Abstract
1. Rabbit Purkinje fibres were studied using micro-electrode recordings of electrical activity or a two-micro-electrode voltage clamp. Previous morphological work had suggested that these preparations offer structural advantages for the analysis of ionic permeability mechanisms. 2. Viable preparations could be obtained consistently by exposure to a K glutamate Tyrode solution during excision and recovery. In NaCl Tyrode solution, the action potential showed a large overshoot and fully developed plateau, but no pacemaker depolarization at negative potentials. 3. The passive electrical properties were consistent with morphological evidence for the accessibility of cleft membranes within the cell bundle. Electrotonic responses to intracellular current steps showed the behaviour expected for a simple leaky capacitative cable. Capacitative current transients under voltage clamp were changed very little by an eightfold reduction in the external solution conductivity. 4. Slow current changes attributable to K depletion were small compared to those found in other cardiac preparations. The amount of depletion was close to that predicted by a cleft model which assumed free K diffusion in 1 micron clefts. 5. Step depolarizations over the plateau range of potentials evoked a slow inward current which was resistant to tetrodotoxin but blocked by D600. 6. Strong depolarizations to potentials near 0 mV elicited a transient outward current and a slowly activating late outward current. Both components resembled currents found in sheep or calf Purkinje fibres. 7. These experiments support previous interpretations of slow plateau currents in terms of genuine permeability changes. The rabbit Purkinje fibre may allow various ionic channels to be studied with relatively little interference from radial non-uniformities in membrane potential or ion concentration.
Full text
PDF

























Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Adrian R. H., Almers W. Membrane capacity measurements on frog skeletal muscle in media of low ion content. J Physiol. 1974 Mar;237(3):573–605. doi: 10.1113/jphysiol.1974.sp010499. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aronson R. S., Gelles J. M. The effect of ouabain, dinitrophenol, and lithium on the pacemaker current in sheep cardiac Purkinje fibers. Circ Res. 1977 May;40(5):517–524. doi: 10.1161/01.res.40.5.517. [DOI] [PubMed] [Google Scholar]
- Attwell D., Cohen I. The voltage clamp of multicellular preparations. Prog Biophys Mol Biol. 1977;31(3):201–245. doi: 10.1016/0079-6107(78)90009-3. [DOI] [PubMed] [Google Scholar]
- BARR L., HEADINGS V. E., BOHR D. F. Potassium and the recovery of arterial smooth muscle after cold storage. J Gen Physiol. 1962 Sep;46:19–33. doi: 10.1085/jgp.46.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barry P. H., Adrian R. H. Slow conductance changes due to potassium depletion in the transverse tubules of frog muscle fibers during hyperpolarizing pulses. J Membr Biol. 1973;14(3):243–292. doi: 10.1007/BF01868081. [DOI] [PubMed] [Google Scholar]
- Baumgarten C. M., Isenberg G. Depletion and accumulation of potassium in the extracellular clefts of cardiac Purkinje fibers during voltage clamp hyperpolarization and depolarization. Pflugers Arch. 1977 Mar 11;368(1-2):19–31. doi: 10.1007/BF01063450. [DOI] [PubMed] [Google Scholar]
- Beeler G. W., Jr, Reuter H. Voltage clamp experiments on ventricular myocarial fibres. J Physiol. 1970 Mar;207(1):165–190. doi: 10.1113/jphysiol.1970.sp009055. [DOI] [PMC free article] [PubMed] [Google Scholar]
- CORABOEUF E., WEIDMANN S. Temperature effects on the electrical activity of Purkinje fibres. Helv Physiol Pharmacol Acta. 1954;12(1):32–41. [PubMed] [Google Scholar]
- Cohen I., Daut J., Noble D. The effects of potassium and temperature on the pace-maker current, iK2, in Purkinje fibres. J Physiol. 1976 Aug;260(1):55–74. doi: 10.1113/jphysiol.1976.sp011504. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Connor J., Barr L., Jakobsson E. Electrical characteristics of frog atrial trabeculae in the double sucrose gap. Biophys J. 1975 Oct;15(10):1047–1067. doi: 10.1016/S0006-3495(75)85882-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DE Hemptinne A. The double sucrose gap as a method to study the electrical properties of heart cells. Eur J Cardiol. 1973 Dec;1(2):157–162. [PubMed] [Google Scholar]
- DECK K. A., KERN R., TRAUTWEIN W. VOLTAGE CLAMP TECHNIQUE IN MAMMALIAN CARDIAC FIBRES. Pflugers Arch Gesamte Physiol Menschen Tiere. 1964 Jun 9;280:50–62. doi: 10.1007/BF00412615. [DOI] [PubMed] [Google Scholar]
