Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-24T08:09:19.210Z Has data issue: false hasContentIssue false
  • English
  • Français

Dendritic development of retinal ganglion cells after prenatal intracranial infusion of tetrodotoxin

Published online by Cambridge University Press:  02 June 2009

Gregor Campbell ,
Ary S. Ramoa ,
Michael P. Stryker  and
Carla J. Shatz
Gregor Campbell
Affiliation:
Department of Anatomy, University College London, London, UK
Ary S. Ramoa
Affiliation:
Department of Anatomy, Medical College of Virginia, Virginia Commonwealth University, Richmond
Michael P. Stryker
Affiliation:
Department of Physiology, University of California, San Francisco
Carla J. Shatz
Affiliation:
Howard Hughes Medical Institute, Department of Cell and Molecular Biology, University of California, Berkeley
Get access Rights & Permissions [Opens in a new window]

Abstract

The dendritic form of a cell may be established by many factors both intrinsic and environmental. Blockade of action potentials along the course of axons and in their postsynaptic targets dramatically alters the development of axonal morphology. The extent to which blockade of target cell activity retrogradely alters the dendritic morphology of the presynaptic cells is unknown. To determine whether the establishment of dendritic form by developing retinal canclion cells depends on activity within their targets, the sodium channel blocker, tetrodotoxin (TTX), was administered via minipumps to the diencephalon of cat fetuses from embryonic day 43 (E43) to E57. At E57 retinae were removed and living retinal ganglion cells injected in vitro with Lucifer yellow to reveal their dendritic morphology. In the TTX-treated animals both alpha and beta types of retinal ganglion cells were present, as were putative gamma cells. Overall, the dendrites of retinal ganglion cells in TTX-treated animals appeared qualitatively and Quantitatively similar to those of untreated animals. The only significant change in the TTX-treated cases was a small increase in the number of dendritic spines on the non-beta cells. These results indicate that the acquisition of basic dendritic form of developing ganglion cells is not influenced by the action potential activity within their targets, and that it is also independent of the terminal branching patterns of their axons.

Keywords

Visual systemActivity-dependent developmentEnvironmental cuesDendritic developmentCat
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 4 , July 1997 , pp. 779 - 788
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

