Activation of most primary sensory neurons results in transduction currents
that are carried by cations. One notable exception is the vertebrate olfactory
receptor neuron (ORN), where the transduction current is carried largely by the
anion Cl−. However, it remains unclear why ORNs use an anionic current for
signal amplification. We have sought to provide clarification on this topic by
studying the so far neglected dynamics of Na+, Ca2+, K+ and Cl−
in the small space of olfactory cilia during an odorant response. Using
computational modeling and simulations we compared the outcomes of signal
amplification based on either Cl− or Na+ currents. We found that
amplification produced by Na+ influx instead of a Cl− efflux is
problematic due to several reasons: First, the Na+ current amplitude varies
greatly depending on mucosal ion concentration changes. Second, a Na+
current leads to a large increase in the ciliary Na+ concentration during an
odorant response. This increase inhibits and even reverses Ca2+ clearance
by Na+/Ca2+/K+ exchange, which is essential for response termination.
Finally, a Na+ current increases the ciliary osmotic pressure, which could
cause swelling to damage the cilia. By contrast, a transduction pathway based
on Cl− efflux circumvents these problems and renders the odorant response
robust and reliable.Comment: 31 pages, 10 figures (including SI