The unique synaptic circuitry of specialized olfactory glomeruli in Drosophila melanogaster
- Max Planck Institute for Chemical Ecology, Department of Evolutionary Neuroethology, Germany
- Instituto de Investigaciones Biológicas Clemente Estable, Departamento de Biología del, Uruguay
- Neurobiology Division, MRC Laboratory of Molecular Biology, United Kingdom
- Institute of Applied Physics, Abbe Center of Photonics, Friedrich Schiller University Jena, Germany
Figures
Figure 1 with 1 supplement
A correlative approach to analyze the ultrastructure of identified olfactory glomeruli.
(A, B) Two-photon laser scans of the antennal lobe in Orco-Gal4; UAS-GCaMP6s flies where Orco-positive olfactory sensory neurons (OSNs) in the glomerular neuropil were labeled by GCaMP (green fluorescence). Glomeruli DA2 (A) and DL5 (B) are encircled. Schematics show their relative position in the antennal lobe. Once the glomerulus of interest was identified, its boundaries were delineated using fiducial marks (white triangles) via laser branding, which enabled their identification at the ultrastructural level. Representative images of the same glomeruli (DA2 in C and DL5 in D) obtained with focused ion beam-scanning electron microscopy (FIB-SEM), showing their ultrastructure. Asterisks indicate the main neurite of uniglomerular projection neurons entering the glomerulus. White triangle shows a two-photon laser mark (see also A and B). (E) FIB-SEM image of a polyadic synapse: the presynaptic site (red arrowhead) is composed of a T-bar shaped presynaptic density, surrounded by small vesicles, and is opposed to several postsynaptic profiles (cyan dots). Scheme of a tetrad synapse: a presynaptic site with its T-bar (red arrowhead) forms four output connections (arrows) with four postsynaptic input sites (cyan dots). (F) A skeleton-based reconstruction of an OSN axon terminal (green line) with presynaptic (red dots) and postsynaptic sites (cyan dots). The dark gray shading surrounding the OSN trace represents the volume-based reconstruction of the same neuron. Tracing and reconstruction were performed within the FIB-SEM dataset (light gray area).
Figure 1—video 1
Focused ion beam-scanning electron microscopy (FIB-SEM) dataset of a DA2 glomerulus featuring a uniglomerular projection neuron (uPN) reconstruction (see extra file).
The video shows a full FIB-SEM scan of a DA2 glomerulus at pixel resolution 4 × 4 × 20 nm, with the neuron trace of a single uPN (uPN#2) highlighted in yellow.
Figure 2 with 1 supplement
Neuron classification and neuronal composition of the DA2 and DL5 glomeruli.
(A) Representative examples of each neuron class in glomeruli DA2 and DL5. Shown are focused ion beam-scanning electron microscopy (FIB-SEM) images (left column), volumetric neuronal reconstructions (middle column), and skeleton-based neuron traces (right column) for olfactory sensory neurons (OSNs, green), uniglomerular projection neurons (uPNs, magenta), and multiglomerular neurons (MGNs, blue). Key ultrastructural features, including T-bars (black triangle), mitochondria (asterisks), and spinules (white triangle) are indicated on the FIB-SEM images. Volumetric reconstructions (middle column) depict the general morphology of each neuron class. On the skeleton traces, pre- and postsynaptic sites are marked with red and cyan dots, respectively (right column). (B) Average branching intensity (branching points per µm of neuronal fiber length) for each neuron class OSNs, uPNs, and MGNs in DA2 and DL5. Data represent mean + standard deviation (error bars). Data points represent single values. Means were compared using the Wilcoxon two-sample test. No significant differences in branching points/µm were observed for OSNs or MGNs between glomeruli (significance was not tested for uPNs due to the presence of a single uPN in DL5). (C) Schematic summary, for each glomerulus, showing its volume (in µm3), the number of neurons per class (excluding MGNs), the total fiber length of all neurons for each neuron class and the total number of individual synaptic contacts.
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Figure 2—source data 1
Branching point analysis of olfactory sensory neurons (OSNs), uniglomerular projection neurons (uPNs), and multiglomerular neurons (MGNs) in DA2 and DL5 (X_DA2_rAl and X_DL5_lAl).
