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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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Distribution of MBON terminals and DAN dendrites in four brain areas.(A) Schematic of the brain highlighting the areas that exhibit the highest density of MBON terminals and DAN dendrites. (B) A magnified view of a portion of the brain shown in panel A with the CRE, SMP, SIP, and SLP neuropils indicated. (C) Distribution of MBON terminals and DAN dendrites showing their further clustering within the CRE, SMP, SIP, and SLP. Heat map representations of neurite density were computed separately for PAM and PPL1 cluster DAN dendrites and for cholinergic (ACh), GABAergic, and glutamatergic (Glu) MBON terminals. Each horizontal row shows mean intensities in a 10 × 10 × 10 voxel (3.8 × 3.8 × 3.8 μm) cube for each of the indicated neuronal types (columns), represented in an 8-bit scale (0–255). The rows have been sorted based on the sum of the intensity in each volume for all neuronal types. (D–G) Distributions of MBON terminals and DAN dendrites in the CRE (D), SMP (E), SIP (F), and SLP (G) are shown.DOI:http://dx.doi.org/10.7554/eLife.04577.040
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fig19: Distribution of MBON terminals and DAN dendrites in four brain areas.(A) Schematic of the brain highlighting the areas that exhibit the highest density of MBON terminals and DAN dendrites. (B) A magnified view of a portion of the brain shown in panel A with the CRE, SMP, SIP, and SLP neuropils indicated. (C) Distribution of MBON terminals and DAN dendrites showing their further clustering within the CRE, SMP, SIP, and SLP. Heat map representations of neurite density were computed separately for PAM and PPL1 cluster DAN dendrites and for cholinergic (ACh), GABAergic, and glutamatergic (Glu) MBON terminals. Each horizontal row shows mean intensities in a 10 × 10 × 10 voxel (3.8 × 3.8 × 3.8 μm) cube for each of the indicated neuronal types (columns), represented in an 8-bit scale (0–255). The rows have been sorted based on the sum of the intensity in each volume for all neuronal types. (D–G) Distributions of MBON terminals and DAN dendrites in the CRE (D), SMP (E), SIP (F), and SLP (G) are shown.DOI:http://dx.doi.org/10.7554/eLife.04577.040

Mentions: The 34 MBONs represent the sole outputs of the MB lobes. Computational alignment of single-cell images allowed us to localize the axon termini of the MBONs outside the MB. The axon terminals of the MBONs (Figure 18) converge onto five neuropils: the crepine (CRE; a region surrounding the horizontal/medial lobes), the superior medial protocerebrum (SMP), the superior intermediate protocerebrum (SIP), the superior lateral protocerebrum (SLP), and the lateral horn (LH) (Figure 18E). Most MBON types project axons to several of these neuropils (Figure 18—figure supplement 1). Within a neuropil, the axon terminals of each MBON type exhibit distinct and confined projection patterns, suggesting that different MBON types may synapse onto different neurons (Figure 19, also see Figures 14–16 for individual MBON projection patterns). However, we also observed significant overlap between the axon terminals of different MBONs, suggesting that in certain cases MBONs may converge onto the same post-synaptic target neuron (Figure 20A,D,E). These results, obtained by computational alignment, were confirmed for a subset of MBONs by two-color labeling experiments (Figure 20J–L; Video 6).10.7554/eLife.04577.038Figure 18.Projection patterns of the MBON axons and DAN dendrites outside 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)

Distribution of MBON terminals and DAN dendrites in four brain areas.(A) Schematic of the brain highlighting the areas that exhibit the highest density of MBON terminals and DAN dendrites. (B) A magnified view of a portion of the brain shown in panel A with the CRE, SMP, SIP, and SLP neuropils indicated. (C) Distribution of MBON terminals and DAN dendrites showing their further clustering within the CRE, SMP, SIP, and SLP. Heat map representations of neurite density were computed separately for PAM and PPL1 cluster DAN dendrites and for cholinergic (ACh), GABAergic, and glutamatergic (Glu) MBON terminals. Each horizontal row shows mean intensities in a 10 × 10 × 10 voxel (3.8 × 3.8 × 3.8 μm) cube for each of the indicated neuronal types (columns), represented in an 8-bit scale (0–255). The rows have been sorted based on the sum of the intensity in each volume for all neuronal types. (D–G) Distributions of MBON terminals and DAN dendrites in the CRE (D), SMP (E), SIP (F), and SLP (G) are shown.DOI:http://dx.doi.org/10.7554/eLife.04577.040
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fig19: Distribution of MBON terminals and DAN dendrites in four brain areas.(A) Schematic of the brain highlighting the areas that exhibit the highest density of MBON terminals and DAN dendrites. (B) A magnified view of a portion of the brain shown in panel A with the CRE, SMP, SIP, and SLP neuropils indicated. (C) Distribution of MBON terminals and DAN dendrites showing their further clustering within the CRE, SMP, SIP, and SLP. Heat map representations of neurite density were computed separately for PAM and PPL1 cluster DAN dendrites and for cholinergic (ACh), GABAergic, and glutamatergic (Glu) MBON terminals. Each horizontal row shows mean intensities in a 10 × 10 × 10 voxel (3.8 × 3.8 × 3.8 μm) cube for each of the indicated neuronal types (columns), represented in an 8-bit scale (0–255). The rows have been sorted based on the sum of the intensity in each volume for all neuronal types. (D–G) Distributions of MBON terminals and DAN dendrites in the CRE (D), SMP (E), SIP (F), and SLP (G) are shown.DOI:http://dx.doi.org/10.7554/eLife.04577.040
Mentions: The 34 MBONs represent the sole outputs of the MB lobes. Computational alignment of single-cell images allowed us to localize the axon termini of the MBONs outside the MB. The axon terminals of the MBONs (Figure 18) converge onto five neuropils: the crepine (CRE; a region surrounding the horizontal/medial lobes), the superior medial protocerebrum (SMP), the superior intermediate protocerebrum (SIP), the superior lateral protocerebrum (SLP), and the lateral horn (LH) (Figure 18E). Most MBON types project axons to several of these neuropils (Figure 18—figure supplement 1). Within a neuropil, the axon terminals of each MBON type exhibit distinct and confined projection patterns, suggesting that different MBON types may synapse onto different neurons (Figure 19, also see Figures 14–16 for individual MBON projection patterns). However, we also observed significant overlap between the axon terminals of different MBONs, suggesting that in certain cases MBONs may converge onto the same post-synaptic target neuron (Figure 20A,D,E). These results, obtained by computational alignment, were confirmed for a subset of MBONs by two-color labeling experiments (Figure 20J–L; Video 6).10.7554/eLife.04577.038Figure 18.Projection patterns of the MBON axons and DAN dendrites outside 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.

Show MeSH
Related in: MedlinePlus