Two reciprocating current components underlying slow oscillations in Aplysia bursting neurons

  • Carnevale N
  • Wachtel H
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Abstract

The ionic mechanisms of the slow oscillatory potential in burst firing neurons in the abdominal ganglion of Aplysia californica (14L3-L6 and R15) were studied using voltage clamp methods, including a novel track and hold technique. The steady-state negative resistance characteristic (NRC) of these neurons is attributed to the activation of a moderately fast, persistent, inward current over a range of membrane potential below spike threshold. This inward current is quite sensitive to changes in external sodium concentration (Na)0and insensitive to potassium (K)0. By contrast, the portion of the I-V curve below the NRC range is insensitive to (Na)0, but highly sensitive to (K)0The results of 'track and store' voltage clamping show that there are actually two reciprocating currents whose combined action produces the slow oscillation. In addition to the inward current, there is a slow outward current which develops during the depolarized (burst) phase. The slow outward current can also be evoked, and more completely examined, with prolonged depolarizing voltage commands. The extremely slow decay of this current (τ ~ 45 sec) appears to be the factor underlying the slow, ramplike depolarization of Vm during the interburst interval. This slow outward current is insensitive to changes of (Na)0, but changes with (K)0in a manner consistent with the Nernst equation. We conclude that the burst-inducing slow oscillations are generated as follows: a moderately fast inward sodium dependent current (INa) produces a regenerative depolarization, and this in turn, produces a much slower outward potassium current (Is) which hyperpolarizes the cell. The cycle is completed when Ishas decayed sufficiently to allow Vm to depolarize enough to reactivate INa. We have used a quantitative version of this model to determine the time courses of gNaand gKthroughout the oscillation, and to explain why different portions of the oscillatory cycle display 'graded' or 'all-or-none' behavior.

Author-supplied keywords

  • Aplysia-invertebrate neurophysiology
  • bursting neurons
  • slow oscillations
  • voltage clamp

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Authors

  • Nicholas T. Carnevale

  • Howard Wachtel

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