- https://cdn.elifesciences.org/articles/88824/elife-88824-fig2-data1-v1.xlsx
Figure 2—figure supplement 1
Neuronal volume and polyadicity.
(A) Ratio between neuronal fiber volume and length in glomerulus DA2. Data represent mean + standard deviation (error bars) (olfactory sensory neurons [OSNs] n = 30; uniglomerular projection neurons [uPNs] n = 5; multiglomerular neurons [MGNs] n = 15). Frequency of T-bars associated with a number of postsynaptic contacts (polyadicity) in OSNs (B), uPNs (C), and MGNs (D) in DA2 (dark shade) and DL5 (light shade).
Figure 3 with 1 supplement
Innervation density and synaptic density in DA2 and DL5.
Quantification of average glomerular innervation density of olfactory sensory neurons (OSNs) (A), uniglomerular projection neurons (uPNs) (B), multiglomerular neurons (MGNs) (C), and all glomerular neurons combined (D) and synaptic density of input sites (inputs), output sites (outputs), T-bars, and average polyadicity. Innervation density: total length (µm) of each neuronal fiber normalized to one µm3 of glomerular (glom.) volume. Synaptic density: number of input sites, output sites, or T-bars for each neuronal fiber normalized to 1 µm3 of glomerular volume. Polyadicity: average number of single output sites per T-bar for each neuronal fiber. Data for DA2 is shown in dark colors and for DL5 in light colors. Number of neurons in DA2: OSNs (green) n = 44; uPNs (magenta) n = 7; MGNs (blue) n = 180; all neurons n = 231, in DL5: OSNs n = 46; uPN n = 1; MGNs n = 221; all neurons n = 268. Data are presented as mean with standard deviation (error bars). Data points represent single neuron values. Means were compared using either Student’s t-test (OSNs) or Wilcoxon two-sample test (MGNs and all neurons). uPNs were not compared to the single uPN of the DL5 glomerulus. Significance value: p > 0.05 (not significant, no star), p ≤ 0.05 (*), p ≤ 0.01 (**), p ≤ 0.001 (***). Values are provided at data availability; polyadicity values are listed in Table 1, row 14.
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Figure 3—source data 1
Measurements and analysis of neuronal features (olfactory sensory neurons [OSNs], uniglomerular projection neurons [uPNs], and multiglomerular neurons [MGNs]) in DA2 and DL5 (X_DA2_rAl and X_DL5_lAl), visualized in Figure 3.
- https://cdn.elifesciences.org/articles/88824/elife-88824-fig3-data1-v1.xlsx
Figure 3—figure supplement 1
Synaptic density along neuronal fibers in DA2 and DL5.
Counts of synaptic inputs, synaptic outputs, and T-bars normalized to 1 µm of neuronal length along olfactory sensory neuron (OSN) (A), uniglomerular projection neuron (uPN) (B), or multiglomerular neuron (MGN) (C) fibers and collectively sampled for all neurons (D) within the glomeruli DA2 (dark colors) and DL5 (light colors). DA2: OSNs (green) n = 44; uPNs (magenta) n = 7; MGNs (blue) n = 180; all neurons n = 231. DL5: OSNs n = 46; uPN n = 1; MGNs n = 221; all neurons n = 268. Data represent mean + standard deviation (error bars). Data points represent single values. Means are compared using either Student’s t-test (in OSNs) or Wilcoxon two-sample test (in MGNs and all neurons). The uPNs of the DA2 are not compared to the single uPN of the DL5. Significance value: p > 0.05 (not significant, no star), p ≤ 0.01 (**), p ≤ 0.001 (***). Values are listed in Table 1, rows 9–11.
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Figure 3—figure supplement 1—source data 1
Measurements and analysis of neuronal features (olfactory sensory neurons [OSNs], uniglomerular projection neurons [uPNs], and multiglomerular neurons [MGNs]) in DA2 and DL5 (X_DA2_rAl and X_DL5_lAl), visualized in Figure 3—figure supplement 1.
- https://cdn.elifesciences.org/articles/88824/elife-88824-fig3-figsupp1-data1-v1.xlsx
Figure 4 with 1 supplement
Lateralization of olfactory sensory neuron (OSN) terminals in the antennal lobes (ALs).
