Contribution of potassium conductances to a time-dependent transition in electrical properties of a cockroach motoneuron soma

Robert Maurice Pitman, JD Mills

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11 Citations (Scopus)

Abstract

The cell body of the cockroach (Periplaneta americana) fast coral depressor motoneuron (D-f) displays a time-dependent change in excitability. Immediately after dissection, depolarization evokes plateau potentials, but after several hours all-or-none action potentials are evoked. Because K channel blockers have been shown to produce a similar transition in electrical properties, we have used current-clamp, voltage-clamp and action-potential-clamp recording to elucidate the contribution of different classes of K channel to the transition in electrical activity of the neuron. Apamin had no detectable effect on the neuron, but charybdotoxin (ChTX) caused a rapid transition from plateau potentials to spikes in the somatic response of D-f, to depolarization. In neurons that already produced spikes when depolarized, ChTX increased spike amplitude but did not increase their duration nor decrease the amplitude of their afterhyperpolarization. 4-Aminopyridine (4-AP) (which selectively blocks transient K currents) did not cause a transition from plateau potentials to spikes but did enhance oscillations superimposed on plateau potentials. When applied to neurons that already generated spikes when depolarized, 4-AP could augment spike amplitude, decrease the latency to the first spike, and prolong the afterhyperpolarization. Evidence suggests that the time-dependent transition in electrical properties of this motoneuron soma may result, at least in part, from a fall in calcium-dependent potassium current (I-K,I-Ca), consequent on a gradual reduction in Ca2+ ii. Voltage-clamp experiments demonstrated directly that outward K currents in this neuron do fall with a time course that could be significant in the transition of electrical properties. Voltage-clamp experiments also confirmed the ineffectiveness of apamin and showed that ChTX blocked most of I-K,I-Ca. Application of Cd2+ (0.5 mM), however, caused a small additional suppression in outward current. Calcium-insensitive outward currents could be divided into transient (4-AP-sensitive) and sustained components. The action-potential-clamp technique revealed that the ChTX-sensitive current undenwent sufficient activation during the depolarizing phase of plateau potentials to enable it to shunt inward conductances. Although the ChTX-sensitive conductance apparently makes little contribution to spike repolarization, the ChTX-resistant I-K,I-Ca does make a significant contribution to this phase of the action potential. The 4-AP-sensitive current began to develop during the rising phase of both action potentials and plateau potentials but had little effect on the electrical activity of the neuron, probably because of its relatively small amplitude.

Original languageEnglish
Pages (from-to)2253-2266
Number of pages14
JournalJournal of Neurophysiology
Volume81
Publication statusPublished - May 1999

Keywords

  • IDENTIFIED INSECT MOTONEURON
  • CA-2+-DEPENDENT K+ CHANNELS
  • ACTION-POTENTIAL CLAMP
  • LARVAL MUSCLE-FIBERS
  • VOLTAGE-CLAMP
  • PERIPLANETA-AMERICANA
  • PLATEAU POTENTIALS
  • CENTRAL NEURONS
  • IONIC CURRENTS
  • OUTWARD CURRENT

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