Abstract
Single electroplaques of Torpedo nobiliana have been studied with microelectrode recording. Direct evidence is presented that the only electrogenically reactive membrane of the cells is on the innervated surface and that this membrane is electrically inexcitable. Responses are not evoked by depolarizing currents applied to this membrane, but only by stimulating the innervating nerve fibers. The responses arise after a latency of 1 to 3 msec. This latency is not affected by large depolarizing or hyperpolarizing changes in membrane potential. Various properties that have been theoretically associated with electrically inexcitable responses have been also demonstrated to occur in the electroplaques. The neurally evoked response is not propagated actively in the membrane and may have different amplitudes and forms in closely adjacent regions. The maximal responses frequently are slightly larger than the recorded resting potential but the apparent small overshoot may be due to difficulty in recording the full resting potential. The responses are subject to electrochemical gradation and appear inverted in sign on applying strong outward currents across the innervated membrane. This membrane is cholinoceptive and shows marked desensitization. The membrane of the uninnervated surface has a very low resistance, a factor that aids maximum output of current during the discharge of the electric organ.
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Selected References
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- ALBE-FESSARD D., CHAGAS C., COUCEIRO A., FESSARD A. Characteristics of responses from electrogenic tissue in Electrophorus electricus. J Neurophysiol. 1951 May;14(2):243–252. doi: 10.1152/jn.1951.14.3.243. [DOI] [PubMed] [Google Scholar]
- ALBE-FESSARD D. Etude des facteurs périphériques d'organisation de la décharge de la torpille. Arch Sci Physiol (Paris) 1952;6(2):105–123. [PubMed] [Google Scholar]
- ALTAMIRANO M., COATES C. W., GRUNDFEST H. Mechanisms of direct and neural excitability in electroplaques of electric eel. J Gen Physiol. 1955 Jan 20;38(3):319–360. doi: 10.1085/jgp.38.3.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
- ALTAMIRANO M., COATES C. W., GRUNDFEST H., NACHMANSOHN D. Electrical activity in electric tissue. III. Modifications of electrical activity by acetylcholine and related compounds. Biochim Biophys Acta. 1955 Apr;16(4):449–463. doi: 10.1016/0006-3002(55)90263-8. [DOI] [PubMed] [Google Scholar]
- BENNETT M. V., CRAIN S. M., GRUNDFEST H. Electrophysiology of supramedullary neurons in Spheroides maculatus. I. Orthodromic and antidromic responses. J Gen Physiol. 1959 Sep;43:159–188. doi: 10.1085/jgp.43.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
- BENNETT M. V., GRUNDFEST H. Electrophysiology of electric organ in Gymnotus carapo. J Gen Physiol. 1959 May 20;42(5):1067–1104. doi: 10.1085/jgp.42.5.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
- BOISTEL J., FATT P. Membrane permeability change during inhibitory transmitter action in crustacean muscle. J Physiol. 1958 Nov 10;144(1):176–191. doi: 10.1113/jphysiol.1958.sp006094. [DOI] [PMC free article] [PubMed] [Google Scholar]
- BROCK L. G., ECCLES R. M. The membrane potentials during rest and activity of the ray electroplate. J Physiol. 1958 Jul 14;142(2):251–274. doi: 10.1113/jphysiol.1958.sp006014. [DOI] [PMC free article] [PubMed] [Google Scholar]
- BULLOCK T. H., HAGIWARA S. Intracellular recording from the giant synapse of the squid. J Gen Physiol. 1957 Mar 20;40(4):565–577. doi: 10.1085/jgp.40.4.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
- BURKE W., GINSBORG B. L. The electrical properties of the slow muscle fibre membrane. J Physiol. 1956 Jun 28;132(3):586–598. doi: 10.1113/jphysiol.1956.sp005551. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DEL CASTILLO J., KATZ B. Biophysical aspects of neuro-muscular transmission. Prog Biophys Biophys Chem. 1956;6:121–170. [PubMed] [Google Scholar]
- FATT P., GINSBORG B. L. The ionic requirements for the production of action potentials in crustacean muscle fibres. J Physiol. 1958 Aug 6;142(3):516–543. doi: 10.1113/jphysiol.1958.sp006034. [DOI] [PMC free article] [PubMed] [Google Scholar]
