Coding of periodic pulse stimulation in chemoreceptors

Abstract

In natural conditions odorants released continuously by animals and plants are broken in discontinuous clumps and filaments. In the case of flying insects these discontinuities are perceived as periodic variations in the concentration of the stimulus. This periodicity has been shown to be essential to orientation and location of mate and food. We study analytically and numerically a model of the receplor-ligand interaction that takes place in the receptor neurons. We show that this model can account quantitatively for the range of optimum stimulus frequencies measured experimentally in the sex-pheromone system of moths. The results obtained suggest that the rate constants characterising the pheromone-receptor interaction are optimally adapted to the temporal characteristics of the signal it perceives.

Introduction

The question of understanding how the olfactory system encodes a periodic stimulus is biologically meaningful, especially in insects. For example a male moth can locate a conspecific female using the sexual pheromone she emits. It has been shown in natural conditions that air turbulence physically breaks the initially continuous pheromone plume into spatially and temporally discontinuous patches (Murlis et al., 1992, Murlis and Jones, 1981). For an insect flying and zigzagging in the plume the discontinuities appear as a periodic signal. The importance of this periodic stimulation has been experimentally studied and shown to be a necessary condition of odorant perception, because the moth cannot orient in an artificially made uniform cloud. Behavioural (Kennedy et al., 1980, Kennedy et al., 1981, Vickers and Baker, 1992, Willis and Baker, 1984) and neurophysiological (Christensen and Hildebrand, 1988, Marion-Poll and Tobin, 1992, Rumbo and Kaissling, 1989) experiments indicate that the optimum frequency is in the range 1–10 Hz. Our aim in the present paper is to investigate to what extent this optimum frequency can be explained by the characteristics of the peripheral sense organs.

In moths these sense organs, called sensilla, are borne by the featherlike antennae which are much larger in males than in females (Kaissling, 1987). Several types of sensilla exist, the largest one, which are up to half a millimetre long, are responsible for the detection of the pheromone molecules. Each olfactory sensillum is a cylinder of cuticle, riddled with tiny holes, housing two receptor neurons (Steinbrecht, 1999). The membrane of each neuron bears receptor proteins and ion channels that can generate the electrical receptor potential, which is converted in action potentials at the initial segment of the axon (Fig. 1). The odorant molecules reach the receptors through the holes and the perireceptor space lying between the cuticle and the membrane. Chemosensory transduction is a remarkable biochemical and electrical process in which the presence of a single molecule (ligand) at the cell surface can be detected and amplified into an action potential. This is a multistage process (Krieger et al., 1997) that involves the association of the ligand with a receptor protein on the cell membrane. The production of this signaling complex triggers the activation of G-proteins, which in turn activate enzyme units that release second messenger molecules in the cytoplasm. The second messengers open a number of ion channels, resulting in a change of the membrane potential followed by the firing of one or more action potentials. In the present work we are interested in the initial ligand-receptor interaction which can be considered as merely amplified by the subsequent events in the transduction cascade. We will show, by extending our recent research on this topic (Rospars et al., 2000, Lánský et al., 2001), that this dramatically simplified system can nonetheless account for the main feature of the real system.