Hyperpolarization-activated currents, I(H) and I(KIR), in rat dorsal motor nucleus of the vagus neurons in vitro

R. A. Travagli, R. A. Gillis

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Abstract

1. The patch-clamp technique applied to the in vitro thin brain slice preparation was used to record voltage and current traces from visually identified neurons of the rat dorsal motor nucleus of the vagus (DMV). 2. The majority of DMV neurons (102 of 159, i.e., 64%) showed a slowly developing hyperpolarization-activated current that had its threshold generally positive to resting potential and that exhibited a half-maximal activation at -90 mV and full saturation at -127 mV. The activation time constant was strongly voltage dependent, decreasing with hyperpolarization. 3. Ion substitution experiments identified the hyperpolarization-activated current as I(H). In fact, the current was potassium- and sodium-sensitive. Raising the extracellular potassium concentration from 3.75 to 20 mM increased the current peak amplitude in a voltage-dependent manner, whereas lowering extracellular sodium concentration from 146 to 26 mM decreased the current peak amplitude with a shift of the activation threshold toward more hyperpolarized potentials. The I(H) was significantly reduced during perfusion with either external cesium or rubidium but was insensitive to barium and tetraethylammonium (TEA). 4. A subset of DMV neurons (44 of 159, i.e., 28%) showed the presence of fast inward rectification but no I(H). The current was activated at potentials close to the potassium equilibrium potential and reached steady state within 10 ms from the onset of the hyperpolarizing step. 5. Ion substitution experiments identified this hyperpolarization-activated current as I(KIR). In fact, the current was potassium sensitive, its activation curve shifted toward less negative potentials with increasing potassium concentrations. I(KIR) was sodium insensitive, being unaffected by the lowering of the external sodium concentration. I(KIR) was significantly reduced during perfusion with cesium, barium, and TEA. 6. In the DMV neuronal subpopulation expressing I(H), the I(H) contribution to the total cell conductance was ~30% at -87 to -97 mV. Furthermore, the same subpopulation of neurons was hyperpolarized in a voltage-related manner on perfusion with 5 mM cesium: at -57 mV, cesium induced a hyperpolarization of 5.6 ± 1.3 (SE) mV, whereas at -72 mV the cesium-induced hyperpolarization was 26 ± 4.4 mV. 7. Perfusion with 5 mM cesium reduced the spontaneous firing rate of a subset of neurons exhibiting I(H) but cesium never decreased the firing rate of neurons exhibiting I(KIR). 8. When the relationship between amount of current injected into DMV neurons and the steady-state firing rate of DMV neurons was studied it was noted that DMV neurons exhibiting I(H) had a plateau in the firing rate (9 Hz) that was significantly higher than the one obtained from neurons that exhibited I(KIR) but did not exhibit I(H) (6 Hz). 9. It is concluded that rat DMV neurons can be distinguished on the basis of the presence of two hyperpolarization- activated currents. The I(H) current is tonically active at resting potentials and may contribute to the regulation of the spontaneous activity of these neurons.

Original languageEnglish (US)
Pages (from-to)1308-1317
Number of pages10
JournalJournal of neurophysiology
Volume71
Issue number4
DOIs
StatePublished - Jan 1 1994

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

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