- DRAPER M. H., WEIDMANN S. Cardiac resting and action potentials recorded with an intracellular electrode. J Physiol. 1951 Sep;115(1):74–94. doi: 10.1113/jphysiol.1951.sp004653. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dudel J., Peper K., Rüdel R., Trautwein W. The dynamic chloride component of membrane current in Purkinje fibers. Pflugers Arch Gesamte Physiol Menschen Tiere. 1967;295(3):197–212. doi: 10.1007/BF01844100. [DOI] [PubMed] [Google Scholar]
- FRANKENHAEUSER B., HODGKIN A. L. The after-effects of impulses in the giant nerve fibres of Loligo. J Physiol. 1956 Feb 28;131(2):341–376. doi: 10.1113/jphysiol.1956.sp005467. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ferrier G. R. Digitalis arrhythmias: role of oscillatory afterpotentials. Prog Cardiovasc Dis. 1977 May-Jun;19(6):459–474. doi: 10.1016/0033-0620(77)90010-x. [DOI] [PubMed] [Google Scholar]
- Fozzard H. A., Beeler G. W., Jr The voltage clamp and cardiac electrophysiology. Circ Res. 1975 Oct;37(4):403–413. doi: 10.1161/01.res.37.4.403. [DOI] [PubMed] [Google Scholar]
- Fozzard H. A. Membrane capacity of the cardiac Purkinje fibre. J Physiol. 1966 Jan;182(2):255–267. doi: 10.1113/jphysiol.1966.sp007823. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Freygang W. H., Trautwein W. The structural implications of the linear electrical properties of cardiac Purkinje strands. J Gen Physiol. 1970 Apr;55(4):524–547. doi: 10.1085/jgp.55.4.524. [DOI] [PMC free article] [PubMed] [Google Scholar]
- GIBBS C. L., JOHNSON E. A. Effect of changes in frequency of stimulation upon rabbit ventricular action potential. Circ Res. 1961 Jan;9:165–170. doi: 10.1161/01.res.9.1.165. [DOI] [PubMed] [Google Scholar]
- Harrington L., Johnson E. A. Voltage clamp of cardiac muscle in a double sucrose gap. A feasibility study. Biophys J. 1973 Jul;13(7):626–647. doi: 10.1016/S0006-3495(73)86013-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hauswirth O., Noble D., Tsien R. W. The mechanism of oscillatory activity at low membrane potentials in cardiac Purkinje fibres. J Physiol. 1969 Jan;200(1):255–265. doi: 10.1113/jphysiol.1969.sp008691. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hellam D. C., Studt J. W. A core-conductor model of the cardiac Purkinje fibre based on structural analysis. J Physiol. 1974 Dec;243(3):637–660. doi: 10.1113/jphysiol.1974.sp010770. [DOI] [PMC free article] [PubMed] [Google Scholar]
- JOHNSON E. A., TILLE J. Investigations of the electrical properties of cardiac muscle fibres with the aid of intracellular double-barrelled electrodes. J Gen Physiol. 1961 Jan;44:443–467. doi: 10.1085/jgp.44.3.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson E. A., Lieberman M. Heart: excitation and contraction. Annu Rev Physiol. 1971;33:479–532. doi: 10.1146/annurev.ph.33.030171.002403. [DOI] [PubMed] [Google Scholar]
- Johnson E. A., Sommer J. R. A strand of cardiac muscle. Its ultrastructure and the electrophysiological implications of its geometry. J Cell Biol. 1967 Apr;33(1):103–129. doi: 10.1083/jcb.33.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kass R. S., Lederer W. J., Tsien R. W., Weingart R. Role of calcium ions in transient inward currents and aftercontractions induced by strophanthidin in cardiac Purkinje fibres. J Physiol. 1978 Aug;281:187–208. doi: 10.1113/jphysiol.1978.sp012416. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kass R. S., Siegelbaum S., Tsien R. W. Incomplete inactivation of the slow inward current in cardiac Purkinje fibres [proceedings]. J Physiol. 1976 Dec;263(1):127P–128P. [PubMed] [Google Scholar]
- Kunze D. L. Rate-dependent changes in extracellular potassium in the rabbit atrium. Circ Res. 1977 Jul;41(1):122–127. doi: 10.1161/01.res.41.1.122. [DOI] [PubMed] [Google Scholar]
- Lederer W. J., Tsien R. W. Transient inward current underlying arrhythmogenic effects of cardiotonic steroids in Purkinje fibres. J Physiol. 1976 Dec;263(2):73–100. doi: 10.1113/jphysiol.1976.sp011622. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lieberman M., Sawanobori T., Kootsey J. M., Johnson E. A. A synthetic strand of cardiac muscle: its passive electrical properties. J Gen Physiol. 1975 Apr;65(4):527–550. doi: 10.1085/jgp.65.4.527. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MacDonald R. L., Hsu D., Mann J. E., Jr, Sperelakis N. An analysis of the problem of K-+ accumulation in the intercalated disk clefts of cardiac muscle. J Theor Biol. 1975 Jun;51(2):455–473. doi: 10.1016/0022-5193(75)90074-0. [DOI] [PubMed] [Google Scholar]
- Maughan D. W. Some effects of prolonged polarization on membrane currents in bullfrog atrial muscle. J Membr Biol. 1973;11(4):331–352. doi: 10.1007/BF01869829. [DOI] [PubMed] [Google Scholar]
