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. 1980 Jun;303:495–513. doi: 10.1113/jphysiol.1980.sp013300

Calcium spikes in toad rods.

G L Fain, H M Gerschenfeld, F N Quandt
PMCID: PMC1282906  PMID: 6776262

Abstract

1. When the retina of the toad, Bufo marinus, was superfused with 6-12 mM-tetraethylammonium chloride (TEA), intracellular recordings from rods showed large, depolarizing regenerative potentials. For brief exposures to TEA, these potentials occurred during the recovery phase of the light responses; whereas, during longer exposures, they were spontaneous in darkness but suppressed during illumination. Similar regenerative potentials were observed during perfusion with 3-10 mM-4-aminopyridine and 1-2 mM-BaCl2. 2. The amplitude of the regenerative potentials depended upon the extracellular Ca concentration ([Ca2+]o). Lowering [Ca2+]o decreased their amplitude and in zero [Ca2+]o they were reversibly abolished. Increasing [Ca2+]o by 1.5-2 times produced a small hyperpolarization of membrane potential and a large augmentation in regenerative response amplitude. However, larger increases in [Ca2+]o produced large membrane hyperpolarizations and reversibly suppressed the regenerative responses. 3. High concentrations of Sr2+ in TEA also enhanced regenerative activity but did not affect the rod resting membrane potential. The amplitude of regenerative potentials increased continuously with increasing [Sr2+]o, and in 28 mM-Sr2+ the rods generated 60-70 mV action potentials, even in the absence of extracellular Na+. 4. The regenerative potentials were blocked by 25 microM-Cd2+, 50-100 microM-Co2+, 5mM-Mg2+, and 100 microM-D-600. They were unaffected by 2 microM-TTX or 2-5 mM-Na aspartate. 5. In Ringer containing 12 mM-TEA, large anode break responses could be recorded from rods at the termination of inward current pulses. These anode break responses were also suppressed by Co2+ and unaffected by TTX or Na aspartate. 6. We conclude that the membrane of toad rods contains a conductance normally selective for Ca2+, which is activated by depolarization. In normal Ringer, the inward current through this conductance produces little effect, since it is balanced by a large outward current, probably carried by K+. TEA and other agents appear to block this outward current, permitting the Ca2+ current to become regenerative.

