The Journal of Neurophysiology Vol. 77 No. 4 April 1997, pp. 1779-1794
Copyright ©1997 The American Physiological Society

Functional Role of Ca²⁺ Currents in Graded and Spike-Mediated Synaptic Transmission Between Leech Heart Interneurons

Jin Lu, John F. Dalton IV, Darrell R. Stokes, and Ronald L. Calabrese

Department of Biology, Emory University, Atlanta, Georgia 30322

Lu, Jin, John F. Dalton, IV, Darrell R. Stokes, and Ronald L. Calabrese. Functional role of Ca²⁺ currents in graded and spike-mediated synaptic trnasmission between leech heart interneurons. J. Neurophysiol. 77: 1779-1794, 1997. We used intracellular recording and single electrode voltage-clamp techniques to explore Ca²⁺ currents and their relation to graded and spike-mediated synaptic transmissions in leech heart interneurons. Low-threshold Ca²⁺ currents (activation begins below 50 mV) consist of a rapidly inactivating component (I_CaF) and a slowly inactivating component (I_CaS). The apparent inactivation kinetics of I_CaF appears to be influenced by Ca²⁺; both the substitution of Ca²⁺ (5 mM) with Ba²⁺ (5 mM) in the saline and the intracellular injection of the rapid Ca²⁺ chelator, bis-(o-aminophenoxy)-N,N,N,N-tetraacetic acid (BAPTA), from the recording microelectrode, significantly increase its apparent inactivation time constant. The use of saline with a high concentration of Ba²⁺ (37.5 mM) permitted exploration of divalent ion currents over a broader activation range, by acting as an effective charge carrier and significantly blocking outward currents. Ramp and pulse voltage-clamp protocols both reveal a rapidly activating and inactivating Ba²⁺ current (I_BaF) and a less rapidly activating and slowly inactivating Ba²⁺ current with a broad activation range (I_BaS). Low concentrations of Cd²⁺ (100-150 µM) selectively block I_BaS, without significantly diminishing I_BaF. The current that remains in Cd²⁺ lacks the characteristic delayed activation peak of I_BaS and inactivates with two distinct time constants. I_BaF appears to correspond to a combination of I_CaF and I_CaS, i.e., to low-threshold Ca²⁺ currents, that can be described as T-like. I_BaS appears to correspond to a Ca²⁺ current with a broad activation range, which can be described as L-like. Cd²⁺ (100 µM) selectively blocks spike-mediated synaptic transmission between heart interneurons without significantly interfering with low-threshold Ca²⁺ currents and plateau formation in or graded synaptic transmission between heart interneurons. Blockade of spike-mediated synaptic transmission between reciprocally inhibitory heart interneurons with Cd²⁺ (150 µM), in otherwise normal saline, prevents the expression of normal oscillations (during which activity in the two neurons consists of alternating bursts), so that the neurons fire tonically. We conclude that graded and spike-mediated synaptic transmission may be relatively independent processes in heart interneurons that are controlled predominantly by different Ca²⁺ currents. Moreover, spike-mediated synaptic inhibition appears to be required for normal oscillation in these neurons.

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