Abstract
The possible role of Ca ions in mediating the drop in sensitivity associated with light adaptation in Limulus ventral photoreceptors was assessed by simultaneously measuring the sensitivity to light and the intracellular free Ca concentration (Cai); the latter was measured by using Ca-selective microelectrodes. In dark-adapted photoreceptors, the mean resting Cai was 3.5 +/- 2.5 microM SD (n = 31). No correlation was found between resting Cai and absolute sensitivity from cell to cell. Typically, photoreceptors are not uniformly sensitive to light; the Cai rise evoked by uniform illumination was 20-40 times larger and faster in the most sensitive region of the cell (the rhabdomeral lobe) than it was away from it. In response to a brief flash, the Cai rise was barely detectable when 10(2) photons were absorbed, and it was saturated when approximately 10(5) photons were absorbed. During maintained illumination, starting near the threshold of light adaptation, steady Cai increases were associated with steady desensitizations over several log units of light intensity: a 100-fold desensitization was associated with a 2.5-fold increase in Cai. After a bright flash, sensitivity and Cai recovered with different time courses: the cell was still desensitized by approximately 0.5 log units when Cai had already recovered to the prestimulus level, which suggests that under those conditions Cai is not the rate-limiting step of dark adaptation. Ionophoretic injection of EGTA markedly decreased the light-induced Cai rise and increased the time to peak of the light response, but did not alter the resting Cai, which suggests that the time to peak is affected by a change in the capacity to bind Ca2+ and not by resting Cai. Lowering the extracellular Ca2+ concentration (Cao) first decreased Cai and increased sensitivity. Longer exposure to low Cao resulted in a further decrease of Cai but decreased rather than increased sensitivity, which suggests that under certain conditions it is possible to uncouple Cai and sensitivity.
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- Allen D. G., Blinks J. R., Prendergast F. G. Aequorin luminescence: relation of light emission to calcium concentration--a calcium-independent component. Science. 1977 Mar 11;195(4282):996–998. doi: 10.1126/science.841325. [DOI] [PubMed] [Google Scholar]
- Alvarez-Leefmans F. J., Rink T. J., Tsien R. Y. Free calcium ions in neurones of Helix aspersa measured with ion-selective micro-electrodes. J Physiol. 1981 Jun;315:531–548. doi: 10.1113/jphysiol.1981.sp013762. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blinks J. R., Wier W. G., Hess P., Prendergast F. G. Measurement of Ca2+ concentrations in living cells. Prog Biophys Mol Biol. 1982;40(1-2):1–114. doi: 10.1016/0079-6107(82)90011-6. [DOI] [PubMed] [Google Scholar]
- Brinley F. J., Jr Calcium buffering in squid axons. Annu Rev Biophys Bioeng. 1978;7:363–392. doi: 10.1146/annurev.bb.07.060178.002051. [DOI] [PubMed] [Google Scholar]
- Brown H. M., Hagiwara S., Koike H., Meech R. M. Membrane properties of a barnacle photoreceptor examined by the voltage clamp technique. J Physiol. 1970 Jun;208(2):385–413. doi: 10.1113/jphysiol.1970.sp009127. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown H. M. Intracellular Na+, K+, and C1- activities in Balanus photoreceptors. J Gen Physiol. 1976 Sep;68(3):281–296. doi: 10.1085/jgp.68.3.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown J. E., Blinks J. R. Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin. J Gen Physiol. 1974 Dec;64(6):643–665. doi: 10.1085/jgp.64.6.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown J. E., Brown P. K., Pinto L. H. Detection of light-induced changes of intracellular ionized calcium concentration in Limulus ventral photoreceptors using arsenazo III. J Physiol. 1977 May;267(2):299–320. doi: 10.1113/jphysiol.1977.sp011814. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown J. E., Coles J. A. Saturation of the response to light in Limulus ventral photoreceptor. J Physiol. 1979 Nov;296:373–392. doi: 10.1113/jphysiol.1979.sp013011. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown J. E., Lisman J. E. Intracellular Ca modulates sensitivity and time scale in Limulus ventral photoreceptors. Nature. 1975 Nov 20;258(5532):252–254. doi: 10.1038/258252a0. [DOI] [PubMed] [Google Scholar]