(A) Illustration of an ipsilateral (dark green) and a contralateral (light green) OSN with dendrites in the corresponding antennae and their axonal projections to the ipsilateral olfactory glomerulus in the AL (dashed rectangle). (B) Exemplary skeleton traces of an ipsilateral (dark green) and a contralateral (light green) OSN terminal inside glomerulus DA2. The ipsilateral OSN axons reach the glomerulus via the ipsilateral antennal nerve (arrow down) and leave the glomerulus toward the AL commissure (arrow up) while OSN axons originating at the contralateral antenna reach the glomerulus via the AL commissure. Red dots: presynaptic sites; blue dots: postsynaptic sites. (C) Boxplots showing the fraction of synaptic output to uniglomerular projection neurons (uPNs, in magenta), to OSNs (in green), or to multiglomerular neurons (MGNs) (in blue), for the ipsilateral OSNs (dark green boxplot) and contralateral OSNs (light green), respectively, in the DA2, DL5, and VA1v glomeruli. (D) Boxplots showing the fraction of synaptic input of the same ipsilateral and contralateral OSNs that they receive from OSNs and MGNs. Connection polarity is indicated by arrows in the schematic neuronal drawings on the left of each plot. Dots represent single values. Means were compared using Student’s t-test. Significance value: p > 0.05 (not significant, no star), p ≤ 0.01 (**), p ≤ 0.001 (***). Mean and median values are provided at data availability. The data for glomerulus VA1v was extracted from Horne et al., 2018.
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Figure 4—source data 1
Analysis of ipsi- and contralateral olfactory sensory neurons (OSNs) in DA2 (X-DA2_rAl).
- https://cdn.elifesciences.org/articles/88824/elife-88824-fig4-data1-v1.xlsx
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Figure 4—source data 2
Analysis of ipsi- and contralateral olfactory sensory neurons (OSNs) in DL5 (X-DL5_lAl).
- https://cdn.elifesciences.org/articles/88824/elife-88824-fig4-data2-v1.xlsx
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Figure 4—source data 3
Analysis of ipsi- and contralateral olfactory sensory neurons (OSNs) in VA1v extracted from Figure 5 in Horne et al., 2018.
- https://cdn.elifesciences.org/articles/88824/elife-88824-fig4-data3-v1.xlsx
Figure 4—figure supplement 1
Properties of ipsi- and contralateral olfactory sensory neurons (OSNs).
Boxplots depicting the total neuronal fiber length and synaptic density (measured as the number of inputs, outputs, T-bars per unit of neuronal fiber length) for ipsilateral (dark green) and contralateral OSN terminals (light green) for the DA2 (A) and the DL5 (B) glomerulus, respectively. Dots represent single values. Means were compared using Student’s t-test. Significance value: p ≤ 0.05 (*), p ≤ 0.01 (**), p ≤ 0.001 (***).
Figure 5
Strength of synaptic connections between neuron classes in the circuitry of DA2, DL5, and VA1v.
(A) Schematic representation of the principal connection motifs among the neuron classes olfactory sensory neurons (OSNs, green), uniglomerular projection neurons (uPNs, magenta), and multiglomerular neurons (MGNs, blue). Synaptic connections directed toward uPNs are defined as feedforward and those directed toward OSNs or from uPNs to MGNs are classified as feedback connections (indicated by arrows). Alluvial diagrams of the glomerular circuitry in DA2 (B), DL5 (C), and VA1v (D). Each diagram shows the relative synaptic strength calculated as the proportion of 1:1 single synaptic contact between each neuron class in relation to the total number of synaptic contacts in their respective glomerulus. The synaptic strength between each neuron class, given as a percentage, is indicated by the thickness of the lines. The proportions (as percentage) of output (left side) or input (right side) are illustrated by colored rectangles to the left or right of each alluvial diagram. The total number of synaptic contacts is indicated below the diagrams. Percentages of the relative synaptic strength and synaptic counts are listed in the Figure 5—source data 1. (E) Stacked bar charts depict output (E’) and input (E’’) fractions (given as percentages) of each neuron class: OSNs (green), uPNs (magenta), MGNs (blue), schematically illustrated next to the bar charts, respectively, to each of the other neuron classes for glomeruli DA2, DL5, and VA1v. Fractions are color-coded according to the neuron class of the respective connecting partner.
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Figure 5—source data 1
Synaptic connectivity and relative differences between DA2, DL5, and VA1v.