- McAllister R. E., Noble D., Tsien R. W. Reconstruction of the electrical activity of cardiac Purkinje fibres. J Physiol. 1975 Sep;251(1):1–59. doi: 10.1113/jphysiol.1975.sp011080. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McGuigan J. A. Some limitations of the double sucrose gap, and its use in a study of the slow outward current in mammalian ventricular muscle. J Physiol. 1974 Aug;240(3):775–806. doi: 10.1113/jphysiol.1974.sp010634. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mobley B. A., Page E. The surface area of sheep cardiac Purkinje fibres. J Physiol. 1972 Feb;220(3):547–563. doi: 10.1113/jphysiol.1972.sp009722. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noble D., Tsien R. W. Outward membrane currents activated in the plateau range of potentials in cardiac Purkinje fibres. J Physiol. 1969 Jan;200(1):205–231. doi: 10.1113/jphysiol.1969.sp008689. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noble S. J. Potassium accumulation and depletion in frog atrial muscle. J Physiol. 1976 Jul;258(3):579–613. doi: 10.1113/jphysiol.1976.sp011436. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Page E. Quantitative ultrastructural analysis in cardiac membrane physiology. Am J Physiol. 1978 Nov;235(5):C147–C158. doi: 10.1152/ajpcell.1978.235.5.C147. [DOI] [PubMed] [Google Scholar]
- Page S. G., Niedergerke R. Structures of physiological interest in the frog heart ventricle. J Cell Sci. 1972 Jul;11(1):179–203. doi: 10.1242/jcs.11.1.179. [DOI] [PubMed] [Google Scholar]
- Reuter H. Divalent cations as charge carriers in excitable membranes. Prog Biophys Mol Biol. 1973;26:1–43. doi: 10.1016/0079-6107(73)90016-3. [DOI] [PubMed] [Google Scholar]
- Reuter H. Slow inactivation of currents in cardiac Purkinje fibres. J Physiol. 1968 Jul;197(1):233–253. doi: 10.1113/jphysiol.1968.sp008557. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sachs F. Electrophysiological properties of tissue cultured heart cells grown in a linear array. J Membr Biol. 1976 Sep 17;28(4):373–399. doi: 10.1007/BF01869706. [DOI] [PubMed] [Google Scholar]
- Schneider M. F., Chandler W. K. Effects of membrane potential on the capacitance of skeletal muscle fibers. J Gen Physiol. 1976 Feb;67(2):125–163. doi: 10.1085/jgp.67.2.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schoenberg M., Dominguez G., Fozzard H. A. Effect of diameter on membrane capacity and conductance of sheep cardiac Purkinje fibers. J Gen Physiol. 1975 Apr;65(4):441–458. doi: 10.1085/jgp.65.4.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sommer J. R., Johnson E. A. Cardiac muscle. A comparative study of Purkinje fibers and ventricular fibers. J Cell Biol. 1968 Mar;36(3):497–526. doi: 10.1083/jcb.36.3.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tille J. Electrotonic interaction between muscle fibers in the rabbit ventricle. J Gen Physiol. 1966 Sep;50(1):189–202. doi: 10.1085/jgp.50.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsien R. W., Carpenter D. O. Ionic mechanisms of pacemaker activity in cardiac Purkinje fibers. Fed Proc. 1978 Jun;37(8):2127–2131. [PubMed] [Google Scholar]
- Tsien R. W. Mode of action of chronotropic agents in cardiac Purkinje fibers. Does epinephrine act by directly modifying the external surface charge? J Gen Physiol. 1974 Sep;64(3):320–342. doi: 10.1085/jgp.64.3.320. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vassalle M. Analysis of cardiac pacemaker potential using a "voltage clamp" technique. Am J Physiol. 1966 Jun;210(6):1335–1341. doi: 10.1152/ajplegacy.1966.210.6.1335. [DOI] [PubMed] [Google Scholar]
- Vereecke J., Carmeliet E. Sr action potentials in cardiac Purkyne fibres. I. Evidence for a regenerative increase in Sr conductance. Pflugers Arch. 1971;322(1):60–72. doi: 10.1007/BF00586665. [DOI] [PubMed] [Google Scholar]
- WEIDMANN S. The effect of the cardiac membrane potential on the rapid availability of the sodium-carrying system. J Physiol. 1955 Jan 28;127(1):213–224. doi: 10.1113/jphysiol.1955.sp005250. [DOI] [PMC free article] [PubMed] [Google Scholar]
- WEIDMANN S. The electrical constants of Purkinje fibres. J Physiol. 1952 Nov;118(3):348–360. doi: 10.1113/jphysiol.1952.sp004799. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weidmann S. Electrical constants of trabecular muscle from mammalian heart. J Physiol. 1970 Nov;210(4):1041–1054. doi: 10.1113/jphysiol.1970.sp009256. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weidmann S. The diffusion of radiopotassium across intercalated disks of mammalian cardiac muscle. J Physiol. 1966 Nov;187(2):323–342. doi: 10.1113/jphysiol.1966.sp008092. [DOI] [PMC free article] [PubMed] [Google Scholar]