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The neuronal architecture of the mushroom body provides a logic for associative learning.

Aso Y, Hattori D, Yu Y, Johnston RM, Iyer NA, Ngo TT, Dionne H, Abbott LF, Axel R, Tanimoto H, Rubin GM - Elife (2014)

Bottom Line: Each of the 20 dopaminergic neuron (DAN) types projects axons to one, or at most two, of the MBON compartments.Convergence of DAN axons on compartmentalized Kenyon cell-MBON synapses creates a highly ordered unit that can support learning to impose valence on sensory representations.The elucidation of the complement of neurons of the MB provides a comprehensive anatomical substrate from which one can infer a functional logic of associative olfactory learning and memory.

View Article: PubMed Central - PubMed

Affiliation: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States.

ABSTRACT
We identified the neurons comprising the Drosophila mushroom body (MB), an associative center in invertebrate brains, and provide a comprehensive map describing their potential connections. Each of the 21 MB output neuron (MBON) types elaborates segregated dendritic arbors along the parallel axons of ∼2000 Kenyon cells, forming 15 compartments that collectively tile the MB lobes. MBON axons project to five discrete neuropils outside of the MB and three MBON types form a feedforward network in the lobes. Each of the 20 dopaminergic neuron (DAN) types projects axons to one, or at most two, of the MBON compartments. Convergence of DAN axons on compartmentalized Kenyon cell-MBON synapses creates a highly ordered unit that can support learning to impose valence on sensory representations. The elucidation of the complement of neurons of the MB provides a comprehensive anatomical substrate from which one can infer a functional logic of associative olfactory learning and memory.

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Lower density of presynaptic sites at the border between compartments.Comparison of the KC membrane and presynaptic labeling in the γ lobe. (A) Membrane-labeled γd and γmain KCs (MB131B, pJFRC225-5xUAS-IVS-myr::smGFP-FLAG in VK00005); a substack projection of the γ lobe is shown. (B) Presynaptic sites within the γ lobe (nc82; magenta); nc82 staining outside the γ lobe has been eliminated for clarity. Arrows indicate borders between compartments of the γ lobe where synaptic density is low. (C–E) Single confocal slice at the border between the γ5 and γ4 subdomains showing KCs (C), nc82 staining (D), and a merged image (E).DOI:http://dx.doi.org/10.7554/eLife.04577.033
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fig10s1: Lower density of presynaptic sites at the border between compartments.Comparison of the KC membrane and presynaptic labeling in the γ lobe. (A) Membrane-labeled γd and γmain KCs (MB131B, pJFRC225-5xUAS-IVS-myr::smGFP-FLAG in VK00005); a substack projection of the γ lobe is shown. (B) Presynaptic sites within the γ lobe (nc82; magenta); nc82 staining outside the γ lobe has been eliminated for clarity. Arrows indicate borders between compartments of the γ lobe where synaptic density is low. (C–E) Single confocal slice at the border between the γ5 and γ4 subdomains showing KCs (C), nc82 staining (D), and a merged image (E).DOI:http://dx.doi.org/10.7554/eLife.04577.033

Mentions: The 21 MBON types elaborate dendritic arbors in insular, segregated domains of the lobes that we call compartments. MBON dendritic arbors within each compartment exhibit little, if any, overlap with arbors in neighboring compartments (Figure 10). Computational alignment of the dendritic arbors of each of the MBON types within a single reference brain revealed that these compartments collectively tile the MB lobes with minimal overlap (Figure 10G,I,K). The alignment reveals gaps between arbors at four compartment borders; staining of the MB lobes for the presynaptic marker Bruchpilot (Figure 10—figure supplement 1) suggests that these gaps represent areas of reduced synaptic density. Two-color labeling experiments confirmed that the dendritic arbors of different MBONs are segregated in spatially stereotyped compartments (Figure 11A–C). We observed ensheathing glia at the borders between the MB lobes but not between the MBON compartments in each lobe (Figure 11J–L).10.7554/eLife.04577.032Figure 10.Compartmentalization of the MB lobes.


