The connectome of the adult Drosophila mushroom body provides insights into function
- Janelia Research Campus, Howard Hughes Medical Institute, United States
- Department of Neuroscience, Columbia University, Zuckerman Institute, United States
- Drosophila Connectomics Group, Department of Zoology, University of Cambridge, United Kingdom
- Centre for Neural Circuits & Behaviour, University of Oxford, United Kingdom
- Neurobiology Division, MRC Laboratory of Molecular Biology, United Kingdom
Figures
Figure 1 with 2 supplements
The shared circuit architecture of the mushroom body and the cerebellum.
In both the insect MB and the vertebrate cerebellum sensory information is represented by sparse activity in parallel axonal fibers; Kenyon cells (KCs) in the MB and granule cells (GCs) in the …
Figure 1—video 1
Introduction to the MB.
Figure 1—video 2
Introduction to MB compartments.
Figure 2 with 1 supplement
Anatomy of the adult Drosophila MB.
Diagram of structure and information flow in the MB. (A) An image of the brain showing subregions of the MB (see panel B for more detail) and examples of the sensory pathways that provide …
Figure 2—figure supplement 1
The extent of the hemibrain volume and key to brain area nomenclature.
(A) The portion of the central brain (light blue) that was imaged and reconstructed to generate the hemibrain volume (Scheffer et al., 2020) is superimposed on a frontal view of a grayscale …
Figure 3 with 4 supplements
Kenyon cells.
Each panel shows a representative neuron of the indicated KC subtype together with the outline of the MB lobes and CA in gray , in a perspective view from an oblique angle to better display neuronal …
Figure 3—figure supplement 1
APL, DPM, SIFamide, OA-neurons and other modulatory neurons.
Neuronal morphologies are shown. (A) The anterior posterior lateral neuron, APL, innervates the entire MB (Figure 3—video 2). APL is GABAergic and provides negative feedback important for sparse …
Figure 3—video 1
KC types.
Figure 3—video 2
APL and DPM.
Figure 3—video 3
SIFamide and octopaminergic neurons.
Figure 4 with 5 supplements
Morphological hierarchical clustering reveals previously unrecognized KC subtypes.
(A) KC typing workflow, using KCγ as an example. All γ KCs in the population of annotated KCs were identified by excluding all KCs with axons in the vertical lobes. The space filling morphologies of …
Figure 4—figure supplement 1
Successive rounds of whole neuron morphological hierarchical clustering reveal novel KCγ subtypes.
(A) Morphological hierarchical clustering based on NBLAST scores for all-by-all comparison of KCγ cluster 3 (from Figure 4B) cut at height 1.3 (dashed line); six sub-clusters are produced …
Figure 4—figure supplement 2
Three distinct morphological subtypes of KCα′/β′.
(A) Morphological hierarchical clustering based on NBLAST scores for all-by-all comparison of α′/β′ KCs (simplified and pruned to include axon lobes only; black area in inset) is shown. When cut at …
Figure 4—figure supplement 3
Further explanation of KC subtype nomenclature.
(A) Three subtypes of α′/β′ KCs in the hemibrain EM dataset are shown in the coordinates of the JF2018 standard brain in frontal (left) and sagittal view (right). The red dashed line indicates the …
Figure 4—figure supplement 4
Four distinct morphological subtypes of KCα/β.
(A) Morphological hierarchical clustering based on NBLAST scores for all-by-all comparison of KCα/β carried out on that portion of their axons found in the lobes (black area in inset) is shown. When …
Figure 4—video 1
KC lineages.
Figure 5 with 2 supplements
Organizational features of KC projections.
(A) KCs were simplified to skeletons with one major branch point which were used as input for NBLAST all-by-all whole neuron clustering. (B) This clustering revealed the four clonal units that make …
Figure 5—figure supplement 1
Additional organizational features of KC projections.
Figure 5—figure supplement 2
KC-to-KC synapses.
The total number of synapses/1000 made between the indicated KC types in the MB (including the lobes, pedunculus, and calyces) are shown. Only connections totaling > 500 synapses are shown, except …
Figure 6 with 3 supplements
Dopaminergic neurons (DANs).
Each panel shows a DAN cell type, with its name, the compartment(s) it innervates and the number of cells of that type per brain hemisphere indicated; the outline of the MB lobes and CA are shown in …
Figure 6—figure supplement 1
Table of cell types found in each MB compartment.
