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Different photoreceptors within the same retina express unique combinations of potassium channels

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Abstract

Single electrode current and voltage clamp recordings in Calliphora, and whole-cell voltage clamp recordings in Drosophila were used to characterise the voltage-gated K channels in both major classes of photoreceptors, R7/8 (long visual fibres, LVFs) and R1-6 (short visual fibres, SVFs). R7/8 were identified by their unique spectral properties, ca. 3–4 fold higher input resistances and 3–4 fold lower cell capacitance. In Calliphora SVFs possess both fast and slow activating delayed rectifier potassium conductances. Drosophila SVFs possess a slowly inactivating delayed rectifier (IKs), a very rapidly inactivating A channel encoded by the Shaker gene (IA), and, in a minority of cells, a third K conductance with intermediate kinetics (IKf). In both specs the LVFs lack the slowest component, but exhibit the faster K conductance(s) with properties indistinguishable from those in the SVFs. These findings add to established evidence demonstrating the significant role played by potassium channels in tuning the photoreceptor membrane. The results also suggest that R1-6 photoreceptors and R7/8 form inputs to visual subsystems tuned to different temporal frequencies.

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Abbreviations

LVF :

long visual fibre

SVF :

short visual fibre

R1-6 :

retinular cells 1 to 6 inclusive

R7/8 :

retinular cell 7 and 8

I A :

rapidly inactivating ‘A’ type potassium conductance; channel coded by Shaker gene

I Kf :

rapidly activating, slowly inactivating delayed rectifier-like potassium conductance

I Ks :

slowly activating, slowly inactivating delayed rectifier-like potassium conductance

I KDs :

slowly activating delayed rectifier potassium conductance

I KDf :

rapidly activating delayed rectifier potassium conductance

References

  • Barnes S (1994) After transduction: response shaping and control of transmission by ion channels of the photoreceptor inner segment. Neuroscience 58: 447–459

    Google Scholar 

  • Cosens D, Spatz H-Ch (1978) Flicker fusion studies in the lamina and receptor region of the Drosophila eye. J Insect Physiol 21: 1111–1120

    Google Scholar 

  • Cuttle MF, Hevers W, Laughlin SB, Hardie RC (1995) Diurnal modulation of photoreceptor potassium conductance in the locust. J Comp Physiol A 176: 307–316

    Google Scholar 

  • Fatt P, Katz B (1951) An analysis of the end-plate potential recorded with an intracellular electrode. J Physiol (Lond) 121: 374–389

    Google Scholar 

  • Fettiplace R (1985) Electrical tuning of hair cells in the inner ear. Trends Neurosci 10: 421–425

    Google Scholar 

  • Fischbach KF (1983) Neural cell types surviving congenital sensory deprivation in the optic lobes of Drosophila melanogaster. Dev Biol 95: 1–18

    Google Scholar 

  • Fischbach KF, Dittrich APM (1989) The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258: 441–475

    Google Scholar 

  • Hardie RC (1979) Electrophysiological analysis of fly retina I: Comparative properties of R1–6 and R7 and 8. J Comp Physiol 129: 19–33

    Google Scholar 

  • Hardie RC (1985) Functional organisation of the fly retina. Progr Sens Physiol 5: 1–79

    Google Scholar 

  • Hardie RC (1986) The photoreceptor array of the dipteran retina. Trends Neurosci 9: 419–423

    Google Scholar 

  • Hardie RC (1991) Voltage sensitive potassium channels in Drosophila photoreceptors. J Neurosci 11: 3079–3095

    Google Scholar 

  • Hardie RC, Voss D, Pong O, Laughlin SB (1991) Novel potassium channels encoded by the Shaker locus in Drosophila photoreceptors. Neuron 6: 477–486

    Google Scholar 

  • Hardie RC, Mojet MH (1995) Magnesium dependent block of the light-activated- and trp-dependent conductance in Drosophila photoreceptors J Neurophysiol (in press)

