Abstract
The effects of nerve stimulation on the electrical and mechanical activity of the smooth muscle of the proximal renal pelvis of the guinea-pig were investigated using standard tension and microelectrode recording techniques. Spontaneous action potentials were deemed to have been recorded from three cell types. (1) “pacemaker” cells (9 of >120) had membrane potentials (MPs) of -42.1±2.9 mV and fired action potentials of a simple waveform; (2) “driven” cells (>100) had more stable MPs of -56.1±1.2 mV (n=36) and more complex “ureter-like” action potentials; (3) the remaining cells had MPs of -45.5±1.7 mV (n=15) and action potentials with a waveform “intermediate” to groups (1) and (2). Nifedipine (0.1–1 μM) and Cd2+ (0.1–1 mM) blocked all spontaneous action potential discharge and depolarized the membrane to near -40 mV. Intramural nerve stimulation (10–50 Hz for 1–10 s) increased both the amplitude and frequency of the spontaneous contractile activity, this increase peaked in about 30 s and decayed slowly over several minutes Nerve stimulation depolarized pacemaker and driven cells 9.1±3.5 (n=3) and 1.6±0.7 (n=6) mV, respectively; the frequency of their action potential discharge increased from 7.6±2.7 and 9.9±1.1/min to 17.3±0.5 and 11.1±1.4/min, respectively. The duration of the action potentials in driven cells also increased significantly for several minutes. All these effects were blocked by tetrodotoxin (TTX) (1.6 μM). It was concluded that the positive chronotropic and inotropic effects of nerve stimulation on renal pelvis contractility can be correlated with the changes in the frequency and duration of the action potentials recorded in driven cells.
Similar content being viewed by others
References
Bolzer E (1942) The activity of the pacemaker previous to the discharge of a muscle impulse. Am J Physiol 136:543
Bramich NJ, Edwards FR, Hirst GDS (1990) Sympathetic nerve stimulation and applied transmitters on the sinus venosus of the toad. J Physiol 429:349
Constantinou CE, Neubarth JL, Mensah-Dwumah M (1978) Frequency gradient in the autorhythmicity of the pyeloureteral pacemaker system. Experientia 34:614
Dixon JS, Gosling JA (1990) Ultrastructure of smooth muscle cells in the urinary system. In: Motta PM (ed) Ultrastructure of smooth muscle. Kluwer Academic, p 153
Golenhofen K, Hannappel J (1974) Electrical activity in different regions of the pyeloureteral system in the guinea-pig. Experientia 30:33
Gosling JA, Dixon JS (1972) Structural evidence in support of a urinary tract pacemaker. B J Urol 44:550
Gosling JA, Dixon JS (1974) Species variation in the location of upper urinary tract pacemaker cells. Invest Urol 11:418
Hannappel J (1981) Effects of adrenergic activators and inhibitors on the urinary tract. In: Szekeres (ed) Adrenergic activators and inhibitors, Part II. Springer, Berlin Heildelberg, p 289
Hannappel J, Lutzeyer W (1978) Pacemaker localization in the renal pelvis of the unicalyceal kidney. In vitro study in the rabbit. Eur Urol 4:192
Imaizumi Y, Muraki K, Watanabe M (1989) Ionic currents in single smooth muscle cells from the ureter of the guinea-pig. J Physiol 411:131
Imaizumi Y, Muraki K, Watanabe M (1990) Characteristics of transient outward currents in single smooth muscle cells from the ureter of the guinea-pig. J Physiol 427:301
Kuriyama H, Osa T, Toida N (1967) Membrane properties of the smooth muscle of guinea-pig ureter. J Physiol 191:225.
Kuriyama H, Tomita T (1970) The action potential in the smooth muscle of the guinea-pig taenia coli and ureter studied by the double sucros-gap method. J Gen Physiol 55:147
Lang RJ (1989) Identification of the major membrane currents in freshly dispersed single smooth muscle cells of guinea-pig ureter. J Physiol 412:375
Lang RJ (1990) The whole-cell Ca2+-channel current in single smooth muscle cells of the guinea-pig ureter. J Physiol 423:453
Maggi CA, Giuliani S (1992) Non-adrenergic non-cholinergic excitatory innervation of the guinea-pig isolated renal pelvis, involvement of capsaicin-sensitive primary afferent neurons. J Urol 147:1394
Maggi CA, Theodorsson E, Santicioli P, Giuliani S (1992) Tachykinins and calcitonin gene-related peptide as co-transmitters in local motor responses produced by sensory nerve activation in the guinea-pig isolated renal pelvis. Neuroscience 46:549
Morita T, Kondo S, Suzuki T, Shinichi T, Tsuchida, S (1985) Effect of calyceal resection on pelviureteral peristalsis in isolated pig kidney. J Urol 135:151
Potjer RM, Kimoto Y, Constantinou CE (1992) Topological localization of the frequency and amplitude characteristics of the whole and segmented renal pelvis. Urol Int 48:278
Seki N, Suzuki H (1990) Electrical properties of smooth muscle cell membrane in renal pelvis of rabbits. Am J Physiol 259:F888
Tsuchida S, Suzuki T (1992) Pacemaker activity of the pelvicalyceal border recorded by an intracellular glass microelectrode. Urol Int 48:121
Weiss RM, Wagner ML, Hoffman BF (1967) Localization of the pacemaker for peristalsis in the intact canine ureter. Invest Urol 5:42
Zawalinski VC, Constantinou CE, Burnstock G (1975) Ureteral pacemaker potentials recorded with the sucrose gap technique. Experientia 31:931
Zhang Y, Lang RJ (1993a) Characterization of the spontaneous electrical activity recorded in the proximal renal pelvis of the guinea pig. Symposium on Autonomic Neuroeffector Mechanisms. Oxford, U.K.
Zhang Y, Lang RJ (1993b)_Effects of K+ and Ca2+-channel blockers on the spontaneous electrical and mechanical activity in the guinea-pig renal pelvis. Proc Aust Physiol Pharmacol Soc 24:167P
Zhang Y, Lang RJ (1994) Effects of intrinsic prostaglandins on the spontaneous contractile and electrical activity of the proximal renal pelvis of the guinea pig. B J Pharmacol 113:431
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lang, R.J., Zhang, Y., Exintaris, B. et al. Effects of nerve stimulation on the spontaneous action potentials recorded in the proximal renal pelvis of the guinea-pig. Urol. Res. 23, 343–350 (1995). https://doi.org/10.1007/BF00300025
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00300025