This table shows which KCs, DANs, and MBONs are found in each of the 15 compartments of the MB lobes. Both the short names used throughout this paper and the longer names used in Aso et al., 2014a …
Figure 6—figure supplement 2
MBON neurotransmitter predictions.
(A) Neurotransmitters of typical MBONs previously determined by antibody staining (Aso et al., 2014a) are compared to computational predictions (Eckstein et al., 2020). In 17 of 18 cases they agree; …
Figure 6—figure supplement 3
Synapse number distribution for MBON outputs and DAN inputs.
The plots show the fraction of synapses that would fall above thresholds ranging from 1 to 20 synapses. The upper plot shows a line for each MBON, with typical MBONs in black and atypical MBONs is …
Figure 7
Mushroom Body Output Neurons (MBONs).
Each panel shows one of the previously described 20 types of MBONs, with its name, the compartment(s) it innervates and the number of cells of that type per brain hemisphere indicated (Aso et al., …
Figure 8 with 29 supplements
Atypical MBONs.
Each panel shows one of the 14 types of atypical MBONs, with its name, the compartment(s) it innervates and the number of cells of that type per brain hemisphere indicated. Figure 6—figure …
Figure 8—figure supplement 1
Atypical MBON10.
(A) Atypical MBON10 is the only atypical MBON cell type with more than one cell per brain hemisphere. One of the three MBON10s is shown here; all three cells are shown in Figure 8—video 1. …
Figure 8—figure supplement 2
Atypical MBON20.
(A) Atypical MBON20 (γ1γ2) is shown here and in Figure 8—video 2. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON20 receives 45% of its input from sites within …
Figure 8—figure supplement 3
Atypical MBON24.
(A) Atypical MBON24 (β2γ5) is shown here and in Figure 8—video 3. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON24 receives 75% of its inputs from sites within …
Figure 8—figure supplement 4
Atypical MBON25.
(A) Atypical MBON25 (γ1γ2) is shown here and in Figure 8—video 4. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON25 receives input in the γ1 and γ2 compartments. …
Figure 8—figure supplement 5
Atypical MBON26.
(A) Atypical MBON26 (β′2d) is shown here and in Figure 8—video 5. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON26 receives input from the β′2 compartment. (B) …
Figure 8—figure supplement 6
Atypical MBON27.
(A) Atypical MBON27 (γ5d) is shown here and in Figure 8—video 6. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON27 receives about half its input inside the MB, …
Figure 8—figure supplement 7
Atypical MBON28.
(A) Atypical MBON28 (α′3) is shown here and in Figure 8—video 7. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON28 receives about 60% of its input from the α′3 …
Figure 8—figure supplement 8
Atypical MBON29.
(A) Atypical MBON29 (γ4γ5) is shown here and in Figure 8—video 8. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON29 receives about 80% of its input from the γ4 …
Figure 8—figure supplement 9
Atypical MBON30.
(A) Atypical MBON30 (γ1γ2γ3) is shown here and in Figure 8—video 9. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON30 receives about 80% of its input within the …
Figure 8—figure supplement 10
Atypical MBON31.
(A) Atypical MBON31 (α′1a) is shown here and in Figure 8—video 10. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON31 gets about half of its inputs from the α′1 …
Figure 8—figure supplement 11
Atypical MBON32.
(A) Atypical MBON32 (γ2) is shown here and in Figure 8—video 11. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON32 gets about 50% of its synaptic input inside …
Figure 8—figure supplement 12
Atypical MBON33.
(A) Atypical MBON33 (γ2γ3) is shown here and in Figure 8—video 12. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON33 gets about one-third of its input synapses …
Figure 8—figure supplement 13
Atypical MBON34.
(A) Atypical MBON34 (γ2) is shown here and in Figure 8—video 13. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON34 has a small arbor and gets about one-third of …
Figure 8—figure supplement 14
Atypical MBON35.
(A) Atypical MBON35 (γ2) is shown here and in Figure 8—video 14. Presynaptic sites are shown in yellow and postsynaptic sites are shown in gray. MBON35 gets about 20% of its input from the γ2 …
Figure 8—figure supplement 15
Atypical MBON input distribution by brain region and similarity of inputs to different MBONs.
(A–B) Distribution of brain regions providing input to atypical MBON types. The value in each box indicates the effective input to the indicated MBON from the indicated brain region; that is, based …
Figure 8—video 1
Atypical MBON10.