- Calman B. G., Chamberlain S. C. Distinct lobes of Limulus ventral photoreceptors. II. Structure and ultrastructure. J Gen Physiol. 1982 Dec;80(6):839–862. doi: 10.1085/jgp.80.6.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clark A. W., Millecchia R., Mauro A. The ventral photoreceptor cells of Limulus. I. The microanatomy. J Gen Physiol. 1969 Sep;54(3):289–309. doi: 10.1085/jgp.54.3.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coles J. A., Tsacopoulos M. Potassium activity in photoreceptors, glial cells and extracellular space in the drone retina: changes during photostimulation. J Physiol. 1979 May;290(2):525–549. doi: 10.1113/jphysiol.1979.sp012788. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cornwall M. C., Thomas M. V. Glass microelectrode tip capacitance: its measurement and a method for its reduction. J Neurosci Methods. 1981 Feb;3(3):225–232. doi: 10.1016/0165-0270(81)90057-1. [DOI] [PubMed] [Google Scholar]
- FUORTES M. G., HODGKIN A. L. CHANGES IN TIME SCALE AND SENSITIVITY IN THE OMMATIDIA OF LIMULUS. J Physiol. 1964 Aug;172:239–263. doi: 10.1113/jphysiol.1964.sp007415. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fein A., Charlton J. S. A quantitative comparison of the effects of intracellular calcium injection and light adaptation on the photoresponse of Limulus ventral photoreceptors. J Gen Physiol. 1977 Nov;70(5):591–600. doi: 10.1085/jgp.70.5.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fein A., Charlton J. S. A quantitative comparison of the time-course of sensitivity changes produced by calcium injection and light adaptation in Limulus ventral photoreceptors. Biophys J. 1978 Apr;22(1):105–113. doi: 10.1016/S0006-3495(78)85474-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fein A., Charlton J. S. Enhancement and phototransduction in the ventral eye of limulus. J Gen Physiol. 1977 May;69(5):553–569. doi: 10.1085/jgp.69.5.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fein A., Charlton J. S. Increased intracellular sodium mimics some but not all aspects of photoreceptor adaptation in the ventral eye of Limulus. J Gen Physiol. 1977 Nov;70(5):601–620. doi: 10.1085/jgp.70.5.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fein A., Charlton J. S. Local adaptation in the ventral photoreceptors of Limulus. J Gen Physiol. 1975 Dec;66(6):823–836. doi: 10.1085/jgp.66.6.823. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fein A., Charlton J. S. Recovery from adapting light in Limulus ventral photoreceptors. Brain Res. 1978 Sep 29;153(3):585–590. doi: 10.1016/0006-8993(78)90342-6. [DOI] [PubMed] [Google Scholar]
- Fein A., Lisman J. Localized desensitization of Limulus photoreceptors produced by light or intracellular calcium ion injection. Science. 1975 Mar 21;187(4181):1094–1096. doi: 10.1126/science.1114339. [DOI] [PubMed] [Google Scholar]
- Fischmeister R., Horackova M. Variation of intracellular Ca2+ following Ca2+ current in heart. A theoretical study of ionic diffusion inside a cylindrical cell. Biophys J. 1983 Mar;41(3):341–348. doi: 10.1016/S0006-3495(83)84445-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fulpius B., Baumann F. Effects of sodium, potassium, and calcium ions on slow and spike potentials in single photoreceptor cells. J Gen Physiol. 1969 May;53(5):541–561. doi: 10.1085/jgp.53.5.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorman A. L., Levy S., Nasi E., Tillotson D. Intracellular calcium measured with calcium-sensitive micro-electrodes and Arsenazo III in voltage-clamped Aplysia neurones. J Physiol. 1984 Aug;353:127–142. doi: 10.1113/jphysiol.1984.sp015327. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorman A. L., Thomas M. V. Intracellular calcium accumulation during depolarization in a molluscan neurone. J Physiol. 1980 Nov;308:259–285. doi: 10.1113/jphysiol.1980.sp013471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hagins W. A., Yoshikami S. Proceedings: A role for Ca2+ in excitation of retinal rods and cones. Exp Eye Res. 1974 Mar;18(3):299–305. doi: 10.1016/0014-4835(74)90157-2. [DOI] [PubMed] [Google Scholar]
- Harary H. H., Brown J. E. Spatially nonuniform changes in intracellular calcium ion concentrations. Science. 1984 Apr 20;224(4646):292–294. doi: 10.1126/science.6710144. [DOI] [PubMed] [Google Scholar]
- Kushmerick M. J., Podolsky R. J. Ionic mobility in muscle cells. Science. 1969 Dec 5;166(3910):1297–1298. doi: 10.1126/science.166.3910.1297. [DOI] [PubMed] [Google Scholar]
- Levy S., Coles J. A. Intracellular pH of Limulus ventral photoreceptor measured with a double-barrelled pH microelectrode. Experientia. 1977 Apr 15;33(4):553–554. doi: 10.1007/BF01922268. [DOI] [PubMed] [Google Scholar]
