The larval chemosensory system of Drosophila melanogaster: neuroanatomy and neurotransmitter distribution

We provide a detailed analysis of the larval head chemosensory system of Drosophila melanogaster, based on confocal microscopy of cell-specific reporter gene expression in P[GAL4] enhancer trap lines. In particular, we describe the neuronal composition of three external and three pharyngeal chemosensory organs, the nerve tracts chosen by their afferents, and their central target regions. With a total of 21 olfactory and 80 gustatory neurons, the sensory level is numerically much simpler than that of the adult. Moreover, its design is different than in the adult, showing an association between smell and taste sensilla. In contrast, the first order relay of the olfactory afferents, the larval antennal lobe (LAL), exhibits adult-like features both in terms of structure and cell number. It shows a division into approximately 30 subunits, reminiscent of glomeruli in the adult antennal lobe. Taken together, the design of the larval chemosensory system is a ‘hybrid’, with larval-specific features in the periphery and central characteristics in common with the adult. The largely reduced numbers of afferents and the similar architecture of the LAL and the adult antennal lobe, render the larval chemosensory system of Drosophila a valuable model system, both for studying smell and taste, and for examining the development of its adult organization. Abbreviations: AL antennal lobe, AN antennal nerve, DO dorsal organ, DOG ganglion of the DO, DPS dorsal pharyngeal sensilla, LAL larval antennal lobe, LBN, labial nerve, LI local interneuron, LN labral nerve, mAb monoclonal antibody, MN maxillary nerve, PN projection neuron, PPS posterior pharyngeal sensilla, SOG suboesophageal ganglion, TO terminal organ, TOG ganglion of the TO, TR tritocerebrum, VO ventral organ, VOG ganglion of the VO, VPS ventral pharyngeal sensilla