The neuronal architecture of the mushroom body provides a logic for associative learning.

Aso Y, Hattori D, Yu Y, Johnston RM, Iyer NA, Ngo TT, Dionne H, Abbott LF, Axel R, Tanimoto H, Rubin GM - Elife (2014)

Lower density of presynaptic sites at the border between compartments.Comparison of the KC membrane and presynaptic labeling in the γ lobe. (A) Membrane-labeled γd and γmain KCs (MB131B, pJFRC225-5xUAS-IVS-myr::smGFP-FLAG in VK00005); a substack projection of the γ lobe is shown. (B) Presynaptic sites within the γ lobe (nc82; magenta); nc82 staining outside the γ lobe has been eliminated for clarity. Arrows indicate borders between compartments of the γ lobe where synaptic density is low. (C–E) Single confocal slice at the border between the γ5 and γ4 subdomains showing KCs (C), nc82 staining (D), and a merged image (E).DOI:http://dx.doi.org/10.7554/eLife.04577.033
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Related In: Results  -  Collection

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fig10s1: Lower density of presynaptic sites at the border between compartments.Comparison of the KC membrane and presynaptic labeling in the γ lobe. (A) Membrane-labeled γd and γmain KCs (MB131B, pJFRC225-5xUAS-IVS-myr::smGFP-FLAG in VK00005); a substack projection of the γ lobe is shown. (B) Presynaptic sites within the γ lobe (nc82; magenta); nc82 staining outside the γ lobe has been eliminated for clarity. Arrows indicate borders between compartments of the γ lobe where synaptic density is low. (C–E) Single confocal slice at the border between the γ5 and γ4 subdomains showing KCs (C), nc82 staining (D), and a merged image (E).DOI:http://dx.doi.org/10.7554/eLife.04577.033
Mentions: The 21 MBON types elaborate dendritic arbors in insular, segregated domains of the lobes that we call compartments. MBON dendritic arbors within each compartment exhibit little, if any, overlap with arbors in neighboring compartments (Figure 10). Computational alignment of the dendritic arbors of each of the MBON types within a single reference brain revealed that these compartments collectively tile the MB lobes with minimal overlap (Figure 10G,I,K). The alignment reveals gaps between arbors at four compartment borders; staining of the MB lobes for the presynaptic marker Bruchpilot (Figure 10—figure supplement 1) suggests that these gaps represent areas of reduced synaptic density. Two-color labeling experiments confirmed that the dendritic arbors of different MBONs are segregated in spatially stereotyped compartments (Figure 11A–C). We observed ensheathing glia at the borders between the MB lobes but not between the MBON compartments in each lobe (Figure 11J–L).10.7554/eLife.04577.032Figure 10.Compartmentalization of the MB lobes.

Bottom Line: Each of the 20 dopaminergic neuron (DAN) types projects axons to one, or at most two, of the MBON compartments.Convergence of DAN axons on compartmentalized Kenyon cell-MBON synapses creates a highly ordered unit that can support learning to impose valence on sensory representations.The elucidation of the complement of neurons of the MB provides a comprehensive anatomical substrate from which one can infer a functional logic of associative olfactory learning and memory.

View Article: PubMed Central - PubMed

Affiliation: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States.

ABSTRACT
We identified the neurons comprising the Drosophila mushroom body (MB), an associative center in invertebrate brains, and provide a comprehensive map describing their potential connections. Each of the 21 MB output neuron (MBON) types elaborates segregated dendritic arbors along the parallel axons of ∼2000 Kenyon cells, forming 15 compartments that collectively tile the MB lobes. MBON axons project to five discrete neuropils outside of the MB and three MBON types form a feedforward network in the lobes. Each of the 20 dopaminergic neuron (DAN) types projects axons to one, or at most two, of the MBON compartments. Convergence of DAN axons on compartmentalized Kenyon cell-MBON synapses creates a highly ordered unit that can support learning to impose valence on sensory representations. The elucidation of the complement of neurons of the MB provides a comprehensive anatomical substrate from which one can infer a functional logic of associative olfactory learning and memory.

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