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Analysis of extracellular calcium and volume changes in the compound eye of the honeybee drone,Apis mellifera

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Summary

Superfused slices of drone retina were used for a quantitative analysis of light-induced changes in extracellular Ca2+ concentration ([Ca2+]o) and extracellular space (ECS) volume. 20-ms light flashes elicited biphasic changes in [Ca2+]o. For a saturating flash a brief, initial decrease was followed by a transient increase of 120±34 μM. Long, dim steps of light (5 min) produced either a decrease or an increase in [Ca2+]o depending strongly on the previous illumination. Brighter continuous lights caused the [Ca2+]o to increase transiently by 1.4 mM to a peak from which it decayed to a plateau, up to 0.6 mM above the dark concentration.

Light flashes (20 ms) caused a shrinkage in ECS volume not exceeding 4%. Thus, changes in [Ca2+]o were almost completely due to Ca2+ fluxes between the ECS and adjacent cells. Continuous lights caused a shrinkage in ECS volume rarely exceeding 16%–20%. Thus, less than 15% of the measured Ca2+ changes could be attributed to shrinkage of the ECS. These data confirm that the ECS functions as a source and a sink for Ca2+ mobilized by light. For comparison, we also made a few measurements of changes in [Ca2+]o in the retina ofCalliphora.

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Abbreviations

[Ca 2+]i :

intracellular free Ca2+ concentration

[Ca 2+]o :

extracellular free Ca2+ concentration

ECS :

extracellular space

ER :

endoplasmic reticulum

TMA + :

tetramethylammonium ion

References

  • Bader CR, Baumann F, Bertrand D (1976) Role of intracellular calcium and sodium in light adaptation in the retina of the honey bee drone (Apis mellifera). J Gen Physiol 67:475–491

    Google Scholar 

  • Baumann F (1974) Electrophysiological properties of the honey bee retina. In: Horridge GA (ed) The compound eye and vision in insects. Clarendon, Oxford, pp 53–74

    Google Scholar 

  • Baumann O, Walz B (1989) Topography of Ca2+-sequestering endoplasmic reticulum in photoreceptors and pigmented glial cells in the compound eye of the honey bee drone. Cell Tissue Res 255:511–522

    Google Scholar 

  • Baumann O, Walz B (1989) Calcium- and inositol polyphosphate-sensitivity of the calcium-sequestering endoplasmic reticulum in the photoreceptor cells of the honeybee drone. J Comp Physiol A 165:627–636

    Google Scholar 

  • Bertrand D, Fuortes G, Muri R (1979) Pigment transformation and electrical responses in retinula cells of drone,Apis mellifera. J Physiol 296:431–441

    Google Scholar 

  • Bolsover SR, Brown JE (1985) Calcium ion, an intracellular messenger of light adaptation, also participates in excitation ofLimulus ventral photoreceptor cells. J Physiol 364:389–393

    Google Scholar 

  • Brown JE (1986) Calcium and light adaptation in invertebrate photoreceptors. In: Stieve H (ed) The molecular mechanism of photoreception. Springer, Berlin Heidelberg New York, pp 231–240

    Google Scholar 

  • Brown JE, Blinks JR (1974) Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin. J Gen Physiol 64:643–665

    Google Scholar 

  • Brown JE, Mote MI (1974) Ionic dependence of reversal voltage of the light response inLimulus ventral photoreceptors. JGen Physiol 63:337–350

    Google Scholar 

  • Carafoli E (1987) Intracellular calcium homeostasis. Annu Rev Biochem 56:395–433

    Google Scholar 

  • Coles JA, Orkand RK (1983) Modification of potassium movement through the retina of the drone (Apis mellifera) by glial uptake. J Physiol 340:157–174

    Google Scholar 

  • Coles JA, Orkand RK (1985) Changes in sodium activity during light stimulation in photoreceptors, glia, and extracellular space in drone retina. J Physiol 362:415–435

    Google Scholar 

  • Coles JA, Orkand RK, Yamate CL, Tsacopoulos M (1986) Free concentrations of Na, K, and Cl in the retina of the honey bee drone: Stimulus-induced redistribution and homeostasis. Ann NY Acad Sci 481:303–317

