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Severity of ganglion cell death during early postnatal development is modulated by both neuronal activity and binocular competition

Published online by Cambridge University Press:  02 June 2009

A.J. Scheetz ,
Robert W. Williams  and
Mark W. Dubin
A.J. Scheetz
Affiliation:
University of Colorado at Boulder, Department of Psychology, Boulder
Robert W. Williams
Affiliation:
University of Tennessee, College of Medicine, Memphis
Mark W. Dubin
Affiliation:
University of Colorado at Boulder, Department of Biology, Boulder
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Abstract

The influence of postnatal neuronal activity on the magnitude of retinal ganglion cell death has been studied in cats. A constant blockade of activity in one eye starting just after birth does not change the severity of naturally occurring ganglion cell death, and as in normal animals, the ganglion cell population declines from 250,000 to 160,000 over a 4- to 6-week period. However, the population of retinal ganglion cells in the active untreated eye of monocularly deprived cats is increased 12% above normal (180,000 vs. 160,000 in each of four cases). This increase of 20,000 cells is permanent, and presumably reflects the competitive advantage in their target nuclei that the still active axons have over their silenced companions from the treated eye. Surprisingly, in one animal treated successfully for long duration with TTX in both eyes, the population of ganglion cells was elevated in both eyes (200,000 and 208,000 ganglion cells). This increase matches that achieved by early unilateral enucleation (Williams et al., 1983). Our results demonstrate that the complete blockade of activity reduces the severity of naturally occurring cell death in a population of CNS sensory neurons. The effects of unilateral blockade emphasize that the activity-dependent modulation of neuron death only occurs under conditions that do not place the inactive population of neurons at a competitive disadvantage.

Keywords

Neuronal activityRetinal ganglion cellCell deathVisual system development
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 4 , July 1995 , pp. 605 - 610
Copyright
Copyright © Cambridge University Press 1995

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References

Archer, S.M., Dubin, M.W. & Stark, L.A. (1982). Abnormal retinogeniculate connectivity in the absence of action potentials. Science 217, 743–745.CrossRefGoogle ScholarPubMed
Chalupa, L.M. & Williams, R.W. (1984). Organization of the cat's lateral geniculate nucleus following interruption of prenatal binocular competition. Human Neurobiology 3, 103–107.Google ScholarPubMed
Cowan, W.M., Fawcett, J.W., O'Leary, D.D.M. & Stanfield, B.B. (1984). Regressive events in neurogenesis. Science 225, 1258–1265.CrossRefGoogle ScholarPubMed
Dubin, M.W., Stark, L.A. & Archer, S.M. (1986). A role for actionpotential activity in the development of neuronal connections in the kitten retinogeniculate pathway. Journal of Neuroscience 6, 1021–1036.CrossRefGoogle ScholarPubMed
Fawcett, J.W., O'Leary, D.D.M. & Cowan, W.M. (1984). Activity and the control of ganglion cell death in the rat retina. Proceedings of the National Academy of Sciences of the U.S.A. 81, 5589–5593.CrossRefGoogle ScholarPubMed
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-Resta, L. & Resta, G. (1992). A quantitative model for the regulation of naturally occurring cell death in the developing vertebrate nervous system. Journal of Neuroscience 12, 4586–4594.CrossRefGoogle ScholarPubMed
Geisert, E.E., Langsetmo, A. & Spear, P.D. (1981). Influence of cortico-geniculate pathway on response properties of cat lateral geniculate neurons. Brain Research 208, 409–415.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Schall, J.D., Ault, S.J., Provis, J.M. & Vitek, D. (1988). Class-specific cell death shapes the distribution and pattern of central projection cat retinal ganglion cells. Journal of Neuroscience 8, 2011–2027.CrossRefGoogle ScholarPubMed
Lia, B., Williams, R.W. & Chalupa, L.M. (1986). Does axonal branching contribute to overproduction of optic nerve fibers during early development of the cat's visual system. Developmental Brain Research 25, 296–301.CrossRefGoogle Scholar
Linden, R. & Perry, V.H. (1982). Ganglion cell death within the developing retina: A regulatory role for retinal dendrites. Neuroscience 7, 2813–2827.CrossRefGoogle ScholarPubMed
Lipton, S.A. (1986). Blockade of electrical activity promotes the death of mammalian retinal ganglion cells in culture. Proceedings of the National Academy of Sciences of the U.S.A. 83, 9774–9778.CrossRefGoogle ScholarPubMed
Oppenheim, R.W. (1991). Cell death during development of the nervous system. Annual Review of Neuroscience 14, 453–501.CrossRefGoogle ScholarPubMed
Perry, V.H. & Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683–685.CrossRefGoogle ScholarPubMed
Provis, J.M., van Driel, D., Billson, F.A. & Russell, P. (1985). Human fetal optic nerve: Overproduction and elimination of retinal axons during development. Journal of Comparative Neurology 238, 92–101.CrossRefGoogle ScholarPubMed
Rakic, P. (1981). Development of visual centers in the primate brain depends on binocular competition before birth. Science 214, 928–931.CrossRefGoogle ScholarPubMed
Rakic, P. & Riley, K.P. (1983). Regulation of axon number in primate optic nerve by prenatal binocular competition. Nature 305, 135–137.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1983). The prenatal development of the cat's retinogeniculate pathway. Journal of Neuroscience 3, 482–499.CrossRefGoogle ScholarPubMed
Shook, B.L. & Chalupa, L.M. (1986). Organization of geniculocortical connections following prenatal interruption of binocular interactions. Developmental Brain Research 28, 47–62.CrossRefGoogle Scholar
Stone, J. (1983). The Classification of Retinal Ganglion Cells and Its Impact on the Neurobiology of Vision. Parallel Processing in the Visual System. New York, Plenum Press, pp. 33–81.Google Scholar
Wiesel, T.N. & Hubel, D.H. (1965). Extent of recovery from the effects of visual deprivation in kittens. Journal of Neurophysiology 28, 1060–1072.CrossRefGoogle ScholarPubMed
Williams, R.W., Bastiani, M.J. & Chalupa, L.M. (1983). Loss of axons in the cat optic nerve following fetal 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
Williams, R.W., Cavada, C. & Reinoso-Suarez, F. (1993). Rapid evolution of the visual system: A cellular assay of the retina and dorsal lateral geniculate nucleus of the Spanish wildcat and domestic cat. Journal of Neuroscience 13, 208–228.CrossRefGoogle ScholarPubMed
Williams, R.W. & Chalupa, L.M. (1983). An analysis of axon caliber within the optic nerve of the cat: Evidence of size groupings and regional organization. Journal of Neuroscience 3, 1554–1564.CrossRefGoogle ScholarPubMed
Williams, R.W. & Herrup, K. (1988). The control of neuron number. Annual Review of Neuroscience 11, 423–453.CrossRefGoogle ScholarPubMed