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Localized Olfactory Representation in Mushroom Bodies of Drosophila Larvae

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Localized Olfactory Representation in Mushroom Bodies of Drosophila Larvae Localized olfactory representation in mushroom bodies of Drosophila larvae Liria M. Masuda-Nakagawaa,1, Nanae¨ Gendreb, Cahir J. O’Kanec, and Reinhard F. Stockerb aInstitute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-0032, Japan; bDepartment of Biology, University of Fribourg, Chemin du Muse´e 10, CH-1700 Fribourg, Switzerland; and cDepartment of Genetics, University of Cambridge, Downing Street, Cambridge CB2 3EH, United Kingdom Edited by Obaid Siddiqi, Tata Institute for Fundamental Research, Bangalore, India, and approved May 4, 2009 (received for review January 7, 2009) Odor discrimination in higher brain centers is essential for behav- of spatial stereotypy of odor representations in PNs in the calyx ioral responses to odors. One such center is the mushroom body has not yet been functionally defined, and the complexity of the (MB) of insects, which is required for odor discrimination learning. adult calyx makes it difficult to visualize the representation of The calyx of the MB receives olfactory input from projection odor qualities in single identified cells. neurons (PNs) that are targets of olfactory sensory neurons (OSNs) Drosophila larvae, which can perceive a wide variety of odors in the antennal lobe (AL). In the calyx, olfactory information is (14) and perform odor discrimination learning (15, 16), have an transformed from broadly-tuned representations in PNs to sparse olfactory system with the same basic architecture as adults but representations in MB neurons (Kenyon cells). However, the extent numerically much simpler. It contains only 21 unique OSNs (17), of stereotypy in olfactory representations in the calyx is unknown. each expressing a different OR (3, 4) with known ligand spec- Using the anatomically-simple larval olfactory system of Drosoph- ificity (18). Each AL glomerulus appears to be connected to the ila in which odor ligands for the entire set of 21 OSNs are known, MB calyx by a single PN (19). Whereas the adult calyx consists we asked how odor identity is represented in the MB calyx. We first of hundreds of microglomeruli that cannot be individually mapped the projections of all larval OSNs in the glomeruli of the identified, the larval calyx is organized in Ϸ34 glomeruli, in each AL, and then followed the connections of individual PNs from the of which a single identifiable PN contacts hundreds of KC AL to different calyx glomeruli. We thus established a comprehen- dendrites (20). Therefore, the larval olfactory system comprises sive olfactory map from OSNs to a higher olfactory association a small number of identifiable odor quality channels, each center, at a single-cell level. Stimulation of single OSNs evoked carried by a single neuron between successive layers of the strong neuronal activity in 1 to 3 calyx glomeruli, showing that olfactory pathway. broadening of the strongest PN responses is limited to a few calyx Here, we use the simple larval calyx to ask how individual odor glomeruli. Stereotypic representation of single OSN input in calyx qualities are represented in PN terminals and individual calyx glomeruli provides a mechanism for MB neurons to detect and glomeruli. We first generated a 3D map of OSN projections in discriminate olfactory cues. larval AL glomeruli. Using this map, we determined the con- nectivity of individual PNs between specific AL glomeruli and calyx ͉ genetically-encoded calcium indicator ͉ olfactory sensory neurons ͉ calyx glomeruli. Although the 1-to-1 connectivity between OSNs projection neurons and PNs in AL glomeruli predicts that activity in each OSN should stimulate a single calyx glomerulus, it is not easy to e now understand much about how odor information is predict how many calyx glomeruli are activated as a result of Wdetected and conveyed to the brain by sensory neurons, broadening of PN responses relative to OSNs. By carrying out but less about how this information is represented in higher brain the imaging of odor-evoked activity in single PN terminals in the centers to influence behavioral outputs. The mushroom body intact larval MB, we detect only limited dispersal of olfactory (MB) of insects, which in Drosophila is essential for odor signals during their transmission from single OSNs to the calyx. discrimination learning, provides a model to understand olfac- Results tory coding in higher association centers (1, 2). In the periphery, odor identity is detected by sets of olfactory sensory neurons 3D Map of the Larval AL Based on OSN Projections. To identify the (OSNs) whose specificities are determined by the olfactory main sensory pathways from OSNs into PNs in the larval AL, we receptor (OR) that they express (3, 4). OSNs that express the first generated a 3D map of AL glomeruli, defined by the same OR converge on defined glomeruli