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Mature, growing ganglion cells acquire new synapses in the retina of the goldfish

Published online by Cambridge University Press:  02 June 2009

Peter F. Hitchcock
Peter F. Hitchcock
Affiliation:
Departments of Ophthalmology and Anatomy and Cell Biology, The University of Michigan School of Medicine, Ann Arbor
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Abstract

The goldfish retina grows throughout the animal’s life, primarily by a balloon-like expansion. With this expansion, dendritic arbors of ganglion cells show scaled growth; arbors increase in size from small to large with no change in their architecture (Hitchcock & Easter, 1986; Bloomfield & Hitchcock, 1991). The study reported here showed that ganglion cell arbors acquire new synapses with this growth. Arbors from a single type of ganglion cell in retinas of small, young and large, old fish were intracellularly filled with horseradish peroxidase, examined electron microscopically, and the synapses contacting them counted and compared (small arbors vs. large arbors). The small and large arbors had similar numbers and orders of dendritic branches (i.e. similar architectures), but the large arbors were significantly larger than the small ones. The increase in arbor size was correlated with a 2.7x and 1.9x increase in the number of ribbon and conventional synaptic contacts, respectively. The addition of new synapses is proposed as a mechanism by which the signaling properties of the enlarging ganglion cells can remain constant.

Keywords

SynapseDendritic arborsHorseradish peroxidaseElectron microscopyIntracellular injectionSynaptic integrationInput resistance
Type
Research Article
Information
Visual Neuroscience , Volume 10 , Issue 2 , March 1993 , pp. 219 - 224
Copyright
Copyright © Cambridge University Press 1993