Archer, S.M., Dubin, M.W. & Stark, L.A. (1982). Abnormal development of kitten retino-geniculate connectivity in the absence of action potentials. Science 217, 743–745.CrossRefGoogle ScholarPubMed
Ault, S.J., Thompson, K.G., Zhou, Y. & Leventhal, A.G. (1993). Selective depletion of beta cells affects the development of alpha cells in cat retina. Visual Neuroscience 10, 237–245.CrossRefGoogle ScholarPubMed
Barnes, S. & Werblin, F. (1986). Gated currents generate single spike activity in amacrine cells of the tiger salamander retina. Proceedings of the National Academy of Sciences of the U.S.A. 83, 1509–1512.CrossRefGoogle ScholarPubMed
Blöchl, A. & Thoenen, H. (1995). Characterization of nerve growth factor (NGF) release from hippocampal neurons: Evidence for a constitutive and an unconventional sodium-dependent regulated pathway. European Journal of Neuroscience 7, 1220–1228.CrossRefGoogle Scholar
Bloomfield, S.A. (1992). Effects of tetrodotoxin on receptive fields on amacrine and ganglion cells in the rabbit retina. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1173.Google Scholar
Bodnarenko, S.F., Jeyarasasingam, G. & Chalupa, L.M. (1995). Development and regulation of dendritic stratification in retinal ganglion cells by glutamate-mediated afferent activity. Journal of Neuroscience 15, 7037–7045.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology (London) 240, 397–420.CrossRefGoogle ScholarPubMed
Cabelli, R.J., Hohn, A. & Shatz, C.J. (1995). Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 267, 1662–1666.CrossRefGoogle ScholarPubMed
Campbell, G. & Frost, D.O. (1988). Synaptic organization of anomalous retinal projections to the somatosensory and auditory thalamus: Targetcontrolled morphogenesis of axon terminals and synaptic glomeruli. Journal of Comparative Neurology 272, 383–408.CrossRefGoogle Scholar
Card-Linden, D., Guillery, R.W. & Cucchiaro, J. (1981). The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. Journal of Comparative Neurology 203, 189–211.CrossRefGoogle Scholar
Castrén, E., Zafra, F., Thoenen, H. & Lindholm, D. (1992). Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 89, 9444–9448.CrossRefGoogle ScholarPubMed
Catterall, W.A. & Morrow, C.S. (1978). Binding of saxitoxin to electrically excitable neuroblastoma cells. Proceedings of the National Academy of Sciences of the U.S.A. 75, 218–222.CrossRefGoogle ScholarPubMed
Catterall, W.A., Morrow, C.S. & Hartshorne, R.P. (1979). Neurotoxin binding to receptor sites associated with voltage-sensitive sodium channels in intact, lysed, and detergent-solubilized brain membranes. Journal of Biological Chemistry 254, 11379–11387.CrossRefGoogle ScholarPubMed
Dalva, M.B., Ghosh, A. & Shatz, C.J. (1994). Independent control of dendritic and axonal form in the developing lateral geniculate nucleus. Journal of Neuroscience 14, 3588–3602.CrossRefGoogle ScholarPubMed
Eysel, U.T., Peichl, L. & Wässle, H. (1985). Dendritic plasticity in the early postnatal feline retina: Quantitative characteristics and sensitive period. Journal of Comparative Neurology 242, 134–145.CrossRefGoogle ScholarPubMed
Foster, R.E., Connors, B.W. & Waxman, S.G. (1982). Rat optic nerve: Electrophysiological, pharmacological and anatomical studies during development. Developmental Drain Research 3, 371–386.CrossRefGoogle Scholar
Friedman, S. & Shatz, C.J. (1990). The effects of prenatal intracranial infusion of tetrodotoxin on naturally occurring retinal ganglion cell death and optic nerve ultrastructure. European Journal of Neuroscience 2, 243–253.CrossRefGoogle ScholarPubMed
Galli, L. & Maffei, L. (1988). Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science 242, 90–91.CrossRefGoogle ScholarPubMed
Goodman, C. & Shatz, C.J. (1993). Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72/Neuron (Suppl.) 10, 77–98.CrossRefGoogle Scholar
Hahm, J.-O, Langdon, R.B. & Sur, M. (1991). Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors. Nature 351, 568–570.CrossRefGoogle ScholarPubMed
Harris, W. A. (1981). Neural activity and development. Annual Review of Physiology 43, 689–710.CrossRefGoogle Scholar
Hefti, F. (1986). Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. Journal of Neuroscience 6, 2155–2162.CrossRefGoogle ScholarPubMed
Kirby, M.A. & Chalupa, L.M. (1986). Retinal crowding alters the morphology of alpha ganglion cells. Journal of Comparative Neurology 251, 532–541.CrossRefGoogle ScholarPubMed
Lau, K.C., So, K.-F. & Tay, D. (1992 a). Postnatal development of type I retinal ganglion cells in hamsters: A Lucifer yellow study. Journal of Comparative Neurology 315, 375–381.CrossRefGoogle ScholarPubMed
Lau, K.C., So, K.-F. & Tay, D. (1992 b). APV prevents the elimination of transient dendritic spines on a population of retinal ganglion cells. Brain Research 595, 171–174.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Schall, J.D. & Ault, S.J. (1988 a). Extrinsic determinants of retinal ganglion cell structure in the cat. Journal of Neuroscience 8, 2028–2038.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Schall, J.D., Ault, S.J., Provis, J.M. & Vitek, D.J. (1988 b). Class-specific cell death shapes the distribution and pattern of central projection of cat retinal ganglion cells. Journal of Neuroscience 8, 2011–2027.CrossRefGoogle ScholarPubMed
Lewin, G.R. & Barde, Y-A. (1996). Physiology of the neurotrophins. Annual Review of Neuroscience 19, 289–317.CrossRefGoogle ScholarPubMed
Lindholm, D., Castrén, E., Berzaghi, M., Blöchl, A. & Thoenen, H. (1994). Activity-dependent and hormonal regulation of neurotrophin mRNA levels in the brain-implications for neuronal plasticity. Journal of Neurobiology 25, 1362–1372.CrossRefGoogle ScholarPubMed