Figure 8—video 2
Atypical MBON20.
Figure 8—video 3
Atypical MBON24.
Figure 8—video 4
Atypical MBON25.
Figure 8—video 5
Atypical MBON26.
Figure 8—video 6
Atypical MBON27.
Figure 8—video 7
Atypical MBON28.
Figure 8—video 8
Atypical MBON29.
Figure 8—video 9
Atypical MBON30.
Figure 8—video 10
Atypical MBON31.
Figure 8—video 11
Atypical MBON32.
Figure 8—video 12
Atypical MBON33.
Figure 8—video 13
Atypical MBON34.
Figure 8—video 14
Atypical MBON35.
Figure 9 with 4 supplements
Main calyx (CA).
The dendrites of 1757 KCs of the α/β, α′/β′, and γ cell types define the CA. (A) The pie chart shows a breakdown of the inputs to these KCs. The largest source of input is from 129 uniglomerular …
Figure 9—figure supplement 1
Distribution of the termini of olfactory PNs in the CA.
(A-A′′) MB images showing the orientation of the CA (blue) in panels B-E′′: (A) frontal view, (A′) top view, and (A′′) side view. (B-B′′) Four individual DL2d uniglomerular PNs (uPNs), each shown in …
Figure 9—figure supplement 2
Spatial arrangement in the CA of synaptic input from different PN groups.
The synaptic terminals of PNs in the CA are shown. PNs that convey distinct types of olfactory information are shown separately as indicated. (A-A′) MB images indicating the orientation of the …
Figure 9—figure supplement 3
Gustatory input to a subset of KCs.
The PN, VP5+Z adPN, has been reported to receive sensory input with mixed modalities, with hygrosensory input from the VP5 glomerulus in the AL and gustatory input from the SEZ (Marin et al., 2020). …
Figure 9—video 1
Introduction to γ main KCs.
Figure 10 with 6 supplements
Ventral accessory calyx (vACA).
The dendrites of the 99 γd and one γs1 KCs define the vACA. (A) The pie chart shows a breakdown of the inputs to these KCs; the number of cell (n=) and the number of the total synapses contributed …
Figure 10—figure supplement 1
Identification of VPNs.
The arbors of the ME VPNs generally extend into portions of the optic lobes that are not contained in the hemibrain volume. In order to determine the locations in the optic lobes where their …
Figure 10—figure supplement 2
LVINs ranked by amount of visual information conveyed.
(A) Plot of interneurons carrying visual information to the γd and γs1 KCs ranked by the strength of their effective contribution of visual information. For a given interneuron, this quantity is …
Figure 10—figure supplement 3
Further description of LVINs upstream of vACA KCs.
(A) A plot showing the similarity of the 15 LVINs most strongly connected to the vACA KCs, based on the cosine similarity of their inputs. The neuron IDs are color-coded to match the morphologies …
Figure 10—figure supplement 4
Additional views of the morphologies of VPN and LVIN inputs to the vACA.
(A–B) Additional views of the distribution of VPN and LVIN inputs onto γd and γs1 KCs (gray); synapses are color-coded as indicated. The insets show the orientation of the view shown. Note the …
Figure 10—figure supplement 5
Distribution of VPN inputs onto an LVIN.
(A) The LVIN PLP145 (883415238; green) that conveys the third highest amount of visual input to the vACA is shown along with the positions where it makes synaptic output (orange dots) onto a subset …
Figure 10—video 1
Introduction to γ dorsal KCs.
Figure 11 with 5 supplements
Dorsal accessory calyx (dACA).
The dendrites of the 60 α/βp KCs define the dACA. The pie chart shows a breakdown of the inputs to these KCs. The majority convey visual information, either directly from visual projection neurons …
Figure 11—figure supplement 1
VPN and LVIN inputs to the dACA.
(A) Plot of interneurons carrying visual information to the α/βp KCs ranked by the strength of their effective contribution of visual information. For a given interneuron, this quantity is computed …
Figure 11—figure supplement 2
LVINs that conveys visual input onto α/βp KCs.
(A) A plot showing the cosine similarity of inputs to each of the 19 LVINs that most strongly connected (more than 20 synapses) to α/βp KCs. (B) An additional view of the distribution of VPN and …
Figure 11—figure supplement 3
Detailed morphology of a dACA LVIN.
