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Volume 16, Number 13, Issue of July 1, 1996 pp. 4089-4101
Copyright ©1996 Society for Neuroscience

The Role of K⁺ Currents in Frequency-Dependent Spike Broadening in Aplysia R20 Neurons: A Dynamic-Clamp Analysis

Received March 1, 1996; revised April 16, 1996; accepted April 18, 1996.

Minghong Ma^{1, 3, 4} and John Koester^{1, 2, 4}

¹ Center for Neurobiology and Behavior, ² Department of Psychiatry, and ³ Department of Physiology and Cellular Biophysics, College of Physicians and Surgeons, Columbia University, and ⁴ The New York State Psychiatric Institute, New York, New York 10032

The R20 neurons of Aplysia exhibit frequency-dependent spike broadening. Previously, we had used two-electrode voltage clamp to examine the mechanisms of this spike broadening (). We identified three K⁺ currents that mediate action-potential repolarization: a transient A-type K⁺ current (I_Adepol), a delayed rectifier current (I_K-V), and a Ca²⁺-sensitive K⁺ current (I_K-Ca). A major constraint in that study was the lack of completely selective blockers for I_Adepol and I_K-V, resulting in an inability to assess directly the effects of their activation and inactivation on spike broadening. In the present study, the dynamic-clamp technique, which employs computer simulation to inject biologically realistic currents into a cell under current-clamp conditions (,b), was used either to block I_Adepol or I_K-V or to modify their inactivation properties.

The data in this paper, together with earlier results, lead to the following hypothesis for the mechanism of spike broadening in the R20 cells. As the spike train progresses, the primary responsibility for spike repolarization gradually shifts from I_Adepol to I_K-V to I_K-Ca. This sequence can be explained on the basis of the relative rates of activation and inactivation of each current with respect to the constantly changing spike durations, the cumulative inactivation of I_Adepol and I_K-V, and the progressive potentiation of I_K-Ca. Positive feedback interactions between spike broadening and inactivation contribute to the cumulative inactivation of both I_Adepol and I_K-V. The data also illustrate that when two or more currents have similar driving forces and partially overlapping activation characteristics, selectively blocking one current under current-clamp conditions can lead to a significant underestimate of its normal physiological importance.

Key words: spike broadening; dynamic clamp; K⁺ current; I_Adepol; inactivation; Aplysia; R20

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