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References

Adams, J.C. (1977). Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience 2, 141–145CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Hitchcock, P.F. (1991). Dendritic arbors of large-field ganglion cells show scaled growth during expansion of the goldfish retina. Journal of Neuroscience 11, 910–917CrossRefGoogle ScholarPubMed
Brown, R.N. Jr. & Hitchcock, P.F. (1989). Dendritic growth of DAPI-accumulating amacrine cells in the retina of the goldfish. DevelopmentalBrain Research 50, 123–128Google ScholarPubMed
Chung, S.H., Stirling, R.V. & Gaze, R.M. (1975). The structural and functional development of the retina in larval Xenopus. Journal of Embryology and Experimental Morphology 33, 915–940Google Scholar
Cook, J.E., Becker, D.L. & Kapila, R. (1992). Independent mosaics of large inner- and outer-stratified ganglion cells in the goldfish retina. Journal of Comparative Neurology 318, 355–366CrossRefGoogle ScholarPubMed
Dubin, M. (1970). The inner plexiform layer of the vertebrate retina: A quantitative and comparative electron microscopic analysis. Journal of Comparative Neurology 140, 479–506Google Scholar
Fisher, L.J. (1972). Changes during maturation and metamorphosis in the synaptic organization of the tadpole inner plexiform layer. Nature 235, 391–393Google Scholar
Fisher, L.J. (1976). Synaptic arrays of the inner plexiform layer in the developing retina of Xenopus. Developmental Biology 50, 402–412CrossRefGoogle ScholarPubMed
Fisher, L.J. & Easter, S.S. Jr. (1979). Retinal synaptic arrays: Continuing development in the adult goldfish. Journal of Comparative Neurology 185, 373–379CrossRefGoogle ScholarPubMed
Frank, B.D. & Hollyfield, J.G. (1987). Retina of the tadpole and frog: Delayed dendritic development in a subpopulation of ganglion cells coincident with metamorphosis. Journal of Comparative Neurology 266, 435–444Google Scholar
Harris, J.B. & Ribchester, R.R. (1979). The relationship between end-plate size and transmitter release in normal and dystrophic muscles of the mouse. Journal of Physiology 296, 245–265Google Scholar
Hitchcock, P.F. (1987). Constant dendritic coverage by ganglion cells with growth of the goldfish’s retina. Vision Research 27, 17–22CrossRefGoogle ScholarPubMed
Hitchcock, P.F. (1989 a). Exclusionary dendritic interactions in the retina of the goldfish. Development 106, 589–598Google Scholar
Hitchcock, P.F. (1989 b). Morphology and distribution of synapses onto a type of large field ganglion cell in the retina of the goldfish. Journal of Comparative Neurology 283, 177–188Google Scholar
Hitchcock, P.F. (1991). Synaptic contacts increase as mature dendrites grow in the retina of the goldfish. Neuroscience Abstracts 561, 17.Google Scholar
Hitchcock, P.F. & Easter, S.S. Jr., (1986). Retinal ganglion cells in goldfish: A qualitative classification into four morphological types, and a quantitative study of the development of one of them. Journal of Neuroscience 6, 1037–1050Google Scholar
Johns, P.R. (1977). Growth of the adult goldfish eye, III. Source of new retinal cells. Journal of Comparative Neurology 176, 343–358Google Scholar
Johns, P.R. (1982). Formation of photoreceptors in larval and adult goldfish. Journal of Neuroscience 2, 178–198Google Scholar
Johns, P.R. & Easter, S.S. Jr., (1977). Growth of the adult goldfish eye, II. Increase in retinal cell number. Journal of Comparative Neurology 176, 331–342Google Scholar
Kock, J.-H. (1982 a). Neuronal addition and retinal expansion during growth of the crucian carp. Journal of Comparative Neurology 209, 264–274Google Scholar
Kock, J.-H. (1982 b). Dendritic tree structure and dendritic hypertrophy during growth of the crucian carp eye. Journal of Comparative Neurology 209, 275–286Google Scholar
Kock, J.-H. & Stell, W.K. (1985). Formation of new rod photoreceptor synapses onto differentiated bipolar cells in goldfish retina. Anatomical Record 211, 69–74CrossRefGoogle ScholarPubMed
Kuno, M., Turkanis, S.A. & Weakly, J.N. (1971). Correlation between nerve terminal size and transmitter releaseat the neuromus-cular junction of the frog. Journal of Physiology 213, 545–556Google Scholar
Krauth, J. (1983).The interpretation of significance tests for independent and dependent samples. Journal of Neuroscience Methods 9, 269–281Google Scholar
Nicol, D. & Meinertzhagen, I.A. (1982). Regulation in the number of fly photoreceptor synapses: The effects of alterations in the number of presynaptic cells. Journal of Comparative Neurology 207, 45–60CrossRefGoogle ScholarPubMed
Pomeranz, B. (1972). Metamorphosis of frog vision: Changes in ganglion cell physiology and anatomy. Experimental Neurology 34, 187–199Google Scholar
Pomeranz, B. & Chung, S.H. (1970). Dendritic-tree anatomy codes for-vision physiology in tadpole retina. Science 170, 983–984CrossRefGoogle Scholar
Purves, D. & Hume, R.I. (1981). The relation of postsynaptic geometry to the number of presynaptic axons that innervate autonomic ganglion cells. Journal of Neuroscience 1, 441–452Google Scholar
Raymond, P.A. (1985). The unique origin of rod photoreceptors in the teleost retina. Trends in Neuroscience 8, 12–17CrossRefGoogle Scholar
Raymond, P.A. (1990). Horizontal cell axon terminals in growing goldfish. Experimental Eye Research 51, 675–683Google Scholar
Sakaguchi, D.S., Murphey, R.K., Hunt, R.K. & Tompktns, R. (1984). The development of retinal ganglion cells in a tetraploid strain of Xenopus laevis: A morphological study utilizing intracellular dye injection. Journal of Comparative Neurology 224, 231–251Google Scholar
Sargent, P.B. (1983). The number of synaptic boutons terminating on Xenopus cardiac ganglion cells is directly correlated with cell size. Journal of Physiology 343, 85–104Google Scholar