Summary
An experimental procedure which chronically reduces the lumen of the urethra in adult female rats produced distension of the bladder and conspicuous thickening of its wall, resulting within 6–8 weeks in a ten-fold increase in muscle weight (muscle hypertrophy). During this process, the neurons in the pelvic ganglion that innervate the bladder undergo a large increase in size (neuronal hypertrophy). The average neuronal volume increased by 83%; small neurons became less numerous and large neurons became more numerous than in controls, but there was no increase in the maximum neuronal size. Six weeks after re-operation and removal of the urethral obstruction, the weight of the bladder was reduced (although not quite to the control levels), while the average neuronal size reversed to values very close to controls.
In separate experiments, the pelvic ganglion of one side was removed. The nerve fibres in the hemidenervated bladder sprouted, grew and spread to innervate the whole bladder. The neurons in the surviving pelvic ganglion hypertrophied, the average cell volume increasing by 50% in seven weeks.
The experiments showed that: (i) the pelvic neurons of adult rats are capable of very extensive growth when the tissue they innervate (bladder muscle) undergoes hypertrophy; (ii) the neuronal hypertrophy is reversible. This was taken to imply that there are factors within the bladder, including trophic substances, that regulate nerve cell volume not only by inducing growth but also by inducing the opposite effect, a cell size reduction; (iii) unilateral ganglionectomy, which did not induce muscle hypertrophy but doubled the amount of muscle innervated by the contralateral ganglion, was followed by marked neuronal hypertrophy.
Similar content being viewed by others
References
Ambrosi, F. (1942) Sulle alterazioni istologiche dei gangli e dei nervi del tubo digerente nella occlusione interstinale. Ricerche nell'uomo e sperimentali.Archivio De Vecchi di Anatomia Patologica 5, 215–40.
Baljet, B. &Drukker, J. (1980) The extrinsic innervation of the pelvic organs in the female rat.Acta Anatomica 107, 241–67.
Banns, H., Ekström, J. &Mann, S. P. (1980) Recovery of choline acetyltransferase activity in the rat urinary bladder deprived of half its innervation.Acta Physiologica Scandinavica 109, 85–8.
Benninghoff, A. (1951) Vermehrung und Vergrösserung von Nervezellen bei Hypertrophie des Innervationsgebietes.Zeitschrift für Naturforschung 6b, 38–41.
Coggeshall, R. E. (1992) A consideration of neural counting methods.Trends in Neurosciences 15, 9–13.
Collins, F. &Dawson, A. (1983) An effect of nerve growth factor on parasympathetic neurite outgrowth.Proceeding of the National Academy of Sciences (SA) 80, 2091–4.
Dail, W. G., Evan, A. P. Jr. &Eason, H. R. (1975) The major ganglion in the pelvic plexus of the male rat.Cell and Tissue Research 159, 49–62.
Ekström, J., Malmberg, L. &Öberg, S. (1986) Unilateral denervation of the rat urinary bladder and reinnervation: a predominance for ipsilateral changes.Acta Physiologica, Scandinavica 127, 223–31.
Filogamo, G. &Marchisio, P. C. (1970) Choline acetyltransferase activity of rabbit ileum wall. The effect of extrinsic and intrinsic denervation and of combined experimental hypertrophy.Archives Internationales de Physiologie et de Biochimie 78, 141–51.
Filogamo, G. &Vigliani, F. (1954) Ricerche sperimentali sulla corelazione tra estensione del territorio di innervazione e grandezza e numero delle cellule gangliari del plesso mienterico (di Auerbach), nel cane.Rivista di Patologia Nervosa e Mentale 75, 441–62.
Gabella, G. (1984) Size of neurons and glial cells in the intramural ganglia of the hypertrophic intestine of the guinea-pig.Journal of Neurocytology 13, 73–84.
Gabella, G. (1990) Hypertrophy of visceral smooth muscle.Anatomy and Embryology 182, 409–24.
Gabella, G. &Uvelius, B. (1990) Urinary bladder of rat: fine structure of normal and hypertrophic musculature.Cell and Tissue Research 262, 67–79.
