Summary
Counts of neurons of the rat superior cervical ganglion (SCG) were made at two days before birth and at several postnatal ages. There is a significant decline in the number of apparently normal neurons over the first postnatal week, with the number falling from 39 500 at 3 days to 26 500 at 7 days. Cell numbers then remained constant up to day 60 when the number of neurons was 27 500. The incidence of degenerating neurons, identified by light and electron microscopy, was correlated temporally with the loss of normal neurons. The early manifestations of the neuron degeneration were chromatin clumping and the presence of free monoribosomes. Later stages were characterized by increased chromatin clumping, dense aggregations of monoribosomes, numerous intracytoplasmic vacuoles, and only short segments of rough endoplasmic reticulum. The ultrastructure of the majority of these dying neurons is similar to the ‘nuclear’ types of degeneration described by Pilar & Landmesser (1976) and Chu-Wang & Oppenheim (1978). Based on the presence of degenerating neurons coincident with the reduction in neuron numbers, we conclude that neuron death is an important aspect of early postnatal development in the rat SCG.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Abercrombie, M. (1946) Estimation of nuclear population from microtome sections.Anatomical Record 94, 239–47.
Black, I. B. &Geen, S. C. (1974) Inhibition of the biochemistry and morphological maturation of adrenergic neurons by nicotinic receptor blockage.Journal of Neurochemistry 22, 301–6.
Black, I., Hendry, I. A. &Iversen, L. L. (1971) Transsynaptic regulation of growth and development of adrenergic neurons in a mouse sympathetic ganglion.Brain Research 34, 229–40.
Black, I. B., Hendry, I. A. &Iversen, L. L. (1972) Effects of surgical decentralization and Nerve Growth Factor on the maturation of adrenergic neurons in a mouse sympathetic ganglion.Journal of Neurochemistry 19, 1367–77.
Black, I. B., Joh, T. H. &Reid, D. J. (1974) Accumulation of tyrosine hydroxylase molecules during growth and development of the superior cervical ganglion.Brain Research 74, 133–44.
Cammermeyer, J. (1978) Is the solitary dark neuron a manifestation of postmortem trauma to the brain inadequately fixed by perfusion?Histochemistry 56, 97–115.
Carr, V. M. &Simpson, S. G. (1978) Proliferative and degenerative events in the early development of chick dorsal root ganglia.Journal of Comparative Neurology 182, 727–40.
Chu-Wang, I. W. &Oppenheim, R. W. (1978) Cell death of motoneurons in the chick embryo spinal cord. I. A light and electron microscopic study of naturally occurring and induced cell loss during development.Journal of Comparative Neurology 177, 33–58.
Cunningham, T. J. (1982) Naturally occurring neuron death and its regulation by developing neural pathways.International Review of Cytology 74, 163–85.
Cunningham, T. J., Mohler, I. M. &Giordano, D. (1981) Naturally occurring neuron death in the ganglion cell layer of the neonatal rat: Morphology and evidence for regional correspondence with neuron death in superior colliculus.Developmental Brain Research 2, 203–15.
Davies, D. C. (1978) Neuronal numbers in the superior cervical ganglion of the neonatal rat.Journal of Anatomy 127, 43–51.
Dechamplain, J., Malmfors, T., Olsen, L. &Sachs, C. (1970) Ontogenesis of peripheral adrenergic neurons in the rat: Pre- and postnatal observations.Acta physiologica scandinavica 80, 276–88.
Eränko, O. &Soinila, S. (1981) Effect of early postnatal division of the postganglionic nerves on the development of principal cells and small intensely fluorescent cells in the rat superior cervical ganglion.Journal of Neurocytology 10, 1–18.
Giordano, D. L. &Cunningham, T. J. (1982) Effects of deafferentation on neuron death in the superior colliculus.Developmental Brain Research 4, 365–8.
