A Dynamical Feedback Model for Adaptation in the Olfactory Transduction Pathway

Abstract

Olfactory transduction exhibits two distinct types of adaptation, which we denote multipulse and step adaptation. In terms of measured transduction current, multipulse adaptation appears as a decrease in the amplitude of the second of two consecutive responses when the olfactory neuron is stimulated with two brief pulses.Step adaptation occurs in response to a sustained steplike stimulation and is characterized by a return to a steady-state current amplitude close to the prestimulus value, after a transient peak. In this article, we formulate a dynamical model of the olfactory transduction pathway, which includes the kinetics of the CNG channels, the concentration of Ca ions flowing through them, and the Ca-complexes responsible for the regulation. Based on this model, a common dynamical explanation for the two types of adaptation is suggested. We show that both forms of adaptation can be well described using different time constants for the kinetics of Ca ions (faster) and the kinetics of the feedback mechanisms (slower). The model is validated on experimental data collected in voltage-clamp conditions using different techniques and animal species.

Common dynamical features of sensory adaptation in photoreceptors and olfactory sensory neurons

“…Refs. 33 and Supplementary Figure 8 of De Palo et al17). This implies that feedback regulation is crucial for adaptation in our olfactory neurons.…”

“…17 we have observed that the two forms of adaptation mentioned so far, step adaptation and multipulse adaptation, appear to be in a dynamical trade-off: the more step adaptation gets closer to perfect, the slower is the recovery in multipulse adaptation and viceversa. The limiting case of perfect step adaptation corresponds to no recovery at all in multipulse adaptation.…”

“…The ability of a biological system to adjust the sensitivity in a wide range of input amplitudes, has been extensively studied in the literature10111213, especially in recent years1415161718192021222324. The phenomenon occurs in different contexts, like chemotaxis in bacteria1424 and amoeba19, osmotic regulation in yeast25, tryptophan regulation in E.coli 26, and sensory systems171213.…”

“…The phenomenon occurs in different contexts, like chemotaxis in bacteria1424 and amoeba19, osmotic regulation in yeast25, tryptophan regulation in E.coli 26, and sensory systems171213. Most, if not all, of these studies evaluate adaptation through the steady state values reached in response to different constant stimuli.…”

The long tale of the calcium activated Cl−channels in olfactory transduction

“…-binding factors such as Ca 2C -calmodulin, reduces the sensitivity of the channels to cAMP, a mechanism relevant for adaptation. [47][48][49][50][51][52] cAMP activates cationic CNG channels in the ciliary membrane and knockout mice missing the CNG channel subunit CNGA2 lacked electro-olfactogram (EOG) responses (which represent the recorded summated generator potential from the surface of the OE) 53,54 to most odorants tested. 55 The absence of EOG responses indicated that CNGA2 KO mice are anosmic.…”