(A) One of the two SLP371 neurons (5813011738; green) is shown with the positions of its synaptic input from three color-coded classes of VPNs. (B) Synapses from this LVIN (green) onto the subset of …
Figure 11—figure supplement 4
Similarity of VPN inputs to individual LVINs that innervate the vACA or the dACA.
A heatmap showing the similarity of LVIN inputs from VPNs. It reveals the degree of diversity of the VPN inputs received by LVINs, as well as the existence of clusters of LVINs that receive similar …
Figure 11—figure supplement 5
Similarity of non-visual inputs to individual LVINs.
A heatmap in the same format as Figure 11—figure supplement 4 but showing the similarity of LVIN inputs from non-visual (i.e. non-VPN, non-LVIN) neurons. LVINs are shown in the same order as in Figur…
Figure 12 with 2 supplements
Lateral accessory calyx (lACA).
Figure 12—figure supplement 1
DN1a and DNa1-like (aMe23) neurons relay temperature cues from the lACA to the circadian clock.
(A) Morphology of a DNa1-like neuron (aMe23) with the positions where it receives thermosensory input in the lACA (green) and visual inputs (yellow) in the accessory medulla (AME) and the PLP. The …
Figure 12—figure supplement 2
KCγs2 and its inputs.
(A) Distribution of inputs to KCγs2. KCγs2 receives the vast majority of its sensory input in the lACA from thermo/hygrosensory PNs, but also receives a small amount of visual and olfactory …
Figure 13 with 2 supplements
Comparison of KC input connectivity to random models.
(A) Fraction of variance explained by components identified via principal components analysis of the olfactory uPN-to-KC input connectivity matrix—a binary matrix containing ones and zeros for …
Figure 13—figure supplement 1
Clustering KCs based on the similarity of their inputs from PNs.
Cosine similarity of PN inputs to KCs. This metric measures the degree of overlap in the PN inputs, weighted by synapse count, to each pair of KCs. Each PN is treated individually, rather than being …
Figure 13—figure supplement 2
Similarity of KC outputs to MBONs.
Cosine similarity of KC outputs to MBONs. KCs are grouped by subtype, and then indexed in the same order as in Figure 13—figure supplement 1.
Figure 14
Effect of spatial organization on the KC representation.
(A) Histogram of pairwise distances between boutons formed by PNs from the same glomerulus (top) or different glomeruli (bottom). (B) Average number of nearby boutons within a given radius of each …
Figure 15 with 3 supplements
Structure in PN-KC-MBON connectivity.
(A) Effective PN-to-MBON connectivity. MBONs within the α′/β′ lobe receive input primarily from uniglomerular olfactory PNs (uPNs), but they also show a gradation of input from thermo-hygrosensory …
Figure 15—figure supplement 1
PN connections to KC types and effective PN-to-MBON connectivity.
Detailed views of the PN inputs to KCs and MBONs. The uPN types are listed individually. Inputs from multiglomerular PNs (mPN), thermo/hygrosensory (thermo) and visual pathways have been pooled over …
Figure 15—figure supplement 2
PN-to-KC and KC-to-MBON connectivity by sensory modality.
(A) Olfactory input from uniglomerular PNs is carried by most of the KC types (α′/β′m, α′/β′ap2, α/βc, α/βm, α/βs, γm), but thermo/hygrosensory and visual inputs are conveyed by specific KC …
Figure 15—figure supplement 3
MBON connectivity by KC type.
Percentage of input to typical MBONs by KC type. Similar to Figure 15—figure supplement 2C, except that the KCs have been divided by lobes as well as by sensory modality. MBONs exhibit different …
Figure 16 with 4 supplements
MBON input and output similarity structure.
A comparison of MBON inputs and outputs through the lens of similarity structure. Left: cosine similarity of MBONs based on their effective PN inputs via KCs (computed as in Figure 15). Each cell of …
Figure 16—figure supplement 1
MBON output similarity by lobe.
Cosine similarity of MBONs based on the similarity of their outputs to all neurons (unnamed neuronal fragments have been excluded). Each cell of the heat map indicates the output similarity of the …
Figure 16—figure supplement 2
Correlation of MBON output and PN input similarity.
Scatter plot of MBON output similarity vs. similarity of their inputs from PNs, quantifying the relationship between the structure of MBON outputs and their sensory inputs. Each point represents a …
Figure 16—figure supplement 3
MBONs clustered by output similarity.