    Google Scholar 

  • Coles JA, Tsacopoulos M, Rabineau P, Gardner-Medwin AR (1981) Movements of potassium into glial cells in the retina of the drone,Apis mellifera, during photostimulation. In: Syková E (ed) Ion selective microelectrodes and their use in excitable tissue. Plenum, New York, pp 345–349

    Google Scholar 

  • Connors BW, Ransom BR, Kunis DM, Gutnik MJ (1982) Activity-dependent K+ accumulation in the developing rat optic nerve. Science 216:1341–1343

    Google Scholar 

  • Dietzel I, Heinemann U, Hofmeier G, Lux HD (1980) Transient changes in the size of the extracellular space in the sensomotor cortex of cats in relation to stimulus-induced changes in potassium concentration. Exp Brain Res 40:432–439

    Google Scholar 

  • Fein A, Charlton JS (1977) Increased intracellular sodium mimics some but not all aspects of photoreceptor adaptation in the ventral eye ofLimulus. J Gen Physiol 70:601–620

    Google Scholar 

  • Fulpius B, Baumann F (1969) Effects of sodium, potassium and calcium ions on slow and spike potentials in single photoreceptor cells. J Gen Physiol 53:541–561

    Google Scholar 

  • Hagins WA, Zonana HV, Adams RG (1962) Local membrane current in the outer segments of squid photoreceptors. Nature 194:844–847

    Google Scholar 

  • Hansen AJ, Olsen CE (1980) Brain extracellular space during spreading depression and ischemia. Acta Physiol Scand 108:355–365

    Google Scholar 

  • Hochstrate P, Hamdorf K (1985) The influence of extracellular calcium on the response of fly photoreceptors. J Comp Physiol A 156:53–64

    Google Scholar 

  • Hodgkin AL, McNaughton PA, Nunn BJ (1985) The ionic selectivity and calcium dependence of the light-sensitive pathway in toad rods. J Physiol 358:447–468

    Google Scholar 

  • Ivens I, Stieve H (1984) Influence of the membrane potential on the intracellular light induced Ca2+ concentration change of theLimulus ventral photoreceptor monitored by Arsenazo III under voltage clamp conditions. Z Naturforsch 39c:986–992

    Google Scholar 

  • Lasansky A, Fuortes MGF (1969) The site of origin of electrical responses in visual cells of the leech,Hirudo medicinalis. J Cell Biol 42:241–252

    Google Scholar 

  • Lisman JE, Brown JE (1972) The effects of intracellular iontophoretic injection of calcium and sodium ions on the light response ofLimulus ventral photoreceptors. J Gen Physiol 59:701–719

    Google Scholar 

  • Maaz G, Stieve H (1980) The correlation of the receptor potentials with the light-induced transient increase in intracellular Ca concentration measured by absorption change of A III injected intoLimulus ventral nerve photoreceptor cells. Biophys Struct Mech 9:207–223

    Google Scholar 

  • Miller DL, Korenbrot JI (1987) Kinetics of light-dependent Ca fluxes across the plasma membrane of rod outer segments. J Gen Physiol 90:397–425

    Google Scholar 

  • Minke B, Armon E (1984) Activation of electrogenic Na-Ca exchange by light in fly photoreceptors. Vision Res 24:109–115

    Google Scholar 

  • Minke B, Tsacopoulos M (1986) Light induced sodium dependent accumulation of calcium and potassium in the extracellular space of bee retina. Vision Res 26:679–690

    Google Scholar 

  • Muijser H (1979) The receptor potential of retinular cells of the blowfly,Calliphora: the role of sodium, potassium and calcium ions. J Comp Physiol 132:87–95

    Google Scholar 

  • Munoz JL, Deyhimi F, Coles JA (1983) Silanization of glass in the making of ion-sensitive microelectrodes. J Neurosci Meth 8:231–247

