Skip to main content
×
Home
    • Aa
    • Aa

Light regulation of Ca2+ in the cone photoreceptor synaptic terminal

  • SUE-YEON CHOI (a1), SKYLER JACKMAN (a2), WALLACE B. THORESON (a3) and RICHARD H. KRAMER (a1)
Abstract
Abstract

Retinal cones are depolarized in darkness, keeping voltage-gated Ca2+ channels open and sustaining exocytosis of synaptic vesicles. Light hyperpolarizes the membrane potential, closing Ca2+ channels and suppressing exocytosis. Here, we quantify the Ca2+ concentration in cone terminals, with Ca2+ indicator dyes. Two-photon ratiometric imaging of fura-2 shows that global Ca2+ averages ~360 nM in darkness and falls to ~190 nM in bright light. Depolarizing cones from their light to their dark membrane potential reveals hot spots of Ca2+ that co-label with a fluorescent probe for the synaptic ribbon protein ribeye, consistent with tight localization of Ca2+ channels near ribbons. Measurements with a low-affinity Ca2+ indicator show that the local Ca2+ concentration near the ribbon exceeds 4 μM in darkness. The high level of Ca2+ near the ribbon combined with previous estimates of the Ca2+ sensitivity of release leads to a predicted dark release rate that is much faster than observed, suggesting that the cone synapse operates in a maintained state of synaptic depression in darkness.