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Selected References

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  1. Akaike N., Lee K. S., Brown A. M. The calcium current of Helix neuron. J Gen Physiol. 1978 May;71(5):509–531. doi: 10.1085/jgp.71.5.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker P. F., Meves H., Ridgway E. B. Effects of manganese and other agents on the calcium uptake that follows depolarization of squid axons. J Physiol. 1973 Jun;231(3):511–526. doi: 10.1113/jphysiol.1973.sp010246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bastian B. L., Fain G. L. Light adaptation in toad rods: requirement for an internal messenger which is not calcium. J Physiol. 1979 Dec;297(0):493–520. doi: 10.1113/jphysiol.1979.sp013053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baylor D. A., Fuortes M. G. Electrical responses of single cones in the retina of the turtle. J Physiol. 1970 Mar;207(1):77–92. doi: 10.1113/jphysiol.1970.sp009049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baylor D. A., Hodgkin A. L., Lamb T. D. The electrical response of turtle cones to flashes and steps of light. J Physiol. 1974 Nov;242(3):685–727. doi: 10.1113/jphysiol.1974.sp010731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Baylor D. A., Lamb T. D., Yau K. W. The membrane current of single rod outer segments. J Physiol. 1979 Mar;288:589–611. [PMC free article] [PubMed] [Google Scholar]
  7. Brown J. E., Pinto L. H. Ionic mechanism for the photoreceptor potential of the retina of Bufo marinus. J Physiol. 1974 Feb;236(3):575–591. doi: 10.1113/jphysiol.1974.sp010453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brown K. T., Flaming D. G. Opposing effects of calcium and barium in vertebrate rod photoreceptors. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1587–1590. doi: 10.1073/pnas.75.3.1587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cervetto L., MacNichol E. F., Jr Inactivation of horizontal cells in turtle retina by glutamate and aspartate. Science. 1972 Nov 17;178(4062):767–768. doi: 10.1126/science.178.4062.767. [DOI] [PubMed] [Google Scholar]
  10. Cervetto L., Piccolino M. Synaptic transmission between photoreceptors and horizontal cells in the turtle retina. Science. 1974 Feb 1;183(4123):417–419. doi: 10.1126/science.183.4123.417. [DOI] [PubMed] [Google Scholar]
  11. Dacheux R. F., Miller R. F. Photoreceptor-bipolar cell transmission in the perfused retina eyecup of the mudpuppy. Science. 1976 Mar 5;191(4230):963–964. doi: 10.1126/science.175443. [DOI] [PubMed] [Google Scholar]
  12. Dowling J. E., Ripps H. Adaptation in skate photoreceptors. J Gen Physiol. 1972 Dec;60(6):698–719. doi: 10.1085/jgp.60.6.698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dowling J. E., Ripps H. Effect of magnesium on horizontal cell activity in the skate retina. Nature. 1973 Mar 9;242(5393):101–103. doi: 10.1038/242101a0. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. FATT P., KATZ B. The electrical properties of crustacean muscle fibres. J Physiol. 1953 Apr 28;120(1-2):171–204. doi: 10.1113/jphysiol.1953.sp004884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fain G. L., Quandt F. N., Bastian B. L., Gerschenfeld H. M. Contribution of a caesium-sensitive conductance increase to the rod photoresponse. Nature. 1978 Mar 30;272(5652):466–469. doi: 10.1038/272467a0. [DOI] [PubMed] [Google Scholar]
  17. Fain G. L., Quandt F. N., Gerschenfeld H. M. Calcium-dependent regenerative responses in rods. Nature. 1977 Oct 20;269(5630):707–710. doi: 10.1038/269707a0. [DOI] [PubMed] [Google Scholar]
  18. Fain G. L., Quandt F. N. The effects of tetraethylammonium and cobalt ions on responses to extrinsic current in toad rods. J Physiol. 1980 Jun;303:515–533. doi: 10.1113/jphysiol.1980.sp013301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fain G. L. Quantum sensitivity of rods in the toad retina. Science. 1975 Mar 7;187(4179):838–841. doi: 10.1126/science.1114328. [DOI] [PubMed] [Google Scholar]
  20. Gold G. H., Dowling J. E. Photoreceptor coupling in retina of the toad, Bufo marinus. I. Anatomy. J Neurophysiol. 1979 Jan;42(1 Pt 1):292–310. doi: 10.1152/jn.1979.42.1.292. [DOI] [PubMed] [Google Scholar]
  21. Hagins W. A., Penn R. D., Yoshikami S. Dark current and photocurrent in retinal rods. Biophys J. 1970 May;10(5):380–412. doi: 10.1016/S0006-3495(70)86308-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hagiwara S. Ca-dependent action potential. Membranes. 1975;3:359–381. [PubMed] [Google Scholar]