Cosine similarity between each MBON type and their target population. The ordering of MBONs was determined using average clustering. Unlike Figure 16 or Figure 16—figure supplement 1, the ordering …
Figure 16—figure supplement 4
MBON morphologies grouped by output similarity.
Radial dendrogram shows that MBONs with similar downstream connectivity innervate different compartments. A dendrogram based on the MBON cosine similarity matrix (Figure 16—figure supplement 3) was …
Figure 17 with 1 supplement
MBON output similarity by neurotransmitter.
Cosine similarity of MBON outputs to all named neurons. MBONs have been grouped by neurotransmitter and then presented in numerical order. There exist many instances of convergent outputs between …
Figure 17—figure supplement 1
MBON output similarity pooled by neurotransmitter.
Average cosine similarity of pairs of MBONs computed by collapsing the blocks in Figure 17 after separating typical and atypical MBONs. Note that the heat-map scale is different in the two plots.
Figure 18 with 3 supplements
MBON output distribution by neurotransmitter.
(A) Table indicating the percentage of output synapses of each MBON neurotransmitter type, including predicted neurotransmitters, that reside in the given brain area; typical and atypical MBONs were …
Figure 18—figure supplement 1
MBON output distribution by neurotransmitter presented on separated brain areas.
Visualization of the spatial position of MBON output synapses within individual brain areas.
Figure 18—figure supplement 2
Distribution of individual MBON outputs by brain area.
(Left) The value of each cell indicates the percentage of the given MBON’s output synapses that reside in the given brain area. Blank cells indicate values of less than 1%. (Right) The value of each …
Figure 18—figure supplement 3
Same plot as in Figure 18 but with only synapses from neurons whose neurotransmitters had been confirmed by antibody staining ( Aso et al., 2014a) shown color-coded.
Other synapses shown in gray.
Figure 19 with 1 supplement
Direct connections from MBONs to the central complex (CX).
In this diagram, the central column shows those MBONs that make direct connections of 10 or more synapses onto the dendrites of CX neurons. Such direct connections predominantly occur on fan-shaped …
Figure 19—figure supplement 1
The morphology and connectivity of nodulus and CREFB4 neurons.
(A) Morphologies of the LCNp (LCNOp), LCNpm (LCNOpm), and LNO1 (LNO2) nodulus neurons that are downstream of MBONs. The FB, NO, and LAL are shown in gray. Presynaptic sites are shown as yellow dots …
Figure 20 with 5 supplements
Summary of connections from MBONs to the FB.
Heat maps are shown that compare the strength of connection between MBONs and FB neurons in each FB layer. (A) Direct connections. The number of MBON cell types within each layer that make synapses …
Figure 20—figure supplement 1
Examples of MBON to FB connectivity involving an interneuron.
(A–C) Examples of connectivity patterns observed for connections of MBONs to the FB through an interneuron. At the top of each panel the morphologies of the interneuron (blue) and FB neurons …
Figure 20—video 1
MBONs providing direct input to the FB.
Figure 20—video 2
Multiple MBONs converge on an interneuron that provides input to the FB – example 1.
Figure 20—video 3
Multiple MBONs converge on an interneuron that provides input to the FB – example 2.
Figure 20—video 4
Multiple MBONs converge on an interneuron that provides input to the FB – example 3.
Figure 21 with 2 supplements
Downstream targets of MBONs often receive input from more than one MBON.
(A) About 1550 neurons are downstream (including axo-axonal connections) of one or more of the 34 MBON cell types when a threshold of 10 synapses is used. Among them, about 600 are downstream of at …
Figure 21—figure supplement 1
A LH neuron downstream of seven MBON types.
The previously reported LH output neuronal type (LHAD1b2; Dolan et al., 2019) acts as a site of integration of innate and learned information. (A) The morphology of a LHAD1b2_d neuron (544107243) is …
Figure 21—figure supplement 2
A neuron downstream of 11 MBON types.
This neuron LHPV4m1 (518899665) provides an extreme example of a neuron that integrates input from different MBON cell types. (A) The morphology of the neuron is shown in maroon, with its …
Figure 22 with 4 supplements
Spatial distribution of synapses from feedforward MBONs onto the dendrites of other MBONs.