- Lisman J. E., Brown J. E. Effects of intracellular injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. J Gen Physiol. 1975 Oct;66(4):489–506. doi: 10.1085/jgp.66.4.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lisman J. E., Brown J. E. Light-induced changes of sensitivity in Limulus ventral photoreceptors. J Gen Physiol. 1975 Oct;66(4):473–488. doi: 10.1085/jgp.66.4.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lisman J. E., Brown J. E. The effects of intracellular iontophoretic injection of calcium and sodium ions on the light response of Limulus ventral photoreceptors. J Gen Physiol. 1972 Jun;59(6):701–719. doi: 10.1085/jgp.59.6.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lisman J. E. Effects of removing extracellular Ca2+ on excitation and adaptation in Limulus ventral photoreceptors. Biophys J. 1976 Nov;16(11):1331–1335. doi: 10.1016/S0006-3495(76)85777-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lisman J. E., Strong J. A. The initiation of excitation and light adaptation in Limulus ventral photoreceptors. J Gen Physiol. 1979 Feb;73(2):219–243. doi: 10.1085/jgp.73.2.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maaz G., Stieve H. The correlation of the receptor potential with the light induced transient increase in intracellular calcium-concentration measured by absorption change of arsenazo III injected into Limulus ventral nerve photoreceptor cell. Biophys Struct Mech. 1980;6(3):191–208. doi: 10.1007/BF00537293. [DOI] [PubMed] [Google Scholar]
- Martinez J. M., 2nd, Srebro R. Calcium and the control of discrete wave latency in the ventral photoreceptor of Limulus. J Physiol. 1976 Oct;261(3):535–562. doi: 10.1113/jphysiol.1976.sp011573. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Millecchia R., Mauro A. The ventral photoreceptor cells of Limulus. 3. A voltage-clamp study. J Gen Physiol. 1969 Sep;54(3):331–351. doi: 10.1085/jgp.54.3.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Millecchia R., Mauro A. The ventral photoreceptor cells of Limulus. II. The basic photoresponse. J Gen Physiol. 1969 Sep;54(3):310–330. doi: 10.1085/jgp.54.3.310. [DOI] [PMC free article] [PubMed] [Google Scholar]
- PORTZEHL H., CALDWELL P. C., RUEEGG J. C. THE DEPENDENCE OF CONTRACTION AND RELAXATION OF MUSCLE FIBRES FROM THE CRAB MAIA SQUINADO ON THE INTERNAL CONCENTRATION OF FREE CALCIUM IONS. Biochim Biophys Acta. 1964 May 25;79:581–591. doi: 10.1016/0926-6577(64)90224-4. [DOI] [PubMed] [Google Scholar]
- Payne R., Fein A. Localized adaptation within the rhabdomeral lobe of Limulus ventral photoreceptors. J Gen Physiol. 1983 May;81(5):767–769. doi: 10.1085/jgp.81.5.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Skalska-Rakowska J. M., Baumgartner B. Longitudinal continuity of the subrhabdomeric cisternae in the photoreceptors of the compound eye of the drone, Apis mellifera. Experientia. 1985 Jan 15;41(1):43–45. doi: 10.1007/BF02005864. [DOI] [PubMed] [Google Scholar]
- Stern J., Chinn K., Bacigalupo J., Lisman J. Distinct lobes of Limulus ventral photoreceptors. I. Functional and anatomical properties of lobes revealed by removal of glial cells. J Gen Physiol. 1982 Dec;80(6):825–837. doi: 10.1085/jgp.80.6.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsien R. Y., Pozzan T., Rink T. J. Calcium homeostasis in intact lymphocytes: cytoplasmic free calcium monitored with a new, intracellularly trapped fluorescent indicator. J Cell Biol. 1982 Aug;94(2):325–334. doi: 10.1083/jcb.94.2.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsien R. Y., Rink T. J. Ca2+-selective electrodes: a novel PVC-gelled neutral carrier mixture compared with other currently available sensors. J Neurosci Methods. 1981 Jun;4(1):73–86. doi: 10.1016/0165-0270(81)90020-0. [DOI] [PubMed] [Google Scholar]
- Tsien R. Y., Rink T. J. Neutral carrier ion-selective microelectrodes for measurement of intracellular free calcium. Biochim Biophys Acta. 1980 Jul;599(2):623–638. doi: 10.1016/0005-2736(80)90205-9. [DOI] [PubMed] [Google Scholar]
- Walz B. Subcellular calcium localization and AT0-dependent Ca2+-uptake by smooth endoplasmic reticulum in an invertebrate photoreceptor cell. An ultrastrucutral, cytochemical and X-ray microanalytical study. Eur J Cell Biol. 1979 Oct;20(1):83–91. [PubMed] [Google Scholar]
- 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]
- Yeandle S., Spiegler J. B. Light-evoked and spontaneous discrete waves in the ventral nerve photoreceptor of Limulus. J Gen Physiol. 1973 May;61(5):552–571. doi: 10.1085/jgp.61.5.552. [DOI] [PMC free article] [PubMed] [Google Scholar]
