Abstract
Presynaptic Ca2+channels mediate early stages of visual information processing in photoreceptors by facilitating the release of neurotransmitter and by receiving modulatory input that alters transmission. Two types of L-type Ca2+channels, composed of a1F and a1D subunits and having similar biophysical and pharmacological properties, appear to form the principle voltage-dependent Ca2+influx pathways in rods and cones, respectively. The role played by these channels in neurotransmitter release at these graded potential, non-spiking synapses, has been well described. The channels mediate sustained glutamate release in darkness where the cells rest at potentials near —40 mV, and signal increases in light intensity as the cells hyperpolarize negative to this value. Synaptic modulation and integration mediated by these channels has not yet been as fully described but appears to involve GABA, nitric oxide (NO), glutamate, and dopamine. Cal’ permeable cyclic nucleotide gated (CNG) channels appear to have supporting roles at the photoreceptor output synapse and may transduce NO signals from other cells by either directly permitting Ca2+influx or by providing depolarizing influences that gate voltage dependent Ca2+channels.
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References
Kawai F, Horiguchi M, Suzuki H et al. Na+ Action Potentials in Human Photoreceptors. Neuron 2001; 30:451–458.
Dowling JE. The Retina: An approachable part of the brain. Cambridge: Belknapp Press, 1987.
Attwell D. The photoreceptor output synapse. Progress in Retinal Research 1990; 9:337–362.
Baylor DA, Fuortes MGF, O’Bryan PM. Receptive fields of cones in the retina of the turtle. J Physiol 1971; 214:265–294.
Rieke F, Schwartz EA. A cGMP-gated current can control exocytosis at cone synapses. Neuron 1994; 13:863–873.
Copenhagen DR, Jahr CE. Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 1989; 341:536–539.
Schmitz Y, Witkovsky P. Dependence of photoreceptor glutamate release on a dihydropyridine-sensitive Ca2+channel. Neurosci 1997; 78:1209–16.
Nawy S. The metabotropic receptor mGluR6 may signal through G(o), but not phosphodiesterase, in retinal bipolar cells. J Neurosci 1999; 19:2938–2944.
Attwell D, Borges S, Wu S et al. Signal clipping by the rod output synapse. Nature 1987; 328:522–524.
Barnes S, Merchant V, Mahmud F. Modulation of transmission gain by protons at the photoreceptor output synapse. Proceedings of the National Academy of Science (U.S.A.) 1993; 90:10081–10085.
Savchenko A, Barnes S, Kramer RH. Cyclic nucleotide-gated channels in synaptic terminals mediate feedback modulation by nitric oxide. Nature 1997; 390:694–698.
Hare WA, Owen WG. Similar effects of carbachol and dopamine on neurons in the distal retina of the tiger salamander. Vis Neurosci 1995; 12: 443–455.
Bader CR, Bertrand D, Schwartz EA. Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. J Physiol 1982; 331:253–284.
Corey DP, Dubinsky JM, Schwartz EA The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina. J Physiol 1984; 354:557–575.
Maricq, AV, Korenbrot JI. Calcium and calcium-dependant chloride currents generate action potentials in solitary cone photoreceptors. Neuron 1988; 1:503–515.
Barnes S, Hille B. Ionic channels of the inner segment of tiger salamander cone photoreceptors. J Gen Physiol 1989; 94:719–743.
Lasater EM, Witkovsky P. The calcium current of turtle cone photoreceptor axon terminals. Neuroscience Research Supplement 1991; 15:S165–S173.
Yagi T, Macleish PR. Ionic conductances of monkey solitary cone inner segments. J Neurophysiol 1994; 71:656–65.
Wilkinson MF, Barnes S. The dihydropyridine-sensitive Ca2+channel subtype in cone photoreceptors. J Gen Physiol 1996; 107:621–630.
Taylor WR, Morgans C. Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangeri. Vis Neurosci 1998; 15:541–52.
Kourennyi DK, Barnes S. Depolarization-induced calcium channel facilitation in rod photoreceptors is independent of G-proteins and phosphorylation. J Neurophysiol 2000; 84:133–138.