(A) The three MBON types that make feedforward connections to other compartments within the MB lobes are shown. Neurons are shown in blue with presynaptic and postsynaptic sites shown as yellow and …
Figure 22—figure supplement 1
MBON06 and MBON11 make reciprocal axo-axonal connections in the α lobe.
(A) MBON06 (β1>α; green) and MBON11 (γ1pedc>α/β; blue) send axonal processes to the α2, α3 and, to a lesser extent, α1 compartments. (B) MBON06 and MBON11 make reciprocal axo-axonal connections, …
Figure 22—video 1
Feedforward MBON05.
Figure 22—video 2
Feedforward MBON06.
Figure 22—video 3
Feedforward MBON11.
Figure 23 with 3 supplements
Diagram of the connections made between MBONs.
A diagram showing MBON-to-MBON connections. At the bottom, gray boxes representing each of the MB compartments and the core of the distal pedunculus (pedc). DAN inputs, with PPL1 and PAM DANs …
Figure 23—figure supplement 1
Axo-axonal connections among typical MBONs outside the MB presented as a connection matrix.
This matrix shows all axo-axonal connections between pairs of typical MBONs that involve 20 or more synapses. The MBONs on the vertical axis are presynaptic to those of the horizontal axis. MBON …
Figure 23—figure supplement 2
Axo-axonal synapses between MBONs can be highly localized.
(A–F) Each panel shows three images: a low magnification view (upper left) of two neurons that make axo-axonal connections, a low magnification view (upper right) of just the postsynaptic neuron, …
Figure 23—figure supplement 3
Morphology of axo-axonal synapses.
(A) A portion of the MBON01 (γ5β'2a) arbor from within the enlarged area shown in Figure 23—figure supplement 2C is shown in transparent green. The relative locations of axo-axonal synapses from MBON…
Figure 24 with 1 supplement
Connections between MBONs form a multi-layered feedforward network.
Connections between MBONs, including both typical and atypical MBONs are shown, using a threshold of 30 synapses. The color of the arrow, as indicated in the color key, represents the nature and …
Figure 24—figure supplement 1
MBON30 displays an unusual pattern of innervation from other MBONs and FB neurons.
(A) MBON30 receives strong input from MBON05, a feedforward glutamatergic MBON, through three distinct axo-dendritic paths: inside the γ1 and γ2 compartments (260 synapses); inside the γ3 and γ4 …
Figure 25 with 2 supplements
A descending pathway from atypical MBONs to the ventral nerve cord (VNC).
Four LAL-innervating atypical MBONs form strong connections to descending neurons (DN). (A) A comparison between LM (Namiki et al., 2018) and EM morphologies of DNa02 and DNa03. Note that the LM …
Figure 25—figure supplement 1
Top inputs to DNa02 and DNa03.
(A) Left: Expanded connectivity diagram now including MBON30. MBON30 provides strong input to MBON26 and MBON27 (Figure 24) and conveys information from the FB (Figure 24—figure supplement 1B; Figure…
Figure 25—figure supplement 2
Central complex and LO inputs to DNa03.
(A) DNa03 receives strong visual input from lobula tangential (LT) neurons, LT51 (also see Figure 25—figure supplement 1C). The five LT51 neurons make 430 synapses onto DNa03, shown as reddish brown …
Figure 26 with 3 supplements
Feedback from MBONs to DANs.
Input from MBONs onto DANs occurs in three distinct circuit motifs which are diagrammed. MBON connections to DANs from the same compartment are depicted as a yellow arrow, while MBON connections to …
Figure 26—figure supplement 1
Axo-axonal connections from MBON05, MBON06 and MBON11 onto DANs inside MB lobes.
These three MBONs send axonal processes to other MB compartments (Aso et al., 2014a) where they make synapses onto other MBONs (see Figure 22 and Figure 22—figure supplement 1). As summarized here, …
Figure 26—figure supplement 2
MBON-to-DAN feedback mediated by an interneuron.
MBONs also make indirect connections to DANs in which the MBON connects to an interneuron which then connects to a DAN. This matrix shows the effective connection strength of such MBON-to-DAN …
Figure 26—figure supplement 3
Distribution of DAN feedback mediated by an interneuron.
This plot shows the ratio of feedback to the same compartment (self-feedback) to feedback to other compartments (other-feedback) for each MBON type. Circles are color-coded to indicate the MBON …
Figure 27 with 4 supplements
Similarity of input to individual DANs.
