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Volume 17, Number 10, Issue of May 15, 1997 pp. 3412-3424
Copyright ©1997 Society for Neuroscience

Presynaptic Recordings from Drosophila: Correlatin of Macroscopic and Single-Channel K⁺ Currents

Received Dec. 6, 1996; revised Feb. 7, 1997; accepted Feb. 25, 1997.

Manuel Martínez-Padrón and Alberto Ferrús

Instituto Cajal (Consejo Superior de Investigaciones Científicas), 28002 Madrid, Spain

We have performed direct electrophysiological recordings from Drosophila peptidergic synaptic boutons in situ, taking advantage of a mutation, ecdysone, which causes an increase in size of these terminals. Using patch-clamp techniques, we have analyzed voltage-dependent potassium currents at the macroscopic and single-channel level. The synaptic membrane contained at least two distinct voltage-activated potassium currents with different kinetics and voltage sensitivity: an I_A-like current with fast activation and inactivation kinetics and voltage-dependent steady-state inactivation; a complex delayed current that includes a slowly inactivating component, resembling the I_K described in other preparations; and a noninactivating component. The I_A-like current in these peptidergic boutons is not encoded by the gene Shaker, because it is not affected by null mutations at this locus. Rather, synaptic I_A has properties similar to those of the Shal-encoded I_A. Single-channel recordings revealed the presence in synaptic membranes of three different potassium channel types (A₂, K_D, K_L), with biophysical properties that could account for the macroscopic currents and resemble those of the Shal, Shab, and Shaw channels described in heterologous expression systems and Drosophila neuronal somata. A₂ channels (6-9 pS) have brief open times, and like the macroscopic I_A they exhibited voltage-dependent steady-state inactivation and a rapidly inactivating ensemble average current profile. K_D channels (13-16 pS) had longer open times, activate and inactivate with much slower kinetics, and may account for the slowly inactivating component of the macroscopic current. K_L (44-54 pS) channels produced a noninactivating ensemble average and may contribute to the delayed macroscopic current observed.

Key words: Drosophila; presynaptic terminal; K⁺ channels; Shaker; Shal; Shab; neuropeptides

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