Abstract

BackgroundSensory systems often exhibit an adaptation or desensitization after a transient response, making the system ready to receive a new signal over a wide range of backgrounds. Because of the strong influence of thermal stochastic fluctuations on the biomolecules responsible for the adaptation, such as many membrane receptors and channels, their response is inherently noisy, and the adaptive property is achieved as a statistical average.Methodology/Principal FindingsHere, we study a simple kinetic model characterizing the essential aspects of these adaptive molecular systems and show theoretically that, while such an adaptive sensory system exhibits a perfect adaptation property on average, its temporal stochastic fluctuations are able to be sensitive to the environmental conditions. Among the adaptive sensory systems, an extensively studied model system is the bacterial receptor responsible for chemotaxis. The model exhibits a nonadaptive fluctuation sensitive to the environmental ligand concentration, while perfect adaptation is achieved on average. Furthermore, we found that such nonadaptive fluctuation makes the bacterial behavior dependent on the environmental chemoattractant concentrations, which enhances the chemotactic performance.Conclusions/SignificanceThis result indicates that adaptive sensory systems can make use of such stochastic fluctuation to carry environmental information, which is not possible by means of the average, while keeping responsive to the changing stimulus.

Highlights

  • Adaptation is a common mechanism for sensory and regulatory systems to be responsive to a changing stimulus over a wide range of background concentration [1]

  • A simple two state model of adaptive response To study the essential properties of fluctuation in an adaptive system and its underlying mechanism, we here study a simple two state model that responds and adapts to a change in the environmental conditions

  • Since ka and ki are dependent on the ligand concentration L, the relative noise intensity sA=A is dependent on the absolute ligand concentration L, indicating again that it is a nonadaptive property of adaptive sensory systems

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Summary

Introduction

Adaptation is a common mechanism for sensory and regulatory systems to be responsive to a changing stimulus over a wide range of background concentration [1]. When the sensory system is exposed to changes in background stimulus, the system responds by altering its activity, which is followed by adaptation back to its prestimulus level. This adaptive response is considered to reset the system to be ready for a new signal and prevents saturation of the response. Because of this adaptation property, the sensory system cannot carry any information about the background. When the rates of modification and its reverse reactions depend solely on its activity, the stationary activity level is independent of the environmental conditions and exhibits adaptation (Fig. 1). Because of the strong influence of thermal stochastic fluctuations on the biomolecules responsible for the adaptation, such as many membrane receptors and channels, their response is inherently noisy, and the adaptive property is achieved as a statistical average

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