Immature olfactory sensory neurons are intrinsically excitable and show maturation-dependent changes in voltage-gated Na+ and K+ currents

Abstract

Olfactory sensory neurons (OSNs) detect odorants and send electrical signals to glomeruli in the olfactory bulb. Unlike most neurons, OSNs are continuously regenerated throughout life and immature neurons contribute to odorant-evoked responses in glomeruli. However, their intrinsic excitability properties are largely unknown. Here, we used acute slices of the olfactory epithelium from neonatal OMP-GFP mice to visually identify mature and immature OSNs and performed patch-clamp recordings to investigate their functional properties. Loose-patch recordings showed that immature OSNs display spontaneous firing at lower frequency than mature neurons. Whole-cell recordings showed that immature OSNs have more depolarized resting potentials, higher input resistance, fire only with phasic patterns, and generate slower action potentials with more depolarized thresholds. Instead, mature OSNs exhibited both phasic and tonic repetitive firing and faster spike kinetics. Voltage-clamp experiments showed that voltage-gated Na⁺ currents in immature OSNs were almost entirely TTX-sensitive, whereas mature OSNs had both TTX-sensitive and TTX-resistant components whose availability depends on membrane potential. Voltage-gated K⁺ currents also differed with maturation: immature OSNs lacked a transient component and had only a sustained K⁺ current, whereas mature OSNs displayed both a transient component and an increased sustained current. Analysis of single-cell transcriptomic data identified upregulation of some Na⁺ and K⁺ channel genes during OSN maturation, consistent with the functional changes. Together, these results provide insights into the intrinsic excitability of immature OSNs and show how intrinsic properties change as OSNs mature, providing a foundation for future studies on the role of immature OSNs in sensory processing.

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