- FATT P., KATZ B. An analysis of the end-plate potential recorded with an intracellular electrode. J Physiol. 1951 Nov 28;115(3):320–370. doi: 10.1113/jphysiol.1951.sp004675. [DOI] [PMC free article] [PubMed] [Google Scholar]
- FATT P., KATZ B. The effect of inhibitory nerve impulses on a crustacean muscle fibre. J Physiol. 1953 Aug;121(2):374–389. doi: 10.1113/jphysiol.1953.sp004952. [DOI] [PMC free article] [PubMed] [Google Scholar]
- FESSARD A. Diversity of transmission processes as exemplified by specific synapses in electric organs. Proc R Soc Lond B Biol Sci. 1952 Oct 16;140(899):186–191. doi: 10.1098/rspb.1952.0056. [DOI] [PubMed] [Google Scholar]
- Feldberg W., Fessard A. The cholinergic nature of the nerves to the electric organ of the Torpedo (Torpedo marmorata). J Physiol. 1942 Aug 18;101(2):200–216. doi: 10.1113/jphysiol.1942.sp003975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- GILBERT P. W., WOOD F. G., Jr Method of anesthetizing large sharks and rays safely and rapidly. Science. 1957 Aug 2;126(3266):212–213. doi: 10.1126/science.126.3266.212. [DOI] [PubMed] [Google Scholar]
- GRUNDFEST H. An electrophysiological basis for neuropharmacology. Fed Proc. 1958 Dec;17(4):1006–1018. [PubMed] [Google Scholar]
- GRUNDFEST H. Electrical inexcitability of synapses and some consequences in the central nervous system. Physiol Rev. 1957 Jul;37(3):337–361. doi: 10.1152/physrev.1957.37.3.337. [DOI] [PubMed] [Google Scholar]
- GRUNDFEST H. General problems of drugs actions on bioelectric phenomena. Ann N Y Acad Sci. 1957 Mar 14;66(3):537–591. doi: 10.1111/j.1749-6632.1957.tb40748.x. [DOI] [PubMed] [Google Scholar]
- GRUNDFEST H., PURPURA D. P. Inexcitability of cortical dendrites to electric stimuli. Nature. 1956 Aug 25;178(4530):416–417. doi: 10.1038/178416b0. [DOI] [PubMed] [Google Scholar]
- GRUNDFEST H., REUBEN J. P., RICKLES W. H., Jr The electrophysiology and pharmacology of lobster neuromuscular synapses. J Gen Physiol. 1959 Jul 20;42(6):1301–1323. doi: 10.1085/jgp.42.6.1301. [DOI] [PMC free article] [PubMed] [Google Scholar]
- GRUNDFEST H. The mechanisms of discharge of the electric organs in relation to general and comparative electrophysiology. Prog Biophys Biophys Chem. 1957;7:1–85. [PubMed] [Google Scholar]
- HAGIWARA S., TASAKI I. A study on the mechanism of impulse transmission across the giant synapse of the squid. J Physiol. 1958 Aug 29;143(1):114–137. doi: 10.1113/jphysiol.1958.sp006048. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HAGIWARA S., WATANABE A., SAITO N. Potential changes in syncytial neurons of lobster cardiac ganglion. J Neurophysiol. 1959 Sep;22:554–572. doi: 10.1152/jn.1959.22.5.554. [DOI] [PubMed] [Google Scholar]
- HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
- KATZ B., THESLEFF S. A study of the desensitization produced by acetylcholine at the motor end-plate. J Physiol. 1957 Aug 29;138(1):63–80. doi: 10.1113/jphysiol.1957.sp005838. [DOI] [PMC free article] [PubMed] [Google Scholar]
- KEYNES R. D., MARTINS-FERREIRA H. Membrane potentials in the electroplates of the electric eel. J Physiol. 1953 Feb 27;119(2-3):315–351. doi: 10.1113/jphysiol.1953.sp004849. [DOI] [PMC free article] [PubMed] [Google Scholar]
- KRNJEVIC K., MILEDI R. Failure of neuromuscular propagation in rats. J Physiol. 1958 Mar 11;140(3):440–461. [PMC free article] [PubMed] [Google Scholar]
- LLOYD D. P. C. Post-tetanic potentiation of response in monosynaptic reflex pathways of the spinal cord. J Gen Physiol. 1949 Nov;33(2):147–170. doi: 10.1085/jgp.33.2.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LUNDBERG A. Electrophysiology of salivary glands. Physiol Rev. 1958 Jan;38(1):21–40. doi: 10.1152/physrev.1958.38.1.21. [DOI] [PubMed] [Google Scholar]
- TASAKI I., SPYROPOULOS C. S. Membrane conductance and current-voltage relation in the squid axon under voltage-clamp. Am J Physiol. 1958 May;193(2):318–327. doi: 10.1152/ajplegacy.1958.193.2.318. [DOI] [PubMed] [Google Scholar]
- TOMITA T. Peripheral mechanism of nervous activity in lateral eye of horseshoe crab. J Neurophysiol. 1957 May;20(3):245–254. doi: 10.1152/jn.1957.20.3.245. [DOI] [PubMed] [Google Scholar]
- WERMAN R. Electrical inexcitability of the synaptic membrane in the frog skeletal muscle fibre. Nature. 1960 Oct 8;188:149–150. doi: 10.1038/188149a0. [DOI] [PubMed] [Google Scholar]