Synapse counts and synaptic strength of each connection type in the DA2, DL5, and VA1v glomerulus. Three pairwise comparisons are shown: DA2 vs. DL5 (top table), VA1v vs. DL5 (middle table), and VA1v vs. DA2 (bottom table). The relative synaptic strength (rel syn strength) of each connection type (listed on the left) and the relative differences (rel differences) (listed on the right) are color-coded.
- https://cdn.elifesciences.org/articles/88824/elife-88824-fig5-data1-v1.xlsx
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Figure 5—source data 2
Calculations of fractional out- and input based on synaptic counts in DA2 (X-DA2_rAl), DL5 (X-DL5_lAl), and VA1v extracted from Figure 5 in Horne et al., 2018.
- https://cdn.elifesciences.org/articles/88824/elife-88824-fig5-data2-v1.xlsx
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Figure 5—source data 3
Raw data, excel sheet.
- https://cdn.elifesciences.org/articles/88824/elife-88824-fig5-data3-v1.xlsx
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Figure 5—source data 4
Raw data, excel sheet.
- https://cdn.elifesciences.org/articles/88824/elife-88824-fig5-data4-v1.xlsx
Figure 6
Differences in connectivity strength in glomeruli DA2, DL5, and VA1v.
(A) Schematic representation of synaptic connection motifs (arrows) between olfactory sensory neurons (OSNs, green), uniglomerular projection neurons (uPNs, magenta), and multiglomerular neurons (MGNs, blue) in glomeruli DA2, DL5, and VA1v. The number of neurons of each class – or truncated neuronal fibers (indicated in brackets) – is shown within the corresponding circle. (B) Diagrams of connection motifs (left) that are consistently stronger or weaker in DA2 and VA1v compared to DL5. Relative differences (expressed as percentages) between DA2 and DL5, and between VA1v and DL5 are illustrated as upward (stronger) or downward (weaker) arrows, with arrow intensity indicating the magnitude of the difference (see legend at the bottom) from the perspective of the target glomerulus (as defined in the table header). All relative difference values are provided in Figure 5—source data 1.
Figure 7 with 1 supplement
Distribution of pre- and postsynaptic partners of autapses in the uniglomerular projection neuron (uPN) dendrite of the DL5.
(A) Distribution of autaptic presynaptic (red dots) and postsynaptic (cyan dots) sites mapped onto a dendrogram of the single uPN dendrite in glomerulus DL5. The basal root node (black dot) marks the entry site of the uPN dendrite into the glomerulus (i.e., the point closest to its soma). Clusters of autaptic input sites along specific branches are encircled. (B) Simplified dendrogram of the uPN illustrating distinct Strahler orders, with distal branches (orders 1–4) and at basal branches (orders 5–8); see legend on the right. (C) Distribution of autaptic presynaptic (left) and postsynaptic (right) input sites along the dendrite, shown as proportions at each corresponding Strahler order (color-coded). Note that autaptic postsynaptic sites are located almost exclusively at the most distal dendritic branches. (D) Dendrogram of the DL5-uPN showing the locations of presynaptic sites (triangles) and postsynaptic sites (circles) for selected autapses (color-matched pairs). Autapses with large geodesic distance between their components are labeled with numbers; those with short distances are encircled and labeled with letters. (E) Schemes of the dendrogram illustrating the location of the presynaptic (red dot) and postsynaptic (cyan dot) sites of individual autapses, the geodesic distance between them (measured along the dendrite in µm), and the number of branching points (orange dots) separating the pre- and postsynaptic components. (F) Histogram showing the number of autapses grouped by geodesic distance between their pre- and postsynaptic sites (as illustrated in E). (G) The number of autapses categorized by the number of branch points between their pre- and postsynapses along the uPN dendrite (as illustrated in E).
Figure 7—figure supplement 1
Distribution of synapses and autapses along the DL5 uniglomerular projection neuron (uPN) dendrite in DL5 (A).
3D reconstruction of the dendritic tree of the single uPN in glomerulus DL5, shown as a skeleton trace with artificial thickness scaled according to Strahler order. Autapses are indicated as cyan dots. The entry site of the uPN main dendrite into the glomerulus (the point closest to the soma) is defined as the basal root node. (B) Number of autaptic presynaptic (magenta) and postsynaptic (cyan) sites plotted against their geodesic distance from the basal root node (indicated by a black circle in A). (C) Proportional distribution of all pre- and postsynaptic sites (excluding autaptic connections) across Strahler orders in the DL5 uPN dendritic tree (see legend inset). Note the high proportion of postsynaptic sites located on the most distal dendritic branches.
