Resurgent Na⁺ currents promote ultrafast spiking in projection neurons that drive fine motor control

Abstract

The underlying mechanisms that promote precise spiking in upper motor neurons controlling fine motor skills are not well understood. Here we report that projection neurons in the adult zebra finch song nucleus RA display: 1) robust high-frequency firing, 2) ultra-short half-width spike waveforms, 3) superfast Na+ current inactivation kinetics and 4) large resurgent Na+ currents (INaR). These spiking properties closely resemble those of specialized pyramidal neurons in mammalian motor cortex and are well suited for precise temporal coding. They emerge during the critical period for vocal learning in males but not females, coinciding with a complete switch of modulatory Na+ channel subunit expression from Navβ3 to Navβ4. Dynamic clamping and dialysis of Navβ4’s C-terminal peptide into juvenile RA neurons provide evidence that this subunit, and its associated INaR, promote neuronal excitability. We propose that Navβ4 underpins INaR that facilitates precise, prolonged, and reliable high-frequency firing in upper motor neurons.

Extensive GJD2 Expression in the Song Motor Pathway Reveals the Extent of Electrical Synapses in the Songbird Brain

“…Thus, it is likely that the electrical synaptic phenotype of cells was acquired in primitive nidopallial and arcopallial networks before the specialization of song motor nuclei. Note that for many other genes, on the contrary, song nucleus-specific gene expression has been documented (http://www.zebrafinchatlas.org/ accessed on 21 August 2021; [36][37][38]). Our results, therefore, suggest that there has been no major evolutionary pressure to modify the cell-type expression pattern of the gene GJD2 in song control nuclei HVC and RA relative to the expression in the regions they evolved from.…”