Heatmap representing the similarity of inputs received by DANs. Each square represents the cosine similarity of inputs received by each PAM or PPL1 DAN. In order to focus on inputs received outside …
Figure 27—figure supplement 1
Similarity of inputs to PPL1 DANs.
Figure 27—figure supplement 2
Similarity of inputs to DAN cell types.
Average input similarity between DAN cell types computed after pooling the data for all cells of a given type, as compared to Figure 27 where each individual DAN is plotted separately.
Figure 27—figure supplement 3
DAN input distribution by brain region.
(Left) The value in each box indicates the percentage of the given DAN type’s input synapses that lie in the given brain region. Blank boxes indicate values of less than 1%. (Right) Distribution of …
Figure 27—figure supplement 4
Comparing DAN inputs and MBON outputs reveals credit assignment by DANs.
Figure 28 with 1 supplement
Morphologically defined DAN subtypes receive similar input.
Tanglegrams show that DAN subtyping based on hierarchical morphological clustering matches that generated by hierarchical clustering by input connectivity (compare this figure to DAN input …
Figure 28—figure supplement 1
Anatomy of PAM01, PAM12, and PAM11 DAN subtypes.
Morphologies of DAN subtypes discussed in Figure 28. Innervated MB lobes are shown in gray and the relevant compartment in brown. (A) Six PAM01-uc DANs (blue) project across the upper commissure …
Figure 29 with 4 supplements
Relationship between DAN dendritic inputs and DAN axonal outputs to KCs.
These plots explore whether DANs of the same cell type that have distinct inputs also connect to distinct populations of KCs within a compartment. Analysis of eight compartments is shown. Within …
Figure 29—video 1
PAM11 (α1) dopaminergic neurons.
Figure 29—video 2
PAM09 (β1-ped) dopaminergic neurons.
Figure 29—video 3
PAM12 (γ3) dopaminergic neurons.
Figure 29—video 4
PAM07 (γ4<γ1γ2) dopaminergic neurons.
Figure 30 with 3 supplements
Different subtypes of the PAM01, PAM12, and PAM11 DANs synapse onto specific subpopulations of KCs and MBONs within their compartment.
KCs are subtyped as shown in Figure 4—figure supplements 1, 2 and 4. The axons from certain subtypes of DAN occupy different regions of, and together tile, a MB compartment. This permits for …
Figure 30—figure supplement 1
DAN subtypes within a compartment can be biased toward KC types representing different sensory modalities.
These plots reveal that in many cases, selective innervation of KC subclasses by particular DAN subtypes within a compartment is organized according to the sensory modality represented by those KCs. …
Figure 30—figure supplement 2
Within a compartment PAM DAN subtypes synapse onto specific KC subtypes as defined by the clustering shown in Figure 4—figure supplements 1, 2 and 4.
Figure 30—figure supplement 3
PAM DAN subtypes synapse selectively onto particular MBONs within a compartment.
Figure 31
Shared input neurons reveal expected and unexpected across-compartment groupings of DAN subtypes.
Matrix representing the connectivity to DAN subtypes provided by the top 50 strongest input neurons to each DAN subtype in the right hemisphere (n = 901 neurons, excluding MBONs and MB intrinsic …
Figure 32 with 1 supplement
Morphologically distinct subtypes of PAM12-DANs share inputs with either PPL1 or PAM DANs.
(A) The four PAM12-md DANs (maroon) innervate the γ3 compartment (brown) of the MB (gray ). (B) The PAM12-dd subtype (green) has additional dorsal dendritic branches (hollow arrowhead) not found in …
Figure 32—figure supplement 1
Strong inputs to PAM12-dd and PPL101 localize to different dendritic arbors.
More detailed representations of connectivity between input clusters 6, 2, 1, and 5 (Figure 31) and PPL101 and PAM12-dd DANs. Neuropils in which DAN input neurons receive most of their inputs are …
Figure 33 with 1 supplement
Examples of local neurons, SEZONs, and LHONs that target PAM11 DANs.
(A) All PAM11 DAN subtypes are shown, color-coded as in Figure 28 and Figure 28—figure supplement 1; the MB lobes are shown in gray and the α1 compartment is shaded brown. (B–F) Examples of neurons …
Figure 33—figure supplement 1
More information on the cell types shown in Figure 33.
Figure 34
Distinct FB neurons provide input to β lobe PAM or PPL105 DANs.