Figure 8
Graphic summary illustrating general differences between narrowly and broadly tuned olfactory circuits.
Graphic summary of key circuit features that distinguish the two narrowly tuned olfactory glomeruli studied here (dark gray circle) from a broadly tuned on (light gray circle). Olfactory glomeruli are the first relay station where olfactory information is processed before being transmitted to higher brain centers, including the lateral horn (LH) and mushroom body calyces (MBc). The model is based on a comparative analysis of the narrowly tuned circuits of DA2 and VA1v and the broadly tuned circuit of DL5. Circuit components include uniglomerular projection neurons (uPNs, magenta), local interneurons (LNs, blue), and olfactory sensory neurons (OSNs, green) from both ipsilateral and contralateral brain hemispheres. In the narrowly tuned circuits, multiple uPNs are present, whereas in the broadly tuned circuit LNs are more numerous, as indicated by the number of circles. Connectivity strength between neuronal types is inferred from synaptic counts (1:1 presynaptic–postsynaptic sites) and is represented by the size of the connecting triangles. Differences in neuron number are indicated by the number of circles. In narrowly tuned circuits, OSNs exhibit stronger synaptic output (1) and form stronger reciprocal connections with sister OSNs (2) and uPNs (3). The lateralization of OSN connectivity is reduced compared to broadly tuned circuits, where ipsilateral output to uPNs and contralateral output to the LNs dominates (4). Feedback synapses from uPNs to LNs (5) and from LNs to OSNs (6) are weaker in narrowly tuned circuits. In contrast, the broadly tuned circuit DL5 exhibits weaker OSN output and stronger lateralization of OSN inputs. Additionally, autapses are observed in the single uPN of DL5, whereas reciprocal uPN connections are a feature of narrowly tuned circuits. The model attributes to LNs the features quantified for a larger group of neurons (multiglomerular neurons, MGNs), of which the great majority are LNs, as discussed in the main text.
Tables
Table 1
Glomerular innervation and synaptic composition.
Quantitative comparison of neuronal and synaptic parameters between glomeruli DA2 and DL5 for each neuron class – olfactory sensory neurons (OSNs, green), uniglomerular projection neurons (uPNs, magenta), and multiglomerular neurons (MGNs, blue) – as well as the combined totals. Row 1: Total length of all neurons per neuron class and the overall total length for all neurons for each glomerulus. Rows 2–4: Synapse counts: number of input sites (inputs), output sites (outputs), and T-bars. Row 5: Innervation density: calculated as total neuron length (µm; row 1)/glomerular volume (µm3); glomerular volumes: DA2 = 1500 µm3 and DL5 = 2600 µm3 (see Figure 1C). Rows 6–8: Synaptic density per unit glomerular volume (µm3): total number of all input sites (inputs), output sites (outputs), and T-bars for each neuron class and all neurons divided by glomerular volume. Rows 9–11: Average synaptic density along neuronal fibers (see also Figure 3—figure supplement 1): number of inputs, outputs, or T-bars per µm of neuron length. Rows 12 and 13: Average synaptic ratios: T-bars-to-inputs or outputs-to-inputs. Row 14: Polyadicity: the average number of postsynaptic sites at each T-bar in DA2 and DL5. The ratios in rows 12–14 were calculated based on synaptic counts normalized to neuron length (rows 9–11). The color shading highlights values with a relative difference greater than 20% between DA2 and DL5 (see relative differences, Supplementary file 1). Highlighted values greater in DA2 than DL5 are underlined.