in the first olfactory innervation patterns of larval OSNs. We analyzed confocal center of the brain, the antennal lobe (AL), analogously to the sections of the AL projections of 22 OrX-GAL4 lines that are convergence of OSNs on olfactory bulb glomeruli in mammals. each expressed in a single OSN (3, 4). Terminals of single OSNs Projection neurons (PNs) then carry olfactory information from each ramified within a single AL glomerulus into branches and single AL glomeruli to the higher brain, the MB, and the lateral varicosities of variable number, density, size, and shape (Fig. horn. However, excitatory interneurons that innervate multiple 1A). The arrangement of OSN presynaptic terminals within AL glomeruli lead to broadening of PN specificity compared glomeruli was confirmed by visualizing terminals of all OSNs n-syb GFP B with OSNs (5, 6). PNs then connect to Kenyon cells (KCs) in the using :: (Fig. 1 ). In contrast, PN dendrites filled up most of the volume of AL glomeruli in which they arborized calyx of the MB, where the representation of odor qualities is (Fig. 1C). radically transformed; individual KCs respond much more se- lectively to odors than do either OSNs or PNs (7–9). The extent of stereotypy in olfactory processing in the calyx Author contributions: L.M.M.-N., C.J.O., and R.F.S. designed research; L.M.M.-N., N.G., and has been a matter of debate, in contrast to the clearly stereotypic R.F.S. performed research; C.J.O. contributed new reagents/analytic tools; L.M.M.-N., N.G., connections between OSNs and PNs in the AL. In Drosophila C.J.O., and R.F.S. analyzed data; and L.M.M.-N., C.J.O., and R.F.S. wrote the paper. adults, apparently stereotypic projections of PNs and KCs have The authors declare no conflict of interest. been defined anatomically only at the level of broad zones This article is a PNAS Direct Submission. (10–12), and odors can evoke localized PN activity in large 1To whom correspondence should be addressed. E-mail: [email protected]. regions of the calyx (13). However, at least some subsets of KCs This article contains supporting information online at www.pnas.org/cgi/content/full/ show apparently nonstereotypic responses to odors (9). The level 0900178106/DCSupplemental. 10314–10319 ͉ PNAS ͉ June 23, 2009 ͉ vol. 106 ͉ no. 25 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0900178106 Downloaded by guest on October 2, 2021 NEUROSCIENCE Fig. 1. 3D organization of the larval antennal lobe. All AL panels in this and subsequent figures show frontal confocal sections through the AL, with dorsal to the top, lateral to the left. (A) OSN terminals, labeled by expression of GFP under control of Or45b-GAL4, form varicosities within a single AL glomerulus (partly outlined by a broken line). (B) Expression of the synaptic vesicle marker n-syb::GFP in OSN presynaptic terminals using Or83b-GAL4, is found in varicosities within glomeruli (outlined by broken lines and labeled using anti-Dlg). (C) Arborization of GH146 PN dendrites in a posterior section of a larval AL, in which mCD8::GFP is expressed using GH146-GAL4. Two glomeruli subsequently identified as 67b and 74a (broken lines) are not labeled by GH146.(D) Confocal sections from successive anteroposterior (AP) levels (from left to right, increments of 4 ␮m) of a representative larval AL, stained by anti-Dlg. Although glomeruli are not always completely separated from each other, prominent glomeruli are distinct (broken lines). For a complete AP sequence and for panels free of annotations, see Fig. S4.(E) 3D model of the larval AL, viewed from different angles. A, P, M, and L denote anterior, posterior, medial, and lateral faces of the AL, respectively. Full rotations of the model are in Movie S2 and Movie S3. Colors of glomeruli denote predicted responses to broad classes of odorant (18): green, aromatic; red, broad-range aliphatic, principally esters and ketones; blue, esters; brown, alcohols; yellow, inhibitory responses; pale blue, no known responses. In general, glomerular position, shape and size were con- glomeruli. Labeled PN clones were generated by FLP-out (21) served between individuals (Fig. S1). The average center posi- in the GH146-GAL4 line (Fig. 2A), reported to label Ϸ16–18 tions of 21 glomeruli were mapped by calculating the relative larval PNs (22). GH146-expressing PNs arborized throughout positions of OSN terminals within a virtual grid constructed most AL glomeruli except for 67b and 74a (Fig. 1C), suggesting from the average dimensions of the larval AL (Figs. S1–S3 and that the arborizations of PNs in 19 glomeruli could be studied by Table S1). Most of the glomeruli could be identified by anti-Dlg this approach. Arborizations of 142 labeled PNs in the AL clearly neuropile labeling that showed them as discrete structures at matched the glomerular organization of OSN terminals, thus conserved locations, even though the borders were not always allowing the identification of 19 classes of PN according to their clearly defined (Fig.
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