Functional coupling between h-channels and Na⁺-K⁺ pumps in microdomain of mesencephalic trigeminal sensory neurons

Abstract

In the mesencephalic trigeminal sensory neurons (MTNs), both the Na⁺-K⁺ pump current (I-p) and the h-current (I-h) participate in generating the resting potential, while these two currents have been thought to be produced independently.
We show here functional coupling between Na⁺-K⁺ pumps and h-channels in the rat MTNs. Under whole-cell voltage-clamp condition, activation of I-h in response to hyperpolarizing command pulse leads to the generation of two types of ouabain-sensitive I-p with temporal profiles similar to those of instantaneous and slow components of I-h, reflecting Na⁺-transients in a restricted cellular space (microdomain). Moreover, the I-p activated by instantaneous I-h can facilitate the subsequent activation of slow I-h. Such counteractive and cooperative interactions were also disclosed by replacing extracellular Na⁺ with Li⁺. These observations indicate that the interactions are mediated by Na⁺ ions and reflected in Na⁺-transient in presumed microdomain. Consistent with these findings, h-channels and Na⁺-K⁺ pumps were colocalized in plasma membrane of MTNs covered by numerous spines. Therefore, the bidirectional interactions between Na⁺-K⁺ pumps and h-channels are likely to be mediated by a novel mechanism of Na⁺-microdomain, presumably created by the morphological specialization of spines in primary sensory neurons of MTN. The presence of Na⁺-microdomain was further investigated by measuring Na⁺ transient just beneath the plasma membrane and at the center of soma, using sodium-binding benzofuran isophthalate (SBFI). [Jpn J Physiol 54 Suppl:S134 (2004)]