  23. Hagiwara S., Fukuda J., Eaton D. C. Membrane currents carried by Ca, Sr, and Ba in barnacle muscle fiber during voltage clamp. J Gen Physiol. 1974 May;63(5):564–578. doi: 10.1085/jgp.63.5.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Horn R. Propagating calcium spikes in an axon of Aplysia. J Physiol. 1978 Aug;281:513–534. doi: 10.1113/jphysiol.1978.sp012437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kaneko A., Shimazaki H. Synaptic transmission from photoreceptors to bipolar and horizontal cells in the carp retina. Cold Spring Harb Symp Quant Biol. 1976;40:537–546. doi: 10.1101/sqb.1976.040.01.050. [DOI] [PubMed] [Google Scholar]
  26. Katz B., Miledi R. Tetrodotoxin-resistant electric activity in presynaptic terminals. J Physiol. 1969 Aug;203(2):459–487. doi: 10.1113/jphysiol.1969.sp008875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kirsch G. E., Narahashi T. 3,4-diaminopyridine. A potent new potassium channel blocker. Biophys J. 1978 Jun;22(3):507–512. doi: 10.1016/S0006-3495(78)85503-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lasansky A., Marchiafava P. L. Light-induced resistance changes in retinal rods and cones of the tiger salamander. J Physiol. 1974 Jan;236(1):171–191. doi: 10.1113/jphysiol.1974.sp010429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Llinás R., Nicholson C. Calcium role in depolarization-secretion coupling: an aequorin study in squid giant synapse. Proc Natl Acad Sci U S A. 1975 Jan;72(1):187–190. doi: 10.1073/pnas.72.1.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Llinás R., Steinberg I. Z., Walton K. Presynaptic calcium currents and their relation to synaptic transmission: voltage clamp study in squid giant synapse and theoretical model for the calcium gate. Proc Natl Acad Sci U S A. 1976 Aug;73(8):2918–2922. doi: 10.1073/pnas.73.8.2918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Meves H., Pichon Y. The effect of internal and external 4-aminopyridine on the potassium currents in intracellularly perfused squid giant axons. J Physiol. 1977 Jun;268(2):511–532. doi: 10.1113/jphysiol.1977.sp011869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Murakami M., Otsu K., Otsuka T. Effects of chemicals on receptors and horizontal cells in the retina. J Physiol. 1972 Dec;227(3):899–913. doi: 10.1113/jphysiol.1972.sp010065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Murakami M., Otsuka T., Shimazaki H. Effects of aspartate and glutamate on the bipolar cells in the carp retina. Vision Res. 1975 Mar;15(3):456–458. doi: 10.1016/0042-6989(75)90101-7. [DOI] [PubMed] [Google Scholar]
  34. Narahashi T. Chemicals as tools in the study of excitable membranes. Physiol Rev. 1974 Oct;54(4):813–889. doi: 10.1152/physrev.1974.54.4.813. [DOI] [PubMed] [Google Scholar]
  35. Normann R. A., Pochobradský J. Oscillations in rod and horizontal cell membrane potential: evidence for feed-back to rods in the vertebrate retina. J Physiol. 1976 Sep;261(1):15–29. doi: 10.1113/jphysiol.1976.sp011546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ripps H., Shakib M., MacDonald E. D. Peroxidase uptake by photoreceptor terminals of the skate retina. J Cell Biol. 1976 Jul;70(1):86–96. doi: 10.1083/jcb.70.1.86. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schwartz E. A. Electrical properties of the rod syncytium in the retina of the turtle. J Physiol. 1976 May;257(2):379–406. doi: 10.1113/jphysiol.1976.sp011374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sillman A. J., Ito H., Tomita T. Studies on the mass receptor potential of the isolated frog retina. II. On the basis of the ionic mechanism. Vision Res. 1969 Dec;9(12):1443–1451. doi: 10.1016/0042-6989(69)90060-1. [DOI] [PubMed] [Google Scholar]
  39. Waloga G., Pak W. L. Ionic mechanism for the generation of horizontal cell potentials in isolated axolotl retina. J Gen Physiol. 1978 Jan;71(1):69–92. doi: 10.1085/jgp.71.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Werblin F. S. Regenerative hyperpolarization in rods. J Physiol. 1975 Jan;244(1):53–81. doi: 10.1113/jphysiol.1975.sp010784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wu S. M., Dowling J. E. L-aspartate: evidence for a role in cone photoreceptor synaptic transmission in the carp retina. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5205–5209. doi: 10.1073/pnas.75.10.5205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yeh J. Z., Oxford G. S., Wu C. H., Narahashi T. Dynamics of aminopyridine block of potassium channels in squid axon membrane. J Gen Physiol. 1976 Nov;68(5):519–535. doi: 10.1085/jgp.68.5.519. [DOI] [PMC free article] [PubMed] [Google Scholar]

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