Summary
The aim of this study was to investigate age-related changes in preganglionic neurons of the lumbar and sacral spinal cord of the male rat that may underlie impaired control of the urogenital system in old age. Preganglionic sympathetic and parasympathetic neurons of 4- and 24-month-old rats were identified by retrograde axonal tracing with cholera toxin subunit-B followed by immunocytochemistry. Labelled preganglionic neurons were scanned on the confocal microscope. Measurements were made of soma area, number of primary dendrites, number of dendritic branch points and total dendritic length. there were significant decreases in the number of dendritic branch points and total dendritic length of sympathetic preganglionic neurons in the aged rats compared to the adult group. The soma area and number of primary dendrites were not significantly different. Some cells exhibited signs of degeneration, such as swelling of the soma and distension of the proximal part of primary dendrites. No significant differences were found in any of the parameters measured for the parasympathetic neurons. The changes in dendritic morphology of sympathetic preganglionic neurons may reflect altered central and peripheral control of pelvic viscera in old age.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andrews, T. J., Li, D., Halliwell, J. &Cowen, T. (1994) The effect of age on dendrites in the rat superior cervical ganglion.Journal of Anatomy 184, 111–17.
Cabot, J. B. (1990) Sympathetic preganglionic neurons: cytoarchitecture, ultrastructure, and biophysical properties. InCentral Regulation of Autonomic Functions (edited byA. D. Loewy &K. M. Spyer), pp. 44–67. New York: Oxford University Press.
Chun, A. L., Wallace, L. J., Gerald, M. C., Levin, R. M. &Wein, A. J. (1988) Effect of age onin vivo urinary bladder function in the rat.Journal of Urology 139, 625–7.
Cowen, T. (1993). Ageing in the autonomic nervous system: a result of nerve-target interactions? A review.Mechanisms of Ageing and Development 68, 163–73.
Crutcher, K. A. (1990) Age-related decrease in sympathetic sprouting is primarily due to decreased target receptivity: implications for understanding brain aging.Neurobiology of Ageing 11, 175–83.
De Groat, W. C. (1990). Central neural control of the lower urinary tract. InNeurobiology of Incontinence. Ciba Foundation Symposium, Vol. 151 (edited byBock, G. &Whelan, J.) pp. 27–56. Chichester: Wiley.
De Groat, W. C. &Booth, A. M. (1980) Inhibition and facilitation in parasympathetic ganglia.Federation Proceedings 39, 2990–6.
De Groat, W. C. &Lalley, P. M. (1972) Reflex firing in the lumbar sympathetic outflow to activation of vesical afferent fibers.Journal of Physiology 226, 289–309.
De Groat, W. C. &Steers, W. D. (1990) Autonomic Regulation of the Urinary Bladder and Sexual Organs. InCentral Regulation of Autonomic Functions (edited byA. D. Loewy &K. M. Spyer), pp. 310–33. New York: Oxford University Press.
Donovan, M. K., Winternitz, S. R. &Wyss, J. M. (1983). An analysis of the sensory innervation of the urinary system in the rat.Brain Research Bulletin 11, 321–4.
Gavazzi, I. (1995). Collateral sprouting and responsiveness to nerve growth factor of ageing neurons.Neuroscience Letters 189, 47–50.
Gavazzi, I. &Cowen, T. (1993). Axonal regeneration from transplanted sympathetic ganglia is not impaired by age.Experimental Neurology 122, 57–64.
Gavazzi, I., Andrews, T. J., Thrasivoulou, C. &Cowen, T. (1992). Influence of target tissues on their innervation in old age: a transplantation study.NeuroReport 3, 717–20.
Gilpin, S. A., Gilpin, C. J., Dixon, J. S., Gosling, J. A. &Kirby, R. S. (1986). The effect of age on the autonomic innervation of the urinary bladder.British Journal of Urology 58, 378–81.
Hancock, M. B. &Peveto, C. A. (1979). A preganglionic autonomic nucleus in the dorsal gray commissure of the lumbar spinal cord of the rat.Journal of Comparative Neurology 183, 65–72.
Hendry, I. A. &Hill, C. E. (1980). Retrograde axonal transport of target tissue-derived macromolecules.Nature 287, 647–9.
Hotta, H., Morrison, J. F. B., Sato, A. &Uchida, S. (1995). The effects of aging on the rat bladder and its innervation.Japanese Journal of Physiology 45, 823–36.
