The role of linear and voltage-dependent ionic currents in the generation of slow wave oscillations

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Abstract

Neuronal oscillatory activity is generated by a combination of ionic currents, including at least one inward regenerative current that brings the cell towards depolarized voltages and one outward current that repolarizes the cell. Such currents have traditionally been assumed to require voltage-dependence. Here we test the hypothesis that the voltage dependence of the regenerative inward current is not necessary for generating oscillations. Instead, a current INLthat is linear in the biological voltage range and has negative conductance is sufficient to produce regenerative activity. The current INLcan be considered a linear approximation to the negative-conductance region of the current–voltage relationship of a regenerative inward current. Using a simple conductance-based model, we show that INL, in conjunction with a voltage-gated, non-inactivating outward current, can generate oscillatory activity. We use phase-plane and bifurcation analyses to uncover a rich variety of behaviors as the conductance of INLis varied, and show that oscillations emerge as a result of destabilization of the resting state of the model neuron. The model shows the need for well-defined relationships between the inward and outward current conductances, as well as their reversal potentials, in order to produce stable oscillatory activity. Our analysis predicts that a hyperpolarization-activated inward current can play a role in stabilizing oscillatory activity by preventing swings to very negative voltages, which is consistent with what is recorded in biological neurons in general. We confirm this prediction of the model experimentally in neurons from the crab stomatogastric ganglion.

Original languageEnglish (US)
Pages (from-to)229-242
Number of pages14
JournalJournal of Computational Neuroscience
Volume37
Issue number2
DOIs
StatePublished - Oct 1 2014

All Science Journal Classification (ASJC) codes

  • Sensory Systems
  • Cognitive Neuroscience
  • Cellular and Molecular Neuroscience

Keywords

  • Inward current
  • Leak
  • Linear current
  • Oscillations
  • Pacemaker
  • Regenerative
  • Stability

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