Copyright
Corresponding author
*Address correspondence to: Richard H. Kramer, Department of Molecular and Cell Biology, University of California, 121 Life Sciences Addition, Berkeley, CA 94720-3200. E-mail: rhkramer@berkeley.edu
References
Hide All
Augustine G.J., Santamaria F. & Tanaka K. (2003). Local calcium signaling in neurons. Neuron 40, 331346.
Baldridge W.H., Kurennyi D.E. & Barnes S. (1998). Calcium-sensitive calcium influx in photoreceptor inner segments. J Neurophysiol 79, 30123018.
Baylor D.A. & Fuortes M.G. (1970). Electrical responses of single cones in the retina of the turtle. J Physiol 207, 7792.
Cadetti L., Bryson E.J., Ciccone C.A., Rabl K. & Thoreson W.B. (2006). Calcium-induced calcium release in rod photoreceptor terminals boosts synaptic transmission during maintained depolarization. Eur J Neurosci 23, 29832990.
Cervetto L. & Piccolino M. (1974). Synaptic transmission between photoreceptors and horizontal cells in the turtle retina. Science 183, 417419.
Choi S.Y., Borghuis B.G., Rea R., Levitan E.S., Sterling P. & Kramer R.H. (2005 a). Encoding light intensity by the cone photoreceptor synapse. Neuron 48, 555562.
Choi S.Y., Sheng Z. & Kramer R.H. (2005 b). Imaging light-modulated release of synaptic vesicles in the intact retina: Retinal physiology at the dawn of the post-electrode era. Vision Res 45, 34873495.
Corey D.P., Dubinsky J.M. & Schwartz E.A. (1984). The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina. J Physiol 354, 557575.
Demuro A. & Parker I. (2006). Imaging single-channel calcium microdomains. Cell Calcium 40, 413422.
DeVries S.H. & Schwartz E.A. (1999). Kainate receptors mediate synaptic transmission between cones and ‘Off’ bipolar cells in a mammalian retina. Nature 397, 157160.
Fesenko E.E., Kolesnikov S.S. & Lyubarsky A.L. (1985). Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313, 310313.
Grynkiewicz G., Poenie M. & Tsien R.Y. (1985). A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260, 34403450.
Heidelberger R., Thoreson W.B. & Witkovsky P. (2005). Synaptic transmission at retinal ribbon synapses. Prog Retin Eye Res 24, 682720.
Helmchen F. (2000). Calibration of fluorescent calcium indicators. In Imaging Neurons: A Laboratory Manual, ed. Yuste R., Lanni F. & Konnerth A., chap. 32, pp. 132. New York: Cold Spring Harbor Laboratory Press.
Issa N.P. & Hudspeth A.J. (1996). Characterization of fluo-3 labeling of dense bodies at the hair cell's presynaptic active zone. J Neurocytol 25, 257266.
Johnson J.E. Jr, Perkins G.A., Giddabasappa A., Chaney S., Xiao W., White A.D., Brown J.M., Waggoner J., Ellisman M.H. & Fox D.A. (2007). Spatiotemporal regulation of ATP and Ca2+ dynamics in vertebrate rod and cone ribbon synapses. Mol Vis 13, 887919.
Krizaj D., Bao J.X., Schmitz Y., Witkovsky P. & Copenhagen D.R. (1999). Caffeine-sensitive calcium stores regulate synaptic transmission from retinal rod photoreceptors. J Neurosci 19, 72497261.
Krizaj D. & Copenhagen D.R. (1998). Compartmentalization of calcium extrusion mechanisms in the outer and inner segments of photoreceptors. Neuron 21, 249256.
Krizaj D., Lai F.A. & Copenhagen D.R. (2003). Ryanodine stores and calcium regulation in the inner segments of salamander rods and cones. J Physiol 547, 761774.
Matthews G. (1996). Synaptic exocytosis and endocytosis: Capacitance measurements. Curr Opin Neurobiol 6, 358364.
Morgans C.W. (2001). Localization of the δ1F calcium channel subunit in the rat retina. Invest Ophthalmol Vis Sci 42, 24142418.
Morgans C.W., El Far O., Berntson A., Wässle H. & Taylor W.R. (1998). Calcium extrusion from mammalian photoreceptor terminals. J Neurosci 18, 24672474.
Nachman-Clewner M., St. Jules R. & Townes-Anderson E. (1999). L-type calcium channels in the photoreceptor ribbon synapse: Localization and role in plasticity. J Comp Neurol 415, 116.
Naraghi M. & Neher E. (1997). Linearized buffered Ca2+ diffusion in microdomains and its implications for calculation of [Ca2+] at the mouth of a calcium channel. J Neurosci 17, 69616973.
Prescott E.D. & Zenisek D. (2005). Recent progress towards understanding the synaptic ribbon. Curr Opin Neurobiol 15, 4314343146.
Rabl K., Cadetti L. & Thoreson W.B. (2005). Kinetics of exocytosis is faster in cones than rods. J Neurosci 25, 46334640.
Rabl K., Cadetti L. & Thoreson W.B. (2006). Paired-pulse depression at photoreceptor synapses. J Neurosci 26, 25552563.
Raviola E. & Gilula N.B. (1975). Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. J Cell Biol 75, 192222.
Rea R., Li J., Dharia A., Levitan E.S., Sterling P. & Kramer R.H. (2004). Streamlined synaptic vesicle cycle in cone photoreceptor terminals. Neuron 4, 755766.
Rieke F. & Schwartz E. (1996). Asynchronous transmitter release: Control of exocytosis and endocytosis at the salamander rod synapse. J Physiol 493, 18.
Savchenko A., Barnes S. & Kramer R.H. (1997). Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide. Nature 390, 694698.
Schneggenburger R. & Neher E. (2005). Presynaptic calcium and control of vesicle fusion. Curr Opin Neurobiol 15, 266274.
Sheng Z., Choi S.Y., Dharia A., Li J., Sterling P. & Kramer R.H. (2007). Synaptic Ca2+ in darkness is lower in rods than cones, causing slower tonic release of vesicles. J Neurosci 27, 50335042.
Stelzer E.H. (2000). Practical limits to resolution in fluorescence light microscopy. In Imaging Neurons: A Laboratory Manual, ed. Yuste R., Lanni F. & Konnerth A., pp. 12.112.9. New York: Cold Spring Harbor Laboratory Press.
Suryanarayanan A. & Slaughter M.M. (2006). Synaptic transmission mediated by internal calcium stores in rod photoreceptors. J Neurosci 26, 17591766.
Thoreson W.B., Rabl K., Townes-Anderson E. & Heidelberger R. (2004). A highly Ca2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42, 595605.
Thoreson W.B., Tranchina D. & Witkovsky P. (2003). Kinetics of synaptic transfer from rods and cones to horizontal cells in the salamander retina. Neuroscience 122, 785798.
tom Dieck S., Altrock W.D., Kessels M.M., Qualmann B., Regus H., Brauner D., Fejtova A., Bracko O., Gundelfinger E.D. & Brandstätter J.H. (2005). Molecular dissection of the photoreceptor ribbon synapse: Physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J Cell Biol 168, 825836.
Wilkinson M.F. & Barnes S. (1996). The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors. J Gen Physiol 197, 621630.
Zenisek D., Davila V., Wan L. & Almers W. (2003). Imaging calcium entry sites and ribbon structures in two presynaptic cells. J Neurosci 23, 25382548.
Zenisek D., Horst N.K., Merrifield C., Sterling P. & Matthews G. (2004). Visualizing synaptic ribbons in the living cell. J Neurosci 24, 97529759.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 3
Total number of PDF views: 8 *
Loading metrics...

Abstract views

Total abstract views: 154 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 22nd October 2017. This data will be updated every 24 hours.