Currents in the presynaptic terminal arbors of barnacle photoreceptors

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+]o 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 Ca(2+)-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 Ca(2+)-activated K+ conductance in this membrane. When the Ca(2+)-activated outward current was reduced to zero by increasing the [K+]o 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 Ca(2+)-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.