Williams ME, Feldman, DH, McCue AF et al. Structure and functional expression of alphal, alpha2, and beta subunits of a novel human neuronal calcium channel. Neuron 1992; 8:71–84.
Bech-Hansen NT, Naylor MJ, Maybaum TA et al. Loss-of-function mutations in a calcium-channel alphal-subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness. Nat Genet 1998; 19:264–7
Strom TM, Nyakatura G, Apfelstedt-Sylla E et al. An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nat Genet 1998; 19:260–263.
Morgans CW. Localization of the alpha(1F) Calcium channel subunit in the rat retina. Invest Ophth Vis Sci 2001; 42:2414–2418.
Morgans CW. Calcium channel heterogeneity among cone photoreceptors in the tree shrew retina. Eur J Neurosci 2000; 11:2989–2993.
Nachman-Clewner M, St. Jules R, Townes-Anderson E. L-type calcium channels in the photoreceptor ribbon synapse: Localization and role in plasticity. J Comp Neurol 1999; 415:1–16.
Barnes S. Modulation of vertebrate retinal function by pH. In: K Kaila, BR Ransom, eds. pH and Brain Function. New York: John Wiley & Sons Inc., 1998.
Harsanyi K, Mangel SC. Modulation of cone to horizontal cell transmission by calcium and pH in the fish retina. Vis Neurosci 1993; 10:81–91.
DeVries SH. Exocytosed protons feedback to suppress the Ca2+current in mammalian cone photoreceptors. Neuron 2001; 32:1107–1117.
Piccolino M, Byzov AL, Kurenny DE et al. Low-calcium-induced enhancement of chemical synaptic transmission from photoreceptors to horizontal cells in the vertebrate retina. Proceedings of the National Academy of Science (USA) 1996; 93:2302–2306.
Piccolino M, Vellani V, Rakotobe LA et al. Manipulation of synaptic sign and strength with divalent cations in the vertebrate retina: Pushing the limits of tonic, chemical neurotransmission. Eur J Neurosci 1999; 11:1–5.
Baldridge WK, Kurennyi DK, Barnes S. Calcium-sensitive calcium influx in photoreceptor inner segments. J Neurophysiol 1998; 79:3012–3018.
Thoreson WB, Nitzan R, Miller RF. Reducing extracellular Cl-suppresses dihydropyridine-sensitive Ca2+ currents and synaptic transmission in amphibian photoreceptors. J Neurophysiol 1997; 77:2175–90.
Thoreson WB, Stella SL. Anion modulation of calcium current voltage dependence and amplitude in salamander rods. Biochem Biophys Acta 2000; 1464:142–50.
Byzov AL, Shura-Bura TM. Electric feedback mechanism in the processing of signals in the outer plexiform layer of the retina. Brain Res 1986; 26:33–44.
Watanabe S, Matthews G. Regional distribution of cGMP-activation ion channels in plasma membrane of rod photoreceptors. J Neurosci 1988; 8:2334–2337.
Werblin FS, Dowling JE. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J Neurophysiol. 1969; 32:339–355.
Cook PB, McReynolds JS. Lateral inhibition in the inner retina is important for spatial tuning of ganglion cells. Nature Neurosci 1998; 1:711–719.
Kaneko A, Shimazaki H. Synaptic transmission from photoreceptors to bipolar and horizontal cells in the carp retina. Cold Spring Harbor Symp Quant Biol 1976; 40:537–546.
Burkhardt DA. Synaptic feedback, depolarization, and color opponency in cone photoreceptors. Vis Neurosci 1993; 10:981–9.
Lam DMK. Biosynthesis of gamma-aminobutyric acid by isolated axons of cone horizontal cells in the goldfish retina. Nature 1975; 254:345–347.
Murakami M, Shimoda Y, Nakatani K et al. GABA-mediated negative feedback from horizontal cells to cones in carp retina. Jap J Physiol 1982; 32:911–926.
Kaneko A, Tachibana M. Effects of gamma-butyric acid on isolated cone photoreceptors of the turtle retina. J Physiol 1986; 373:443–461.