Giordano, D. L., Murray, M. &Cunningham, T. J. (1980) Naturally occurring neuron death in the optic layers of superior colliculus of the postnatal rat.Journal of Neurocytology 9, 603–14.
Hamburger, V., Brunso-Bechtold, J. K. &Yip, J. W. (1981) Neuronal death in the spinal ganglia of the chick embryo and its reduction by nerve growth factor.Journal of Neuroscience 1, 60–71.
Henry, I. A. (1976) A method to correct adequately for the change in neuronal size when estimating neuronal numbers after nerve growth factor treatment.Journal of Neurocytology 5, 337–49.
Hendry, I. A. (1977) Cell division in the developing sympathetic nervous system.Journal of Neurocytology 6, 299–309.
Hendry, I. A. &Campbell, J. (1976) Morphometric analysis of rat superior cervical and ganglion after axotomy and NGF treatment.Journal of Neurocytology 5, 351–60.
Hughes, W. F. &McLoon, S. C. (1979) Ganglion cell death during normal retinal development in the chick: Comparisons with cell death induced by early target field destruction.Experimental Neurology 66, 587–601.
Levi-Montalcini, R. (1966) The nerve growth factor: Its mode of action on sensory and sympathetic nerve cells.Harvey Lectures 60, 217–59.
Levi-Montalcini, R. &Booker, B. (1960) Excessive growth of the sympathetic ganglia evoked by a protein isolated from mouse salivary glands.Proceedings of the National Academy of Sciences USA 46, 373–84.
Oppenheim, R. W. (1981) Neuronal cell death and some related regressive phenomena during neurogenesis: A selective historical review and progress report. InStudies in Development Neurobiology: Essays in Honor of Viktor Hamburger, (edited byW. M. Cowan). Oxford: Oxford University Press.
Owman, C., Sjoberg, N. O. &Swedin, G. (1971) Histochemical and chemical studies on pre- and postnatal development of the different system of ‘short’ and ‘long’ adrenergic neurons in peripheral organs of the rat.Zeitschrift für Zellforschung und mikroskopische Anatomie 116, 319–41.
Pannese, E. (1976) An electron microscopic study of cell degeneration in chick embryo spinal ganglia.Neuropathology and Applied Neurobiology 2, 247–67.
Papka, R. E. (1972) Ultrastructural and fluorescence histochemical studies of developing sympathetic ganglion in the rabbit.American Journal of Anatomy 134, 337–64.
Pilar, G. &Landmesser, L. (1976) Ultrastructural differences during embryonic neuron death in normal and peripherally deprived ciliary ganglia.Journal of Cell Biology 68, 339–56.
Sohal, G. S. &Weidman, T. A. (1978) Ultrastructural sequence of embryonic cell death in normal and peripherally deprived trochlear nucleus.Experimental Neurology 61, 53–64.
Smolen, A. J. &Raisman, G. (1980) Synapse formation in the rat superior cervical ganglion during normal development and after neonatal deafferentation.Brain Research 181, 315–23.
Smolen, A. J., Wright, L. L. &Cunningham, T. J. (1983) Neuron numbers in the superior cervical ganglion of the rat: A critical comparison of methods for cell counting.Journal of Neurocytology 12, 739–750.
Smith, P., Slotkin, T. &Mills, E. (1982) Development of sympathetic ganglionic neurotransmition in the neonatal rat. Pre- and postganglionic nerve response to asyphyxia and 2-deoxyglucose.Neuroscience 7, 501–7.
Thoenen, H., Saner, A., Angeletti, P. U. &Levi-Montalcini, R. (1972) Increased activity of choline acetyltransferase in sympathetic ganglia after prolonged administration of Nerve Growth Factor.Nature New Biology 236, 26–8.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wright, L.L., Cunningham, T.J. & Smolen, A.J. Developmental neuron death in the rat superior cervical sympathetic ganglion: cell counts and ultrastructure. J Neurocytol 12, 727–738 (1983). https://doi.org/10.1007/BF01258147
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01258147