Two morphological clusters (31 and 10, Figure 31) of neurons from FB are among the strongest DAN inputs. These FB neurons have arbors of mixed polarity both in the SMP and in the FB, as can be seen …
Figure 35 with 1 supplement
Output neurons from different areas of the SEZ tile the SMP where they synapse onto select DAN subtypes.
(A) Axons from multiple SEZON cell types in clusters 22, 23, 24, 25, 26, 27, and 28 (see Figure 31) that provide strong inputs to DAN subtypes are shown together. (A′) The same SEZON axons shown …
Figure 35—figure supplement 1
Most strongly connected SEZON clusters exclusively synapse onto positive-valence PAM DANs.
(A–C) Further examples of clusters consisting of SEZONs that connect to specific DAN subtypes. In each panel the neuronal morphology is shown on the left with the brain regions where they contact …
Figure 36 with 2 supplements
A number of input neurons specifically target DAN groups of the PAM or PPL1 clusters.
Neurons providing strong input to PAM or PPL1 DANs are shown. Neuropil areas of inputs to these neurons are shown in gray in (A–C) and synapses to DANs are shown color-coded in (A′-C′); synapse …
Figure 36—figure supplement 1
Inputs specific to PAM DANs.
Neurons providing strong input to DANs of the PAM cluster are shown. Neuropil areas indicated (gray) and synapses to DANs are color-coded ; synapse numbers are given in parentheses. (A-A′) The seven …
Figure 36—figure supplement 2
Inputs specific to PPL1 DANs.
Neuropil areas indicated (gray) and synapses to DANs are color-coded ; synapse numbers are given in parentheses. (A-A′) The two neurons (light blue) of cluster 13 receive inputs in the contralateral …
Figure 37 with 1 supplement
Neurons that provide strong input to both PAM and PPL1 DANs.
Neuropil areas indicated in gray and synapses to DANs are color-coded ; synapse numbers are given in parentheses. (A-A′) The four neurons of cluster 35 receive inputs in the AVLP and provide strong …
Figure 37—figure supplement 1
Additional examples of neurons providing common input to both PAM and PPL1 DANs.
Neuropil areas where neurons of clusters 33 and cluster 9 receive input are shown in gray and their synapses onto DANs are color-coded ; synapse numbers are given in parentheses. (A-A′) The three …
Figure 38
Effects of segregated or mixed-modality signals.
(A) Schematic of two possible architectures for an MB-like circuit, in which KCs are either specialized for one sensory modality (left) or receive mixed input (right). Bottom layer circles represent …
Figure 39
Schematic of subcompartment DAN and MBON innervation within γ3.
The two PAM12 (γ3) DAN subtypes likely represent opposite valence based on their shared input with either aversively reinforcing PPL1-DANs or appetitively reinforcing PAM08 (γ4) DANs. Whereas …
Figure 40
MBON network representation of aversive memory.
Shock responsive DANs innervating γ1, γ2 and γ3 depress odor-specific KC synapses onto the respective MBONs. Depression of MBON11 (γ1pedc>α/β) and MBON09 (γ3β′1) releases their feedforward …
Figure 41
MBON network representation of appetitive memory.
Sugar-responsive DANs innervating γ4, γ5, β′2, and β1 depress odor-specific KC synapses onto the respective MBONs. Depression of the odor-specific response of MBON06 (β1>α) reduces odor-specific …
Figure 42 with 1 supplement
Multiple paths from atypical MBONs to DNs.
A simplified circuit diagram illustrating some of the prominent motifs used to connect atypical MBONs with the dendrites of DNs in the right hemisphere LAL. While several atypical MBONs synapse …
Figure 42—figure supplement 1
Morphologies of LAL051 and LAL171.
Presynaptic sites are shown as yellow dots and postsynaptic sites as gray dots. Because the left hemisphere LAL is incomplete in the hemibrain volume, the full morphology of LAL171 was constructed …
Additional files
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Supplementary file 1
Constituents of each of the 402 PAM subtype clusters.
- https://cdn.elifesciences.org/articles/62576/elife-62576-supp1-v2.xlsx
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Supplementary file 2
Constituents of each of the DAN input clusters shown in Figure 32.
- https://cdn.elifesciences.org/articles/62576/elife-62576-supp2-v2.xlsx
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Transparent reporting form
- https://cdn.elifesciences.org/articles/62576/elife-62576-transrepform-v2.docx
