Development of electrophysiological properties of fusiform neurons from the dorsal cochlear nucleus of mice before and after hearing onset

Abstract

The dorsal cochlear nucleus (DCN) in the auditory brainstem integrates auditory and somatosensory information. Mature DCN fusiform neurons fall into two qualitatively distinct types: quiet, with no spontaneous regular action potential firing, or active, with regular spontaneous action potential firing. However, how these firing states and other electrophysiological properties of fusiform neurons develop during early post-natal days to adulthood is not known. Thus, we recorded fusiform neurons from mice from P4 to P21 and analyzed their electrophysiological properties. In the pre-hearing phase (P4-P13), we found that most fusiform neurons are quiet, with active neurons emerging after hearing onset at P14. Subthreshold properties underwent significant changes before hearing onset, whereas changes to the action potential waveform occurred mainly after P14, with the depolarization and repolarization phases becoming markedly faster and half-width significantly decreased. The activity threshold in post-hearing neurons was more negative than in pre-hearing cells. Persistent sodium current (INaP) was increased after P14, coinciding with the emergence of spontaneous firing. Thus, we suggest that post-hearing expression of INaP leads to hyperpolarization of the activity threshold and the active state of the fusiform neuron. At the same time, other changes refine the passive membrane properties and increase the speed of action potential firing of fusiform neurons.

Calcium-sensitive subthreshold oscillations and electrical coupling in principal cells of mouse dorsal cochlear nucleus

“…The capacity to generate 1-2 Hz oscillations developed between P9 and P16, and this was paralleled by maturation of other features of fusiform cell firing. Some, such as rheobase and the AP threshold, rate of rise and width, are consistent with a developmental enhancement of Na + current (Benites et al, 2023), thus explaining the lack of oscillations at younger ages. It is notable that hearing in mice begins within this time frame (P12-13), suggesting that sensory activity may be a driving force for electrical maturation of fusiform cells.…”

“…External Ca 2+ had a large effect on oscillation power, likely explaining why previous studies in DCN that used > 2 mM Ca 2+ had not noted the presence of these rather striking and persistent oscillations (Gardner et al, 2001;Fujino and Oertel, 2003;Manis et al, 2003;Tzounopoulos et al, 2004). Similarly, recent studies (Olsen et al, 2018;Benites et al, 2023) using 2 mM external Ca 2+ also did not report oscillations. Indeed, lowering external divalent in vivo levels (specifically from 2 to 1 mM Mg 2+ and from 2 to 1.2 mM Ca 2+ ).…”