From taste to touch: sensory signaling in model organisms

Abstract

The ability to perceive our environment has fascinated scientists and philosophers for thousands of years. According to some interpretations of Aristotle’s writings, the sense organs are able to perceive the environment by being transformed so that they are more like the object they are detecting. An eye can see a specific color by taking on that color; an animal can perceive warmth by becoming warm, and so forth. In recent years, our understanding of the inner workings of the Aristotelian senses of sight, smell, taste, touch, and hearing has gone through a revolution, and many of the key insights have emerged through analyses of model organisms. The reviews in this special issue of Pflugers Archiv highlight the progress achieved through work in genetically tractable metazoan animals ranging from worms to flies and mice. Although the various sensory modalities operate through a diversity of activation mechanisms and timescales, a recurring theme is that members of the transient receptor potential (TRP) superfamily of cation channels function broadly in sensory physiology and throughout animal phylogeny. The most ancient among the five classical senses are touch, taste, and smell. These three sensory modalities are present in the worm, Caenorhabditis elegans, and all metazoan organisms analyzed. In fact, the first mutations to affect touch were identified in the worm, and a review by Alexander Bounoutas and Martin Chalfie describes the current state of knowledge of the cells and proteins that function in the response to gentle touch. The fruitfly, Drosophila melanogaster, has also been invaluable for dissecting the genetics of gentle and noxious touch, and Maurice Kernan reviews the functions and development of the various types of sense organs in flies and the proteins essential for mechanotransduction. Among the players identified is no mechanoreceptor potential C (NOMPC), which is required for light touch and is the first TRP channel shown to function in mechanotransduction. The other of the primordial sensory modalities, taste and smell are important not only for identifying nutrient-rich sources but for avoiding noxious chemicals and predators. In many animals, the pheromone response contributes to mate selection, mating behavior, aggressiveness, and other behaviors. In worms, chemosensation impacts on a developmental program as the animals arrest at a nonreproductive, nonfeeding stage in environments with a paucity of food or food-derived odors. The perception of chemical cues in the environment can also impact lifespan, at least in invertebrates. Four reviews in the current special issue focus on the responses to volatile (olfactory) and nonvolatile (gustatory) chemical stimuli. These include a contribution by Piala Sengupta, outlining the cells, circuitry, and molecules involved in chemically induced behaviors in worms. Michelle Ebbs and Hubert Amrien provide an overview of the anatomical sites and receptors required for the taste and pheromone responses in Drosophila. In addition, they review fly taste transduction and the behaviors controlled by nonvolatile chemicals. As outlined in a separate review by Dean Smith, Drosophila has also provided important insights into the detection and processing of olfactory stimuli. While most pheromones are nonvolatile, at least one volatile chemical serves as a pheromone in flies, and this latter review describes the requirement for this pheromone for mating and for aggressive behavior. Pflugers Arch Eur J Physiol (2007) 454:689–690 DOI 10.1007/s00424-007-0265-8