We have studied the function of the major central olfactory pathway in fruit flies. Key elements of this pathway, the projection neurons (PNs), connect the antennal lobes with the lateral protocerebrum both directly and indirectly, the latter via the mushroom bodies (MBs). Transgenic expression of tetanus toxin in the majority of PNs and few MB neurons leads to defects in odor detection and male courtship. Considering behavioral data from flies lacking MBs, our results argue that the direct PN-to-lateral protocerebrum pathway is necessary and sufficient to process these experienceindependent behaviors. Moreover, the involvement of an olfactory pathway in male courtship suggests a role of volatile attractive female pheromones in Drosophila. Providing structure-function relationships is a central issue in behavioral neuroscience (1, 2). The development of the enhancer trap technique in Drosophila (3, 4) made it possible to manipulate subsets of identified neurons in a noninvasive manner. In particular, the P[GAL4]͞UAS system allows ectopic expression of any gene of interest (4). When expressing tetanus toxin light chain (TeTxLC) (5), synaptic transmission is locally blocked, and the behavioral consequences can be observed (6-9).We investigate the function of projection neurons (PNs), the major elements of the central olfactory pathway of Drosophila melanogaster ( Fig. 6) (10). Olfactory receptor neurons project to the antennal lobes (ALs), the first-order olfactory brain area. The information is then transmitted by PNs via the antennocerebral tract to two target areas, the mushroom bodies (MBs), involved in experience-dependent olfactory processing (2, 11), and the lateral protocerebrum (LPR) (12). Because subsets of MB extrinsic neurons project to the LPR (13, 14), the PNs provide the LPR with olfactory information both directly and, indirectly, via the MBs.Flies with an intact direct pathway, lacking the indirect one, are impaired in experience-dependent but not -independent olfactory behavior (15). We have generated a P[GAL4] line, GH146, which enables us to shut down about two-thirds of all PNs (Figs. 1 and 6) (16) through ectopic expression of TeTxLC. Both the direct and the indirect input into the LPR are thus blocked, which allows us to investigate possible effects on experience-independent olfactory processing. We show that odor detection and male courtship are severely impaired. We also test gustatory processing to address the question of effect specificity. Furthermore, neurons showing reporter gene expression in the visual system are identified as necessary for movement detection. Materials and MethodsDrosophila Strains. P[GAL4] line GH146 was described in ref. 16. UAS-reporter strains were UAS-lacZ (4), UAS-tau (17), UAStra (18), and the UAS-TeTxLC line TNT-E (called TNT for simplicity) (5). These lines and the wild-type strain Canton-S (CS) were used as controls in behavioral tests.Immunocytochemistry. -Galactosidase and antibody staining of whole mount preparations and sections was done according to...
GAL4-driven targeted expression of tetanus toxin light chain (UAS-TeTxLC) in a subset of chemosensory neurons of the larval antennomaxillary complex (AMC) and pharynx causes abnormal chemosensory behavior in Drosophila melanogaster. Consistent with strongest staining in the dorsal organ (DO), the presumed olfactory organ of the AMC, tetanus toxin-expressing larvae subjected to an olfactory preference assay show anosmic behavior to most volatile substances tested. Furthermore, we observed reduced responses to sodium chloride, fructose, and sucrose in gustatory plate assays. Surprisingly, the entire subset of labeled sensory neurons from the terminal (maxillary) organ (TO) of the AMC was found to project via the antennal nerve to the larval antennal lobe region. The maxillary nerve remained completely unstained. Hence, a subset of neurons from the TO builds an anatomical entity with projections from the DO. Our results suggest that the AMC contains both olfactory and gustatory sensilla, and that the DO is the main olfactory organ in larvae.
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