  • Hateren JH van (1992) A theory of maximising sensory information. Biol Cybern 68: 23–29

    Google Scholar 

  • Hevers W, Hardie RC (1995) Serotonin modulates the voltage dependence of delayed rectifier and Shaker potassium channels in Drosophila photoreceptors. Neuron 14: 845–856

    Google Scholar 

  • Hodgkin AL, Huxley AF (1952) Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J Physiol (Lond) 116: 449–472

    Google Scholar 

  • Kirschfeld K, Feiler R, Franceschini N (1978) A photostable pigment within the rhabdomere of fly photorecepor no. 7. J Comp Physiol 125: 275–284

    Google Scholar 

  • Laughlin SB (1987) Form and function in retinal processing. Trends Neurosci 10: 478–483

    Google Scholar 

  • Laughlin SB (1994) Matching, coding, circuits, cells and molecules to signals: general principles of retinal design in the fly's eye. Prog Ret Eye Res 13: 165–196

    Google Scholar 

  • Laughlin SB, Weckström M (1993) Fast and slow photoreceptors — a comparative study of the functional diversity of coding and conductances in the Diptera. J Comp Physiol A 172: 593–609

    Google Scholar 

  • Pongs O, Kecskemethy N, Muller R, Krah-Jentgens I, Baumann A, Kiltz H, Canal I, Llamazares S, Ferrus A (1988) Shaker encodes a family of putative potassium channel proteins in the nervous system of Drosophila. EMBO J 77: 1087–1096

    Google Scholar 

  • Ramon y, Cajal S, Sanchez D (1915) Contribucion al conocimiento de los insectos. Trab Lab Invest Biol Univ Madrid 13: 1–168

    Google Scholar 

  • Roberts WM (1994) Localisation of Calcium signals by a mobile Calcium buffer in frog saccular hair cells. J Neurosci 14: 3246–3262

    Google Scholar 

  • Roberts WM, Jacobs RA, Hudspeth AJ (1990) Colocalisation of ion channnels involved in frequency-selectivity and synaptic transmission at presynaptic zones of hair cells. J Neurosci 10: 3664–3684

    Google Scholar 

  • Rudy B (1988) Diversity and ubiquity of K channels. Neuroscience 25: 729–749

    Google Scholar 

  • Strausfeld NJ, Blest D (1970) Golgi studies on insects Part I. The optic lobes of Diptera. Phil Trans R Soc Lond B 258: 81–223

    Google Scholar 

  • Strausfeld NJ (1989) Beneath the compound eye: neuroanatomical analysis and physiological correlates in the study of insect vision. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Berlin/Heidelberg, pp 317–359

    Google Scholar 

  • Troje N (1993) Spectral categories in the learning behaviour of blowflies. Z Naturforsch 48: 96–104

    Google Scholar 

  • Trujillo-Cenóz O (1972) The structural organisation of the compound eye in insects. In: Fuortes MGF (ed) Handbook of sensory physiology, vol. VII/2. Springer, Berlin/Heidelberg New York, pp5–62

    Google Scholar 

  • Weckström M, Laughlin SB (1995) Visual ecology and voltage-gated ion channels in insect photoreceptors. Trends Neurosci 18: 17–21

    Google Scholar 

  • Weckström M, Hardie RC, Laughlin SB (1991) Voltage-activated potassium channels in Blowfly photoreceptors and their role in light adaptation. J Physiol (Lond) 440: 635–657

    Google Scholar 

  • Wu C-F, Wong F (1977) Frequency characteristics in the visual system of Drosophila: genetic dissection of electroretinogram components. J Gen Physiol 69: 705–724

    Google Scholar 

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Anderson, J., Hardie, R.C. Different photoreceptors within the same retina express unique combinations of potassium channels. J Comp Physiol A 178, 513–522 (1996). https://doi.org/10.1007/BF00190181

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