Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-23T04:24:59.208Z Has data issue: false hasContentIssue false

Currents in the presynaptic terminal arbors of barnacle photoreceptors

Published online by Cambridge University Press:  02 June 2009

Jon H. Hayashi
Affiliation:
Department of Physiology, University of North Carolina at Chapel Hill
Ann E. Stuart
Affiliation:
Department of Physiology, University of North Carolina at Chapel Hill

Abstract

We have described the currents flowing across the presynaptic membranes of the four median photoreceptors of the giant barnacle, Balanus nubilus, using a quasi-voltage clamp arrangement. Membrane potential, measured in the terminal region of one photoreceptor, was controlled in all four terminals by feedback current supplied through the nerve containing the photoreceptors’ axons. The [Ca2+] in the saline was reduced to decrease the Ca2+ current, enabling better voltage control, and tetraethylammonium ion (TEA, 20 mM) was added to block a fast voltage-dependent K+ conductance.

Depolarizing voltage steps from the resting potential in the dark (−60 mV) evoked slow, inward Ca2+-dependent currents which could be blocked by Co2+, Mg2+, or Cd2+. The Ca2+ currents were followed by large outward currents that persisted for many seconds after the offset of moderate or large pulses. These tail currents increased in magnitude and duration with pulse duration and reversed at about −80 mV, consistent with previous evidence for a Ca2+-activated K+ conductance in this membrane. When the Ca2+-activated outward current was reduced to zero by increasing the [K+] so as to set EK at −20 mV, and then stepping the voltage to this value, the step evoked a steady inward Ca2+ current. Thus, the Ca2+ current did not show voltage- or Ca2+-dependent inactivation. When Ba2+ was substituted for Ca2+, 500-ms depolarizing steps evoked steady inward currents but no outward currents. In any given experiment, the activation voltage of the Ca2+ or Ba2+ current did not depend on holding potential.

