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Coexpression of auxiliary Kvβ2 subunits with Kv1.1 channels is required for developmental acquisition of unique firing properties of zebrafish Mauthner cells.

Takaki Watanabe, Takashi Shimazaki, Aoba Mishiro, Takako Suzuki, Hiromi Hirata, Masashi Tanimoto, Yoichi Oda

J. Neurophysiol., 2013 Dec 11 , ,

Each neuron possesses a unique firing property, which is largely attributed to heterogeneity in the composition of voltage-gated ion channel complexes. The zebrafish Mauthner (M) cells, which are bilaterally paired giant reticulospinal neurons (RSNs) in the hindbrain and induce rapid escape behavior, generate only a single spike at the onset of depolarization. This single spiking is in contrast with the repetitive firing of the M-cell's morphologically homologous RSNs, MiD2cm and MiD3cm, which are also involved in escapes. However, how the unique firing property of the M-cells is established and the underlying molecular mechanisms remain unclear. In the present study, we first demonstrated that the single-spiking property of the M-cells was acquired at 4 days post-fertilization (dpf), accompanied with an increase in dendrotoxin-I (DTX)-sensitive low-threshold K(+) currents, prior to which the M-cell repetitively fires as its homologs. Second, in situ hybridization showed that among DTX-sensitive Kv1 channel α-subunits, zKv1.1a was unexpectedly expressed in the homologs and the bursting M-cells at 2 dpf. In contrast, zKvβ2b, an auxiliary β-subunit of Kv1 channels, was expressed only in the single-spiking M-cells. Third, zKv1.1a expressed in Xenopus oocytes functioned as low-threshold K(+) channels, and its currents were enhanced by coexpression of zKvβ2b subunits. Finally, knockdown of zKvβ2b expression in zebrafish larvae resulted in repetitive firing of the M-cells at 4 dpf. Taken together, these results suggest that associative expression of Kvβ2 subunits with Kv1.1 channels is crucial for developmental acquisition of the unique firing properties of the M-cells among homologous neurons.