Smelling, tasting, learning: Drosophila as a study case

Understanding brain function is to account for how the sensory system is integrated with the organism's needs to organize behaviour. We review what is known about these processes with regard to chemosensation and chemosensory learning in Drosophila. We stress that taste and olfaction are organized rather differently. Given that, e.g., sugars are nutrients and should be eaten (irrespective of the kind of sugar) and that toxic substances should be avoided (regardless of the kind of death they eventually cause), tastants are classified into relatively few behavioural matters of concern. In contrast, what needs to be done in response to odours is less evolutionarily determined. Thus, discrimination ability is warranted between different kinds of olfactory input, as any difference between odours may potentially be or become important. Therefore, the olfactory system has a higher dimensionality than gustation, and allows for more sensory-motor flexibility to attach acquired behavioural 'meaning' to odours. We argue that, by and large, larval and adult Drosophila are similar in these kinds of architecture, and that additionally there are a number of similarities to vertebrates, in particular regarding the cellular architecture of the olfactory pathway, the functional slant of the taste and smell systems towards classification versus discrimination, respectively, and the higher plasticity of the olfactory sensory-motor system. From our point of view, the greatest gap in understanding smell and taste systems to date is not on the sensory side, where indeed impressive advances have been achieved; also, a satisfying account of associative odour-taste memory trace formation seems within reach. Rather, we lack an understanding as to how sensory and motor formats of processing are centrally integrated, and how adaptive motor patterns actually are selected. Such an understanding, we believe, will allow the analysis to be extended to the motivating factors of behaviour, eventually leading to a comprehensive account of those systems which make Drosophila do what Drosophila's got to do.