Italiano, G., Calabrò, A., Artibani, W., Cisternino, A., Oliva, G. &Pagano, F. (1995). Bladder function in the aged rat: a functional and morphological study.European Urology 27, 232–5.
Jenner, C. S., Gavazzi, I., Song, G. X. &Cowen, T. (1994). Loss of responsiveness of ageing sympathetic neuronesin vitro to laminin and NGF.European Journal of Neuroscience (Suppl. 7), 185.
Kinder, M. V., Bastiaanssen, E. H. C., Janknegt, R. A. &Marani, E. (1995). Neuronal circuitry of the lower urinary tract; central and peripheral neuronal control of the micturition cycle.Anatomy and Embryology 192, 195–209.
Koistinaho, J. (1986). Difference in the age-related accumulation of lipopigments in the adrenergic and noradrenergic peripheral neurons in the male rat.Gerontology 32, 300–7.
Langworthy, O. R. (1965). Innervation of the pelvic organs of the rat.Investigative Urology 2, 491–511.
Malone-lee, J. (1994). Lower urinary tract function in later life. InHandbook of Neuro-urology (edited byRushton, D. N.) pp. 349–68. New York: Marcel Dekker, Inc.
Masih, M. A., Santer, R. M. &Watson, A. H. D. (1995). The use of confocal microscopy to investigate age-related changes in preganglionic neurons projecting to the rat hypogastric ganglion.Clinical Autonomic Research 5, 348.
Njå, A. &Purves, D. (1978). The effects of nerve growth factor and its antiserum on synapses in the superior cervical ganglion of the guinea-pig.Journal of Physiology 277, 53–75.
Peters, A., Palay, S. L. &Webster, HDEF. (1991).The fine Structure of the Nervous System: Neurons and their Supporting Cells, 3rd Ed. New York: Oxford University Press.
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, 441–52.
Ruit, K. G., Osbourne, P. A., Schmidt, R. E., Johnson Jr, E. M. &Snider, W. D. (1990). Nerve growth factor regulates sympathetic ganglion cell morphology and survival in the adult mouse.Journal of Neuroscience 10, 2412–19.
Schwab, M. E. &Thoenen, H. (1977). Selective trans-synaptic migration of tetanus toxin after retrograde axonal transport in peripheral sympathetic rierves: a comparison with nerve growth factor.Brain Research 122, 459–74.
Su, H. C., Wharton, J., Polak, J. M., Mulderry, P. K., Ghatei, M. A., Gibson, S. J., Terenghi, G., Morrison, J. F. B., Ballesta, J. &Bloom, S. R. (1986). CGRP-immunoreactivity in aggerent neurons supplying the urinary tract: combined retrograde tracing and immunohistochemistry.Neuroscience 18, 727–47.
Vera, P. L. &Nadelhaft, I. (1992). Afferent and sympathetic innervation of the dome and the base of the urinary bladder of the female rat.Brain Research Bulletin 29, 651–8.
Voyvodic, J. T. (1987). Development and regulation of dendrites in the rat superior cervical ganglion.Journal of Neuroscience 7, 904–12.
Warburton, A. L. &Santer, R. M. (1993). Localisation of NADPH-diaphorase and acetylcholinesterase activities and of tyrosine hydroxylase and neuropeptide-Y immunoreactivity in neurons of the hypogastric ganglion of young adult and aged rats.Journal of the Autonomic Nervous System 45, 155–63.
Warburton, A. L. &Santer, R. M. (1994). Sympathetic and sensory innervation of the urinary tract in young adult and aged rats: a semi-quantitative histochemical and immunohistochemical study.Histochemical Journal 26, 127–33.
Warburton, A. L. &Santer, R. M. (1995). Decrease in synapsin I staining in the hypogastric ganglion of aged rats.Neuroscience Letters 194, 157–60.
Yawo, H. (1987). Changes in the dendritic geometry of mouse superior cervical ganglion cells following postganglionic axotomy.Journal of Neuroscience 7, 3703–11.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Dering, M.A., Santer, R.M. & Watson, A.H.D. Age-related changes in the morphology of preganglionic neurons projecting to the rat hypogastric ganglion. J Neurocytol 25, 555–563 (1996). https://doi.org/10.1007/BF02284823
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02284823