Watanabe, T., Shimazaki, T., Mishiro, A., Suzuki, T., Hirata, H., Tanimoto, M., and Oda, Y. (2014) Coexpression of auxiliary Kvbeta2 subunits with Kv1.1 channels is required for developmental acquisition of unique firing properties of zebrafish Mauthner cells. Journal of neurophysiology. 111(6):1153-64.
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 &beta-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.