Wu SM. Effects of gamma-butyric acid on cones and bipolar cells of the tiger salamander retina. Brain Res 1986; 365:70–77.
Skrzypek J, Werblin F. Lateral interactions in the absence of feedback to cones. J Neurophysiol 1983; 49:1007–1017.
O’Bryan PM. Properties of the depolarizing synaptic potential evoked by peripheral illumination in cones of the turtle retina. J Physiol 1973; 235:207–223.
Lasansky A. Synaptic action mediating cone responses to annular illumination in the retina of the larval tiger salamander. J Physiol 1981; 310:205–14.
Piccolino M, Gerschenfeld HM. Activation of a regenerative calcium conductance in turtle cones by peripheral stimulation. Proc R Soc London B 1978; 201:309–315.
Thoreson WB, Burkhardt DA. Effects of synaptic blocking agents on the depolarizing responses of turtle cones evoked by surround illumination. Vis Neurosci 1990 5:571–83.
Snyder SH. Nitric oxide and neurons. Curr Opin Neurobiol 1992; 2:323–327.
Kelly MEM, Barnes S. Physiology and pathophysiology of nitric oxide in the retina. The Neuroscientist 1997; 3:357–360.
Peretz MTR, Larsson B, Alm P et al. Localisation of neuronal nitric oxide synthaseimmunoreactivity in rat and rabbit reitnas. Exp Brain Res 1995; 104:207–217.
Yamamoto R, Bredt DS, Snyder SH et al. The localization of nitric oxide synthase in the rat eye and related cranial ganglia. Neuroscience 1993; 54:189–200.
Liepe BA, Stone C, Koistanaho J et al. Nitric oxide synthase in Muller cells and neurons of salamander and fish retina. J Neurosci 1994; 14:7641–7654
Blute TA, Mayer B, Eldred WD. Immunocytochemical and histochemical localization of nitric oxide synthase in the turtle retina. Vis Neurosci 1997; 14:717–729.
Kurenny DE, Moroz LL, Turner RW et al. Modulation of ion channels in rod photoreceptors by nitric oxide. Neuron 1994; 13:315–324.
Kurennyi DE, Baldridge W, Hart J et al. Differential action of the nitric oxide donor S-nitrosocysteine on calcium channels in cone versus rod photoreceptors. Soc Neurosci Abstr 1997; 23:449.
Morgan IG, Boelen MK. A retinal light-dark switch: a review of the evidence. Vis Neurosci 1996; 13:399–409.
Djamgoz MB, Hankins MW, Hirano J et al. Neurobiology of retinal dopamine in relation to degenerative states of the tissue. Vis Res 1997; 37:3509–3529.
Krizaj D, Witkovsky P. Effects of submicromolar concentrations of dopamine on photoreceptor to horizontal cell communication. Brain Res 1993; 627:122–128.
Akopian A, Witkovsky P. D2-dopamine receptor mediated inhibition of a hyperpolarization-activated current in rod photoreceptors. J Neurophysiol 1996; 76:1828–1835.
Barnes S. After transduction: Response shaping and control of transmission by ion channels of the photoreceptor inner segment. Neuroscience 1994; 58:447–459.
Stella SL, Thoreson WB. Differential modulation of rod and cone calcium currents in tiger salamander retina by D2 dopamine receptors and cAMP. Eur J Neurosci 2000; 12:3537–48.
Koulen P, Kuhn R, Wassle H et al. Modulation of the intracellular calcium concentration in photoreceptor terminals by a presynaptic metabotropic glutamate receptor. PNAS 1996; 96:9909–9914
Kamermans M, Fahrenfort I, Schultz K et al. Hemichannel-mediated inhibition in the outer retina. Science 2001; 292:1178–1180.
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Barnes, S., Kelly, M.E.M. (2002). Calcium Channels at the Photoreceptor Synapse. In: Baehr, W., Palczewski, K. (eds) Photoreceptors and Calcium. Advances in Experimental Medicine and Biology, vol 514. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0121-3_28
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DOI: https://doi.org/10.1007/978-1-4615-0121-3_28
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