W.J. (1990). Restoration of the plasticity of binocular maps by NMDA after the critical period in Xenopus. Science 249, 669–672.CrossRefGoogle Scholar
Waagepetersen, H.S., Sonnewald, U., & Schousboe, A. (1999). The GABA paradox: Multiple roles as metabolite, neurotransmitter, and neurodifferentiative agent. Journal of Neurochemistry 73, 1335–1342.CrossRefGoogle Scholar
Wang, S. & Wu, G. (1997). Intracellular recording and morphology of tectal neurons activated by contralateral nucleus isthmi in toads. Chinese Science Bulletin 42, 1647–1651.CrossRefGoogle Scholar
Watt, C.B., Glazebrook, P.A., & Florack, V.J. (1994). Localization of substance P and GABA in retinotectal ganglion cells of the larval tiger salamander. Visual Neuroscience 11, 355–362.CrossRefGoogle Scholar
Yen, L.H., Sibley, J.T., & Constantine-Paton, M. (1993). Fine-structural alterations and clustering of developing synapses after chronic treatments with low levels of NMDA. Journal of Neuroscience 13, 4949–4960.Google Scholar