Lo, D.C. (1995). Neurotrophic factors and synaptic plasticity. Neuron 15, 979–981.CrossRefGoogle ScholarPubMed
Luskin, M.B. & Shatz, C.J. (1985). Studies of the earliest generated cells of the cat's visual cortex: Cogeneration of subplate and marginal zones. Journal of Neuroscience 5, 1062–1075.CrossRefGoogle ScholarPubMed
Maslim, J. & Stone, J. (1988). Time course of stratification of the dendritic fields of ganglion cells in the retina of the cat. Developmental Brain Research 44, 87–93.CrossRefGoogle ScholarPubMed
Maslim, J., Webster, M. & Stone, J. (1986). Stages in the structural differentiation of retinal ganglion cells. Journal of Comparative Neurology 254, 383–402.Google ScholarPubMed
McAllister, A.K., Lo, D.C. & Katz, L.C. (1995). Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15, 791–803.CrossRefGoogle ScholarPubMed
Meister, M., Wong, R.O.L., Baylor, D.A. & Shatz, Cj. (1991). Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939–943.CrossRefGoogle ScholarPubMed
Montague, P.R. & Friedlander, M.J. (1991). Morphogenesis and territorial coverage by isolated mammalian retinal ganglion cells. Journal of Neuroscience 11, 1440–1457.CrossRefGoogle ScholarPubMed
Mooney, R., Madison, D.V. & Shatz, C.J. (1993). Enhancement of transmission at the developing retinogeniculate synapse. Neuron 10, 815–825.CrossRefGoogle ScholarPubMed
Morest, D.K. (1968). The collateral system of the medial nucleus of the trapczoid body of the cat, its neuronal architecture and relation to the olivo-cochlear bundle. Brain Research 9, 288–311.CrossRefGoogle Scholar
Perry, V.H. & Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683–685.CrossRefGoogle ScholarPubMed
Perry, V.H., Henderson, Z. & Linden, R. (1983). Postnatal changes in retinal ganglion cell and optic axon populations in the pigmented rat. Journal of Comparative Neurology 219, 356–370.CrossRefGoogle ScholarPubMed
Provis, J.M. & Penfold, P.L. (1988). Cell death and the elimination of retinal axons during development. Progress in Neurobiology 31, 331–347.CrossRefGoogle ScholarPubMed
Purves, D. & Lichtman, J.N. (1985). Principles of Neural Development. Sunderland, Massachusetts: Sinauer Associates, Inc., pp. 155–178.Google Scholar
Purves, D., Snider, W.D. & Voyvodic, J.T. (1988). Trophic regulation of nerve cell morphology and innervation in the autonomie nervous system. Nature 336, 123–128.CrossRefGoogle Scholar
Ramoa, A.S., Campbell, G. & Shatz, C.J. (1988). Dendritic growth and remodeling of cat retinal ganglion cells during fetal and postnatal development. Journal of Neuroscience 8, 4239–4261.CrossRefGoogle ScholarPubMed
Ramoa, A.S. & Yamasaki, E.N. (1996). Transient retinal ganglion cells in the developing rat are characterized by specific morphological propertics. Journal of Comparative Neurology 368, 582–596.3.0.CO;2-0>CrossRefGoogle Scholar
Ramon Y Cajal, S. (1909). Histologie du systeme nerveux de l'homme et des vertebres, Vol. I (second reprint). Madrid: Institut Ramon y Cajal, pp. 754–838.Google Scholar
Sakaguchi, D.S. (1989). The development of retinal ganglion cells deprived of their targets. Developmental Biology 134, 103–111.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1983). The prenatal development of the cat's retinogeniculate pathway. Journal of Neuroscience 3, 482–499.CrossRefGoogle ScholarPubMed
Shatz, C.J. & Kirkwood, P.A. (1984). Prenatal development of junctional connections in the cat's retinogeniculate pathway. Journal of Neuroscience 4, 1378–1397.CrossRefGoogle Scholar
Shatz, C.J. & Stryker, M.P. (1988). Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242, 87–89.CrossRefGoogle ScholarPubMed
Skaliora, I., Scobey, R.P. & Chalupa, L.M. (1993). Prenatal development of excitability in cat retinal ganglion cells: Action potentials and sodium currents. Journal of Neuroscience 13, 313–323.CrossRefGoogle ScholarPubMed
Sretavan, D.W., Shatz, C.J. & Stryker, M.P. (1988). Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336, 468–471.CrossRefGoogle ScholarPubMed
Thoenen, H., Otten, U. & Schwab, M. (1979). Orthograde and retrograde signals for the regulation of gene expression: The peripheral sympathetic nervous system as a model. In The Neurosciences, 4th Study Program, ed. Schmitt, P.O. & Worden, F.G., pp. 911–928. Cambridge, Massachusetts: MIT Press.Google Scholar
Williams, R.W., Bastiani, M.J. & Chalupa, L.M. (1983). Loss of axons in the cat optic nerve following fetal unilateral enucleation: An electron microscopic analysis. Journal of Neuroscience 3, 133–144.CrossRefGoogle ScholarPubMed
Williams, R.W., Bastiani, M.J., Lia, B. & Chalupa, L.M. (1986). Growth cones, dying axons, and developmental fluctuations in the fiber population of the cat's optic nerve. Journal of Comparative Neurology 246, 32–69.CrossRefGoogle ScholarPubMed
Wingate, R.J.T. & Thompson, I.D. (1995 a). Axonal target choice and dendritic development of ferret beta retinal ganglion cells. European Journal of Neuroscience 7, 723–731.CrossRefGoogle ScholarPubMed
Wingate, R.J.T. & Thompson, I.D. (1995 b). Targeting and activity-related dendritic modification in mammalian retinal ganglion cells. Journal of Neuroscience 14, 6621–6637.CrossRefGoogle Scholar
Wong, R.O.L., Herrmann, K. & Shatz, C.J. (1991). Remodeling of retinal ganglion cell dendrites in the absence of action potential activity. Journal of Neurobiology 22, 685–697.CrossRefGoogle ScholarPubMed
Yamasaki, E.N. & Ramoa, A.S. (1993). Dendritic remodelling of retinal ganglion cells during development of the rat. Journal of Comparative Neurology 329, 277–289.CrossRefGoogle ScholarPubMed