Hygroreceptors in insect: testing models of stimulus action

Hygroreceptive sensilla are organelles designed specifically for the transduction of humidity in neural signals. They have been found on the antennae of insects and on the legs of a spider. The structures which conduct the stimulus from the sensillum surface to the membrane of the sensory cells do permit some functional inferences. Actually though, the mechanism of humidity perception is not yet understood. The question of whether the humidity sense must be included among the mechanical, the thermal or the chemical sense is still under debate. In the three models hygroreceptors are proposed to operate as 1) mechanical hygrometers in which the activity is initiated by swelling or shrinking of hygroscopic sensillum structures, 2) psychrometers in which the degree of cooling due to evaporation is used to measure humidity, and 3) chemical hygrometers in which humidity affects the electrolyte concentration just outside the dendrites of the sensory cells. While the mechanical and the psychrometric models are developed to explain the transduction mechanism of hygroreceptive sensilla in insects, the chemical model is at variance with insect hygroreceptors but fits into the organization and physiological responses of the spider hygroreceptors. This project will test with electrophysiological methods the accuracy of the mechanical and the psychrometer model in insect hygroreceptive sensilla. Direct mechanical stimulation of the sensillum by touching or bending is obstructed by the small size of the sensilla and their location protected and surrounded by elevated structures. The mechanical stimulus exerted by water vapour on the sensillum will by simulated by changing the atmospheric pressure. Hygroreceptors which act as mechanical hygrometer will respond to given changes in pressure irrespectively whether they are brought about by changing the atmospheric pressure at constant water vapor or by changing the water vapor at constant atmospheric pressure. The psychrometric function will be investigated by comparing the response of the hygro- and thermoreceptive sensory cells innervating a hygroreceptive sensillum to changes in humidity which produce different temperature depressions. In hygroreceptors which act as psychrometer, the difference in the discharge rates between these cells will vary with temperature depression and become a precise measure for humidity, both absolute and relative. Knowledge of the transduction mechanisms of hygroreceptive sensilla will determine our understanding of the behavioral responses of arthropods to ambient humidity. This proposal responds to a perceived need in the sensory transduction community and will establish a basis for future research in this area. The research on hygroreceptors seems to stand out as being more universal, more unusual and less developed, than others in the field of neurosciences.

In this project we have clarified the mechanisms underlying humidity transduction by means of elec- trophysiological studies of the moist cells and the dry cells associated with cuticular sensilla on the an- tenna of the cockroach. We have used air streams for stimulation and developed a device that allowed the application of slow and continuous humidity changes at different temperature levels.The model most favored for humidity transduction resembles a mechanical hygrometer. It envisions the humidity-dependent swelling and shrinking of hygroscopic sensillum structures as governing the responses of the moist and the dry cells. This model implies that water moves from the air into the sensillum and from the sensillum into the air depending on ambient humidity. In accordance with this model, the moist and dry cells respond antagonistically to changes in relative humidity. By contrast, their responses to same change in relative humidity increase with rising temperature. A hair hygrometer, however, indicates the relative humidity irrespectively of ambient temperature.An alternative model proposes that hygroreceptors act as evaporation detectors in which the concentration of electrolytes immediately surrounding the moist and dry cells are varying with ambient humidity. The drier the air, the greater the evaporation rate of water out of the sensillum and the greater the change in electrolyte concentration. A hygroscopic material would appear unnecessary. Rather, lymph is moving in one direction only, towards outside, depending on the saturation deficit of the air. Thus the moist and dry cells would respond to changes in saturation deficit depending on ambient tempera- ture. While the responses of the moist cell support functioning as evaporation detector, the dry-cells responses precludes it.The third model holds that hygroreceptors operate as psychrometers in which the degree of cooling due to evaporation of water from the sensillum surface is used to measure the humidity (or dryness) of the air. The drier the ambient air (absolutely) and the higher the temperature, the greater the evaporative temperature depression and the power to desiccate. To determine the temperature depression, two temperature measurements are needed; one may function as wet-bulb thermometer and one as a dry-bulb thermometer. Our study verifies the psychrometer function. The moist cell responds to the wet-bulb temperature due to the cooling effect of water evaporating from the sensillum surface and the dry cell to the dry-bulb temperature. Thus the hygroreceptor discharge is modulated by cooling and warming due to the change in evaporation which is governed by the saturation deficit of the atmosphere.