At the barnacle photoreceptor’s synapse, the postsynaptic cell adapts to maintained presynaptic voltage by a mechanism that is not understood. We conclude that neither Ca2+ current inactivation nor a shift in activation voltage with holding potential can account for this adaptation.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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., Charlton, M.P. & Smith, S.J. (1985 a). Calcium entry into voltage-clamped presynaptic terminals of squid. Journal of Physiology (London) 367, 143162CrossRefGoogle ScholarPubMed
Augustine, G.J., Charlton, M.P. & Smith, S.J. (1985 b). Calcium entry and transmitter release at voltage-clamped nerve terminals of squid. Journal of Physiology (London) 367, 163181CrossRefGoogle ScholarPubMed
Bader, C.R., Bertrand, D. & Schwartz, E.A. (1982). Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. Journal of Physiology (London) 331, 253284CrossRefGoogle ScholarPubMed
Barrett, J.N., Magleby, K.L. & Pallotta, B.S. (1982). Properties of single calcium-activated potassium channels in cultured rat muscle. Journal of Physiology (London) 331, 211230CrossRefGoogle ScholarPubMed
Callaway, J.C., Lasser-Ross, N., Stuart, A.E. & Ross, W.N. (1993). Dynamics of intracellular free calcium concentration in the presynaptic arbors of individual barnacle photoreceptors. Journal of Neuroscience (in press).CrossRefGoogle ScholarPubMed
Cole, K.S. & Moore, J.W. (1960). Ionic current measurements in the squid giant axon membrane. Journal of General Physiology 44, 123167CrossRefGoogle ScholarPubMed
Corey, D.P., Dubinsky, J.M. & Schwartz, E.A. (1984). The calcium current in inner segments of rods from the salamander (Ambystoma tigrunum) retina. Journal of Physiology (London) 354, 557575CrossRefGoogle ScholarPubMed
Edgington, D.R. & Stuart, A.E. (1979). Calcium channels in the high resistivity axonal membrane of photoreceptors of the giant barnacle. Journal of Physiology (London) 294, 433445CrossRefGoogle ScholarPubMed
Edgington, D.R. & Stuart, A.E. (1981). Properties of tetraethylam-moniumion-resistant K+ channels in the photoreceptor membrane of the giant barnacle. Journal of General Physiology 77, 629646CrossRefGoogle ScholarPubMed
Furukawa, T. (1986). Sound reception and synaptic transmission in goldfish hair cells. Japanese Journal of Physiology 36, 10591077Google ScholarPubMed
Furukawa, T. & Matsuura, S. (1978). Adaptive rundown of excitatory postsynaptic potentials at synapses between hair cells and eighth nerve fibers in the goldfish. Journal of Physiology (London) 276, 193209CrossRefGoogle Scholar
Gorman, A.L.F. & Thomas, M.V. (1980). Intracellular calcium accumulation during depolarization in a molluscan neurone. Journal of Physiology (London) 308, 259285CrossRefGoogle Scholar
Hayashi, J.H., Moore, J.W. & Stuart, A.E. (1985). Adaptation in the input-output relation of the synapse made by the barnacle’s photoreceptor. Journal of Physiology (London) 368, 179195CrossRefGoogle Scholar
Hudspeth, A.J., Poo, M.M. & Stuart, A.E. (1977). Passive signal propagation and membrane properties in median photoreceptors of the giant barnacle. Journal of Physiology (London) 272, 2543CrossRefGoogle ScholarPubMed
Hudspeth, A.J. & Stuart, A.E. (1977). Morphology and responses to light of the somata, axons, and terminal regions of individual photoreceptors of the giant barnacle. Journal of Physiology (London) 272, 123CrossRefGoogle ScholarPubMed
Kaneko, A. & Tachibana, M. (1985). A voltage-clamp analysis of membrane currents in solitary cells dissociated from Carassius auratus. Journal of Physiology 358, 131152CrossRefGoogle ScholarPubMed
Katz, B. & Miledi, R. (1967). A study of synaptic transmission in the absence of nerve impulses. Journal of Physiology 192, 407436CrossRefGoogle ScholarPubMed
Lasser-Ross, N., Callaway, J.C., Stuart, A.E. & Ross, W.N. (1991). Calcium dynamics in the presynaptic terminal of barnacle photoreceptors. In Calcium Entry and Action at the Presynaptic Nerve Terminal, ed. Stanley, E., Nowicky, M.C. & Triggle, D.J., pp. 475476. New York: Annals of the New York Academy of Science.Google Scholar
Laughlin, S.B., Howard, J. & Blakeslee, B. (1987). Synaptic limitations to contrast coding in the retina of the blowfly Calliphora. Proceedings of the Royal Society B (London) 231, 437467Google ScholarPubMed
Laughlin, S.B. & Osorio, D. (1989). Mechanisms for neural signal enhancement in the blowfly compound eye. Journal of Experimental Biology 144, 113146CrossRefGoogle Scholar
Lee, K.S. & Tsien, R.W. (1982). Reversal of current through calcium channels in dialyzed single heart cells. Nature 297, 498501CrossRefGoogle ScholarPubMed
Lewis, R.S. & Hudspeth, A.J. (1983). Voltage- and ion-dependent conductances in solitary vertebrate hair cells. Nature 304, 538541CrossRefGoogle ScholarPubMed
Lindgren, C.A. & Moore, J.W. (1989). Identification of ionic currents at presynaptic nerve endings in the lizard. Journal of Physiology 414, 201222CrossRefGoogle ScholarPubMed
Llinas, R., Steinberg, I.Z. & Walton, K. (1981). Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophysical Journal 33, 323352CrossRefGoogle ScholarPubMed
Macleish, P.R., Burrous, M.R. & Yagi, T. (1989). Voltage-activated calcium current in solitary primate cones. Investigative Ophthalmology and Visual Science (Suppl.) 30, 163.Google Scholar
Ohmori, H. (1984). Studies of ionic currents in the isolated vestibular hair cell of the chick. Journal of Physiology (London) 350, 561581CrossRefGoogle ScholarPubMed
Roberts, W.M., Jacobs, R.A. & Hudspeth, A.J. (1991). Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. Journal of Neuroscience 10, 36643684CrossRefGoogle Scholar
Ross, W.N. & Stuart, A.E. (1978). Voltage-sensitive calcium channels in the presynaptic terminals of a decrementally conducting photoreceptor. Journal of Physiology (London) 274, 173191CrossRefGoogle ScholarPubMed
Schnapp, B.J. & Stuart, A.E. (1983). Synaptic contacts between physiologically identified neurons in the visual system of the barnacle. Journal of Neuroscience 3, 11001115CrossRefGoogle ScholarPubMed
Smith, S.J. & Augustine, G.J. (1988). Calcium ions, active zones, and synaptic transmitter release. Trends in Neurosciences 11, 458464CrossRefGoogle ScholarPubMed
Smith, S.J., Augustine, G.J. & Charlton, M.P. (1985). Transmission at voltage-clamped giant synapse of the squid: Evidence for cooperativity of presynaptic calcium action. Proceedings of the National Academy of Sciences of the U.S.A. 82, 622625CrossRefGoogle ScholarPubMed
Stockbridge, N. & Ross, W.N. (1984). Localized Ca2+ and calcium-activated potassium conductances in terminals of a barnacle photoreceptor. Nature 309, 266268CrossRefGoogle ScholarPubMed
Stuart, A.E., Hayashi, J.H., Moore, J.W. & Davis, R.E. (1986). Currents in the synaptic terminals of barnacle photoreceptors. In Calcium, Neuronal Function and Transmitter Release, ed. Rahamimoff, R. & Katz, B., pp. 161202. Martinus Nijoff.Google Scholar
Taylor, R.E., Moore, J.W. & Cole, K.S. (1960). Analysis of certain errors in squid axon voltage clamp measurements. Biophysical Journal 1, 161202CrossRefGoogle ScholarPubMed
Tsien, R.W. (1983). Calcium channels in excitable cell membranes. Annual Review of Physiology 45, 341358CrossRefGoogle ScholarPubMed