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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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Examples of off-targeted non-neuronal expression.We screened split-GAL4 lines for expression in tissues outside the central nervous system by imaging the native fluorescence of GFP from the pJFRC2-10xUAS-IVS-mCD8::GFP reporter in VK00005 (Pfeiffer et al., 2010).Examples of lines that we excluded from our collection for use in behavioral assays because of expression in leg muscles (A), cells in the sensory bristles (arrow heads) on the leg (B), or a prothoracic muscle (C; MB062C) are shown. Such lines are not recommended for use in behavioral experiments but can be utilized for anatomical analyses; for example, MB062C is used in Figure 11D.DOI:http://dx.doi.org/10.7554/eLife.04577.012
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fig2s7: Examples of off-targeted non-neuronal expression.We screened split-GAL4 lines for expression in tissues outside the central nervous system by imaging the native fluorescence of GFP from the pJFRC2-10xUAS-IVS-mCD8::GFP reporter in VK00005 (Pfeiffer et al., 2010).Examples of lines that we excluded from our collection for use in behavioral assays because of expression in leg muscles (A), cells in the sensory bristles (arrow heads) on the leg (B), or a prothoracic muscle (C; MB062C) are shown. Such lines are not recommended for use in behavioral experiments but can be utilized for anatomical analyses; for example, MB062C is used in Figure 11D.DOI:http://dx.doi.org/10.7554/eLife.04577.012

Mentions: An example of the use of the split-GAL4 approach to generate a driver line specific for MBON-α′2 (see Table 1 for the naming convention of MBONs and DANs). R20G03-GAL4 in attP2 (left) and R19F09-GAL4 in attP2 (center) both show expression in MBON-α′2 when crossed to pJFRC2-10XUAS-IVS-mCD8::GFP in attP2 and in many other neurons that differ between the two GAL4 lines. The optic lobes (OL), central brain (CB), and ventral nerve cord (VNC) are indicated. The enhancer fragments from these lines were used to generate the fly line MB018B carrying both R20G03-p65ADZp in attP40 and R19F09-ZpGAL4DBD in attP2 (right). The p65ADZp and ZpGAL4DBD proteins are themselves inactive; the reconstitution of an active GAL4 transcription factor requires heterodimerization that occurs only in cells expressing both proteins (Luan et al., 2006; Pfeiffer et al., 2010). This approach, therefore, labels cells in which both enhancers are active. The arrow indicates the cell body of one MBON-α′2 cell visualized using pJFRC225-5xUAS-IVS-myr::smGFP-FLAG reporter in VK00005 (white). Neuropils were visualized with nc82 antibody (orange). Genotypes of 92 split-GAL4 lines and the cell types they label are listed in Supplementary file 1 and raw confocal images are available online (http://www.janelia.org/split-gal4). The expression pattern observed using a split-GAL4 line depends to some extent on the UAS reporter construct used, as illustrated in Figure 2—figure supplement 1. Expression patterns of split-GAL4 lines for KCs (Figure 2—figure supplement 2), PPL1-cluster DANs (Figure 2—figure supplement 3), PAM cluster DANs (Figure 2—figure supplement 4), and MBONs (Figure 2—figure supplement 5) are shown. We also generated split-GAL4 lines for a variety of other modulatory cell types that project to the MB including serotonergic, GABAergic, octopaminergic, and peptidergic neurons (Figure 2—figure supplement 6). We chose lines with minimal off-target expression in neuronal and non-neuronal cells (Figure 2—figure supplement 7) to facilitate the use of these lines in future functional analyses to manipulate the activity of individual cell types.


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)

Examples of off-targeted non-neuronal expression.We screened split-GAL4 lines for expression in tissues outside the central nervous system by imaging the native fluorescence of GFP from the pJFRC2-10xUAS-IVS-mCD8::GFP reporter in VK00005 (Pfeiffer et al., 2010).Examples of lines that we excluded from our collection for use in behavioral assays because of expression in leg muscles (A), cells in the sensory bristles (arrow heads) on the leg (B), or a prothoracic muscle (C; MB062C) are shown. Such lines are not recommended for use in behavioral experiments but can be utilized for anatomical analyses; for example, MB062C is used in Figure 11D.DOI:http://dx.doi.org/10.7554/eLife.04577.012
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4273437&req=5

fig2s7: Examples of off-targeted non-neuronal expression.We screened split-GAL4 lines for expression in tissues outside the central nervous system by imaging the native fluorescence of GFP from the pJFRC2-10xUAS-IVS-mCD8::GFP reporter in VK00005 (Pfeiffer et al., 2010).Examples of lines that we excluded from our collection for use in behavioral assays because of expression in leg muscles (A), cells in the sensory bristles (arrow heads) on the leg (B), or a prothoracic muscle (C; MB062C) are shown. Such lines are not recommended for use in behavioral experiments but can be utilized for anatomical analyses; for example, MB062C is used in Figure 11D.DOI:http://dx.doi.org/10.7554/eLife.04577.012
Mentions: An example of the use of the split-GAL4 approach to generate a driver line specific for MBON-α′2 (see Table 1 for the naming convention of MBONs and DANs). R20G03-GAL4 in attP2 (left) and R19F09-GAL4 in attP2 (center) both show expression in MBON-α′2 when crossed to pJFRC2-10XUAS-IVS-mCD8::GFP in attP2 and in many other neurons that differ between the two GAL4 lines. The optic lobes (OL), central brain (CB), and ventral nerve cord (VNC) are indicated. The enhancer fragments from these lines were used to generate the fly line MB018B carrying both R20G03-p65ADZp in attP40 and R19F09-ZpGAL4DBD in attP2 (right). The p65ADZp and ZpGAL4DBD proteins are themselves inactive; the reconstitution of an active GAL4 transcription factor requires heterodimerization that occurs only in cells expressing both proteins (Luan et al., 2006; Pfeiffer et al., 2010). This approach, therefore, labels cells in which both enhancers are active. The arrow indicates the cell body of one MBON-α′2 cell visualized using pJFRC225-5xUAS-IVS-myr::smGFP-FLAG reporter in VK00005 (white). Neuropils were visualized with nc82 antibody (orange). Genotypes of 92 split-GAL4 lines and the cell types they label are listed in Supplementary file 1 and raw confocal images are available online (http://www.janelia.org/split-gal4). The expression pattern observed using a split-GAL4 line depends to some extent on the UAS reporter construct used, as illustrated in Figure 2—figure supplement 1. Expression patterns of split-GAL4 lines for KCs (Figure 2—figure supplement 2), PPL1-cluster DANs (Figure 2—figure supplement 3), PAM cluster DANs (Figure 2—figure supplement 4), and MBONs (Figure 2—figure supplement 5) are shown. We also generated split-GAL4 lines for a variety of other modulatory cell types that project to the MB including serotonergic, GABAergic, octopaminergic, and peptidergic neurons (Figure 2—figure supplement 6). We chose lines with minimal off-target expression in neuronal and non-neuronal cells (Figure 2—figure supplement 7) to facilitate the use of these lines in future functional analyses to manipulate the activity of individual cell types.

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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