| Row | Values | Unit | OSNs | uPNs | MGNs | All neurons | ||||
|---|---|---|---|---|---|---|---|---|---|---|
| DA2 | DL5 | DA2 | DL5 | DA2 | DL5 | DA2 | DL5 | |||
| 1 | Total neuronal length | µm | 2012 | 2727 | 4652 | 5015 | 10,705 | 14,411 | 17,370 | 22,153 |
| 2 | Total synaptic counts | inputs | 868 | 1083 | 3887 | 3955 | 7229 | 9018 | 11,984 | 14,056 |
| 3 | outputs | 6671 | 6828 | 1624 | 3108 | 5659 | 6749 | 13,954 | 16,685 | |
| 4 | T-bars | 1063 | 1213 | 322 | 602 | 1263 | 1572 | 2648 | 3387 | |
| 5 | Total innervation density (sum of length of all neuronal fibers/glomerular volume) | µm/µm3 | 1.26 | 1.05 | 2.91 | 1.93 | 6.69 | 5.54 | 10.86 | 8.52 |
| 6 | Total glomerular synaptic density (total synaptic counts/glomerular volume) | inputs/µm3 | 0.54 | 0.42 | 2.43 | 1.52 | 4.52 | 3.47 | 7.49 | 5.41 |
| 7 | outputs/µm3 | 4.17 | 2.63 | 1.02 | 1.20 | 3.54 | 2.60 | 8.72 | 6.42 | |
| 8 | T-bars/µm3 | 0.66 | 0.47 | 0.20 | 0.23 | 0.79 | 0.60 | 1.66 | 1.30 | |
| 9 | Neuronal synaptic density (synaptic counts/neuronal length) | inputs/µm | 0.42 | 0.39 | 0.83 | 0.79 | 0.62 | 0.59 | 0.59 | 0.56 |
| 10 | outputs/µm | 3.37 | 2.62 | 0.33 | 0.62 | 0.52 | 0.51 | 1.06 | 0.87 | |
| 11 | T-bars/µm | 0.53 | 0.46 | 0.07 | 0.12 | 0.12 | 0.12 | 0.19 | 0.18 | |
| 12 | Synaptic ratio | T-bars/inputs | 1.31 | 1.27 | 0.08 | 0.15 | 0.23 | 0.24 | 0.43 | 0.42 |
| 13 | outputs/inputs | 8.29 | 7.29 | 0.40 | 0.79 | 1.04 | 1.11 | 2.40 | 2.17 | |
| 14 | Polyadicity | outputs/T-bars | 6.35 | 5.70 | 4.95 | 5.16 | 3.23 | 2.64 | 3.85 | 3.17 |
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Table 1—source data 1
Measurements and analysis of neuronal features (olfactory sensory neurons [OSNs], uniglomerular projection neurons [uPNs], and multiglomerular neurons [MGNs]) in DA2 and DL5 (X_DA2_rAl and X_DL5_lAl), summarized in Table 1.
- https://cdn.elifesciences.org/articles/88824/elife-88824-table1-data1-v1.xlsx
Key resources table
| Reagent type (species) or resource | Designation | Source or reference | Identifiers | Additional information |
|---|---|---|---|---|
| Genetic reagent (D. melanogaster) | Orco-GAL4; UAS-GCaMP6s | Vosshall et al., 2000 | https://bdsc.indiana.edu/ | |
| Software, algorithm | R | RRID:SCR_001905 | https://www.r-project.org/ | |
| Software, algorithm | Fiji | Schindelin et al., 2012 | RRID:SCR_008606 | https://fiji.sc/ |
| Software, algorithm | blender | RRID:SCR_008606 | https://www.blender.org/ | |
| Software, algorithm | TrakEM2 | RRID:SCR_008954 | https://imagej.net/TrakEM2 | |
| Software, algorithm | CATMAID | RRID:SCR_006278 | http://www.catmaid.org | |
| Software, algorithm | neuroboom | https://pypi.org/project/neuroboom/ |
Additional files
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Supplementary file 1
Relative differences of innervation and synaptic composition between glomeruli DA2 and DL5.
The table lists the relative differences between DA2 and DL5 (see Methods for calculations). Values that are at least 20% greater in DA2 than in DL5 are highlighted in dark shades and values that are at least 20% less in DA2 than in DL5 are highlighted in light shades.
- https://cdn.elifesciences.org/articles/88824/elife-88824-supp1-v1.xlsx
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MDAR checklist
- https://cdn.elifesciences.org/articles/88824/elife-88824-mdarchecklist1-v1.pdf
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The unique synaptic circuitry of specialized olfactory glomeruli in Drosophila melanogaster
eLife 12:RP88824.
https://doi.org/10.7554/eLife.88824.3
