Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-18T08:36:11.095Z Has data issue: false hasContentIssue false
  • English
  • Français

Light regulation of Ca2+ in the cone photoreceptor synaptic terminal

Published online by Cambridge University Press:  01 September 2008

SUE-YEON CHOI ,
SKYLER JACKMAN ,
WALLACE B. THORESON  and
RICHARD H. KRAMER
SUE-YEON CHOI
Affiliation:
Department of Molecular and Cell Biology, University of California, Berkeley, California
SKYLER JACKMAN
Affiliation:
Department of Physics, University of California, Berkeley, California
WALLACE B. THORESON
Affiliation:
Department of Ophthalmology and Visual Sciences, University of Nebraska Medical Center, Omaha, Nebraska
RICHARD H. KRAMER*
Affiliation:
Department of Molecular and Cell Biology, University of California, Berkeley, California
*
*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
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

ConePhotoreceptorCa2+Synaptic transmissionExocytosis
Type
Brief Communications
Information
Visual Neuroscience , Volume 25 , Issue 5-6 , September 2008 , pp. 693 - 700
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Augustine, G.J., Santamaria, F. & Tanaka, K. (2003). Local calcium signaling in neurons. Neuron 40, 331–346.CrossRefGoogle ScholarPubMed
Baldridge, W.H., Kurennyi, D.E. & Barnes, S. (1998). Calcium-sensitive calcium influx in photoreceptor inner segments. J Neurophysiol 79, 3012–3018.CrossRefGoogle ScholarPubMed
Baylor, D.A. & Fuortes, M.G. (1970). Electrical responses of single cones in the retina of the turtle. J Physiol 207, 77–92.CrossRefGoogle ScholarPubMed
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, 2983–2990.CrossRefGoogle ScholarPubMed
Cervetto, L. & Piccolino, M. (1974). Synaptic transmission between photoreceptors and horizontal cells in the turtle retina. Science 183, 417–419.CrossRefGoogle ScholarPubMed
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, 555–562.Google Scholar
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, 3487–3495.CrossRefGoogle ScholarPubMed
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, 557–575.CrossRefGoogle ScholarPubMed
Demuro, A. & Parker, I. (2006). Imaging single-channel calcium microdomains. Cell Calcium 40, 413–422.CrossRefGoogle ScholarPubMed
DeVries, S.H. & Schwartz, E.A. (1999). Kainate receptors mediate synaptic transmission between cones and ‘Off’ bipolar cells in a mammalian retina. Nature 397, 157–160.Google Scholar
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, 310–313.CrossRefGoogle ScholarPubMed
Grynkiewicz, G., Poenie, M. & Tsien, R.Y. (1985). A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260, 3440–3450.Google Scholar
Heidelberger, R., Thoreson, W.B. & Witkovsky, P. (2005). Synaptic transmission at retinal ribbon synapses. Prog Retin Eye Res 24, 682–720.CrossRefGoogle ScholarPubMed
Helmchen, F. (2000). Calibration of fluorescent calcium indicators. In Imaging Neurons: A Laboratory Manual, ed. Yuste, R., Lanni, F. & Konnerth, A., chap. 32, pp. 1–32. New York: Cold Spring Harbor Laboratory Press.Google Scholar
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, 257–266.CrossRefGoogle ScholarPubMed
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, 887–919.Google ScholarPubMed
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, 7249–7261.Google Scholar
Krizaj, D. & Copenhagen, D.R. (1998). Compartmentalization of calcium extrusion mechanisms in the outer and inner segments of photoreceptors. Neuron 21, 249–256.Google Scholar
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, 761–774.CrossRefGoogle ScholarPubMed
Matthews, G. (1996). Synaptic exocytosis and endocytosis: Capacitance measurements. Curr Opin Neurobiol 6, 358–364.Google Scholar
Morgans, C.W. (2001). Localization of the δ1F calcium channel subunit in the rat retina. Invest Ophthalmol Vis Sci 42, 2414–2418.Google Scholar
Morgans, C.W., El Far, O., Berntson, A., Wässle, H. & Taylor, W.R. (1998). Calcium extrusion from mammalian photoreceptor terminals. J Neurosci 18, 2467–2474.CrossRefGoogle ScholarPubMed
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, 1–16.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
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, 6961–6973.CrossRefGoogle ScholarPubMed
Prescott, E.D. & Zenisek, D. (2005). Recent progress towards understanding the synaptic ribbon. Curr Opin Neurobiol 15, 43143–43146.Google Scholar
Rabl, K., Cadetti, L. & Thoreson, W.B. (2005). Kinetics of exocytosis is faster in cones than rods. J Neurosci 25, 4633–4640.Google Scholar
Rabl, K., Cadetti, L. & Thoreson, W.B. (2006). Paired-pulse depression at photoreceptor synapses. J Neurosci 26, 2555–2563.CrossRefGoogle ScholarPubMed
Raviola, E. & Gilula, N.B. (1975). Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. J Cell Biol 75, 192–222.CrossRefGoogle Scholar
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, 755–766.CrossRefGoogle Scholar
Rieke, F. & Schwartz, E. (1996). Asynchronous transmitter release: Control of exocytosis and endocytosis at the salamander rod synapse. J Physiol 493, 1–8.Google Scholar
Savchenko, A., Barnes, S. & Kramer, R.H. (1997). Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide. Nature 390, 694–698.Google Scholar
Schneggenburger, R. & Neher, E. (2005). Presynaptic calcium and control of vesicle fusion. Curr Opin Neurobiol 15, 266–274.Google Scholar
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, 5033–5042.Google Scholar
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. 12.1–12.9. New York: Cold Spring Harbor Laboratory Press.Google Scholar
Suryanarayanan, A. & Slaughter, M.M. (2006). Synaptic transmission mediated by internal calcium stores in rod photoreceptors. J Neurosci 26, 1759–1766.CrossRefGoogle ScholarPubMed
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, 595–605.CrossRefGoogle ScholarPubMed
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, 785–798.Google Scholar
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, 825–836.Google Scholar
Wilkinson, M.F. & Barnes, S. (1996). The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors. J Gen Physiol 197, 621–630.CrossRefGoogle Scholar
Zenisek, D., Davila, V., Wan, L. & Almers, W. (2003). Imaging calcium entry sites and ribbon structures in two presynaptic cells. J Neurosci 23, 2538–2548.CrossRefGoogle ScholarPubMed
Zenisek, D., Horst, N.K., Merrifield, C., Sterling, P. & Matthews, G. (2004). Visualizing synaptic ribbons in the living cell. J Neurosci 24, 9752–9759.Google Scholar