Gosling, J. A., Gilpin, S. A., Dixon, J. S. &Gilpin, C. J. (1986) Decrease in the autonomic innervation of human detrusor muscle in outflow obstruction.Journal of Urology 136, 501–4.
Goss, R. J. (1964)Adaptive Growth. London: Logos Press.
Greene, E. C. (1963)Anatomy of the Rat. New York: Hafner.
Greenwood, D., Coggeshall, R. E. &Hulsebosch, C. E. (1985) Sexual dimorphism in the numbers of neurons in the pelvic ganglia of adult rats.Brain Research 340, 160–2.
Kanerva, L. &Teräväinen, H. (1972) Electron microscopy of the paracervical (Frankenhäuser) ganglion of the adult rat.Zeitschrift für Zellforschung 129, 161–77.
Levi, G. (1925) Wachstum und Körpergrösse. Die strukturelle Grundlage der Körpergrösse bei vollausgebildeten und im Wachstum begriffen Tieren.Ergebnisse der Anatomie und Entwicklungsgeschichte 26, 87–341.
Levi-Montalcini, R. &Calissano, P. (1966) The nerve-growth factor.Scientific American 240, (6), 68–77.
Lindner, P., Mattiasson, A., Persson, L. &Uvelius, B. (1988) Reversibility of detrusor hypertrophy and hyperplasia after removal of infravescical outflow obstruction in the rat.Journal of Urology 140, 642–6.
Mattiasson, A., Ekström, J., Larsson, B. &Uvelius, B. (1987) Changes in the nervous control of the rat urinary bladder induced by outflow obstruction.Neurourology and Urodynamics 6, 37–45.
Mattiasson, A. &Uvelius, B. (1982) Changes in contractile properties in hypertrophic urinary bladder.Journal of Urology 128, 1340–2.
Purves, D. (1988)Body and Brain: A Trophic Theory of Neural Connections. Cambridge, MA: Harvard University Press.
Purves, D., Snider, W. D. &Voyvodic, J. T. (1988) Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system.Nature 336, 123–8.
Ruit, K. G., Osborne, P. A., Schmidt, R. E., Johnson, 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.
Shimizu, T., Egan-Konopka, L. M., Ohta, Y. &Dun, N. J. (1982) Localization of postganglionic neurons to the male genital organ in the major pelvic ganglion of the rat.Tohoku Journal of Experimental Medicine 136, 351–4.
Sibley, G. N. A. (1985) An experimental model of detrusor instability in the obstructed pig.British Journal of Urology 57, 292–8.
Speakman, M. J., Brading, A. F., Gilpin, C. J., Dixon, J. S., Gilpin, S. A. &Gosling, J. A. (1987) Bladder outflow obstruction — a cause of denervation supersensitivity.Journal of Urology 138, 1461–6.
Steers, W. D. &De Groat, W. C. (1988) Effect of bladder outlet obstruction on micturition reflex pathways in the rat.Journal of Urology 140, 864–71.
Steers, W. D., Ciambotti, J., Erdman, S. &De Groat, W. C. (1990) Morphological plasticity in efferent pathways to the urinary bladder of the rat following urethral obstruction.Journal of Neuroscience 10, 1943–51.
Steers, W. D., Tuttle, J. B. &Creedon, D. J. (1989) Neurotrophic influence of the bladder following outlet obstruction: implications for the unstable detrusor (abstract).Neurourology and Urodynamics 8, 395–6.
Tabatabai, M., Booth, A. M. &De Groat, W. C. (1986) Morphological and electrophysiological properties of pelvic ganglion cells in the rat.Brain Research 382, 61–70.
Voyvodic, J. T. (1989) Peripheral target regulation of dendritic geometry in the superior cervical ganglion.Journal of Neuroscience 9, 1997–2010.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gabella, G., Berggren, T. & Uvelius, B. Hypertrophy and reversal of hypertrophy in rat pelvic ganglion neurons. J Neurocytol 21, 649–662 (1992). https://doi.org/10.1007/BF01191726
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01191726