    Google Scholar 

  • O'Day PM, Lisman JE, Goldring M (1982) Functional significance of voltage-dependent conductances inLimulus ventral photoreceptors. J Gen Physiol 79:211–232

    Google Scholar 

  • Oehme M, Simon W (1976) Microelectrode for potassium ions based on a neutral carrier and comparison of its characteristics with a cation exchanger sensor. Anal Chim Acta 86:21–25

    Google Scholar 

  • Oehme M, Kessler M, Simon W (1976) Neutral carrier Ca2+- microelectrode. Chimia 30:204–206

    Google Scholar 

  • Orkand RK, Dietzel I, Coles JA (1984) Light-induced changes in extracellular volume in the retina of the drone,Apis mellifera. Neurosci Lett 45:273–278

    Google Scholar 

  • Payne R, Fein A (1986) Localization of the photocurrent ofLimulus ventral photoreceptors using a vibrating probe. Biophys J 50:193–196

    Google Scholar 

  • Payne R, Corson DW, Fein A, Berridge MJ (1986) Excitation and adaptation ofLimulus ventral photoreceptor by inositol (1,4,5,) trisphosphate results from a rise in intracellular calcium. J Gen Physiol 88:127–142

    Google Scholar 

  • Payne R, Walz B, Levy S, Fein A (1988) The localization of calcium release by inositol trisphosphate inLimulus photoreceptors and its control by negative feedback. Phil Trans R Soc B 320:359–379

    Google Scholar 

  • Perrelet A, Bader CR (1978) Morphological evidence for calcium stores in photoreceptors of the honey bee drone retina. J Ultrastruct Res 63:237–243

    Google Scholar 

  • Phillips JM, Nicholson C (1979) Anion permeability in spreading depression investigated with ion-sensitive microelectrodes. Brain Res 173:567–571

    Google Scholar 

  • Raggenbass M (1983) Effects of extracellular calcium and of light adaptation on the response to dim light in honey bee drone photoreceptors. J Physiol 344:527–548

    Google Scholar 

  • Sandler C, Kirschfeld K (1988) Light intensity controls extracellular Ca2+ concentration in the blowfly retina. Naturwissenschaften 75:256–258

    Google Scholar 

  • Tsien RY, Rink TJ (1980) Neutral carrier ion-selective microelectrodes for measurement of intracellular free calcium. Biochim Biophys Acta 599:623–638

    Google Scholar 

  • Waloga G, Brown JE, Pinto LH (1975) Detection of changes in Ca(in) fromLimulus ventral photoreceptors using arsenazo III. Biol Bull 149:449–450

    Google Scholar 

  • Walz B (1982) Calcium-sequestering endoplasmic reticulum in retinula cells of the blowfly. J Ultrastruct Res 81:240–248

    Google Scholar 

  • Walz B (1985) Light-induced changes of extra- and intracellular potassium concentration in photoreceptors of the leechHirudo medicinalis. J Comp Physiol A 157:199–210

    Google Scholar 

  • Walz B, Coles JA, Poitry S, Levy S (1986) Helladaptation und lichtinduzierte Zunahme der intrazellulären Ca2+ (und Na+) Konzentration sind in den Photorezeptoren der Biene räumlich lokalisiert. Verh Dtsch Zool Ges 79:245–246

    Google Scholar 

  • Walz B, Ziegler A, Baumann O (1988) Extracellular space (ECS) and endoplasmic reticulum (ER) as sources and sinks for Ca2+ mobilized by light in photoreceptors of the honey bee drone. In: Elsner E, Barth FG (eds) Sense organs. Thieme, Stuttgart, p 209

    Google Scholar 

  • Yau K-W, Nakatani K (1984) Cation selectivity of light-sensitive conductance in retinal rods. Nature 309:352–354

    Google Scholar 

  • Yau K-W, Nakatani K (1985) Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment. Nature 313:579–582

    Google Scholar 

Download references

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Ziegler, A., Walz, B. Analysis of extracellular calcium and volume changes in the compound eye of the honeybee drone,Apis mellifera . J. Comp. Physiol. 165, 697–709 (1989). https://doi.org/10.1007/BF00611001

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