Odor Coding in a Model Olfactory Organ: The Drosophila Maxillary Palp

Abstract

Odor coding relies on the activity of different classes of receptor neurons, each with distinct response characteristics. We have examined odor coding in a model olfactory organ, the maxillary palp of Drosophila. This organ contains only 120 olfactory receptor neurons, compartmentalized in sensory hairs called sensilla, and provides an opportunity to characterize all neurons in an entire olfactory organ. Extensive extracellular recordings from single sensilla reveal that the neurons fall into six functional classes. Each of the 60 sensilla houses two neurons, which observe a pairing rule: each sensillum combines neurons of two particular classes, thereby yielding three sensillum types. The sensillum types are intermingled on the surface of the palp, but their distribution is not random. The neurons exhibit diverse response characteristics, providing the basis for an olfactory code. A particular odor can excite one neuron and inhibit another, and a particular neuron can be excited by one odor and inhibited by another. Some excitatory responses continue beyond the end of odor delivery, but responses to most odors terminate abruptly after the end of odor delivery, with some followed by a period of poststimulus quiescence. The specificity of odor response is examined in detail for the neurons of one sensillum, which were found to differ in their relative responses to a homologous series of esters. Adaptation and cross-adaptation are documented, and cross-adaptation experiments demonstrate that the two neurons within one type of sensillum can function independently. The analysis of all neuronal types in this model olfactory organ is discussed in terms of its functional organization and the mechanisms by which it encodes olfactory information.