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Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila.

Aso Y, Sitaraman D, Ichinose T, Kaun KR, Vogt K, Belliart-Guérin G, Plaçais PY, Robie AA, Yamagata N, Schnaitmann C, Rowell WJ, Johnston RM, Ngo TT, Chen N, Korff W, Nitabach MN, Heberlein U, Preat T, Branson KM, Tanimoto H, Rubin GM - Elife (2014)

Bottom Line: The behavioral effects of MBON perturbation are combinatorial, suggesting that the MBON ensemble collectively represents valence.We propose that local, stimulus-specific dopaminergic modulation selectively alters the balance within the MBON network for those stimuli.Our results suggest that valence encoded by the MBON ensemble biases memory-based action selection.

View Article: PubMed Central - PubMed

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

ABSTRACT
Animals discriminate stimuli, learn their predictive value and use this knowledge to modify their behavior. In Drosophila, the mushroom body (MB) plays a key role in these processes. Sensory stimuli are sparsely represented by ∼2000 Kenyon cells, which converge onto 34 output neurons (MBONs) of 21 types. We studied the role of MBONs in several associative learning tasks and in sleep regulation, revealing the extent to which information flow is segregated into distinct channels and suggesting possible roles for the multi-layered MBON network. We also show that optogenetic activation of MBONs can, depending on cell type, induce repulsion or attraction in flies. The behavioral effects of MBON perturbation are combinatorial, suggesting that the MBON ensemble collectively represents valence. We propose that local, stimulus-specific dopaminergic modulation selectively alters the balance within the MBON network for those stimuli. Our results suggest that valence encoded by the MBON ensemble biases memory-based action selection.

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Expression patterns of split-GAL4s that caused appetitive visual memory phenotypes.(A–E) Expression patterns of the indicated split-GAL4 drivers as assessed with pJFRC2-10XUAS-IVS-mCD8::GFP (VK00005). Full confocal stacks of these images are available at www.janelia.org/split-gal4.DOI:http://dx.doi.org/10.7554/eLife.04580.025
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fig9s1: Expression patterns of split-GAL4s that caused appetitive visual memory phenotypes.(A–E) Expression patterns of the indicated split-GAL4 drivers as assessed with pJFRC2-10XUAS-IVS-mCD8::GFP (VK00005). Full confocal stacks of these images are available at www.janelia.org/split-gal4.DOI:http://dx.doi.org/10.7554/eLife.04580.025

Mentions: (A) Diagram of the training protocol used for appetitive visual conditioning. Starved flies were trained with sugar and the PI calculated in the same manner as in aversive visual conditioning (see Figure 8A). Flies were trained and tested at the restrictive temperature. (B) Screening for MBONs required for aversive visual conditioning. pJFRC100-20XUAS-TTS-Shibire-ts1-p10 (VK00005) was used to block synaptic transmission. MBONs have been grouped by neurotransmitter and color-coded. The bottom and top of each box represents the first and third quartile, and the line inside the box is the median. The whiskers represent the 10th and 90th percentiles. The gray rectangle spanning the horizontal axis indicates the interquartile range of the control. Statistical tests are described in methods: *, p < 0.05. Gray asterisks indicate lines that were not significantly different from GAL4/+ controls (MB083C, MB082C, MB018B and MB242A) or had altered color preference (MB298B). The relative expression levels produced by the split-GAL4 driver lines in each cell type (indicated in a gray scale) are based on imaging with pJFRC2-10XUAS-IVS-mCD8::GFP (VK00005). Images of the expression patterns of selected drivers are shown in Figure 9—figure supplement 1. (C) Visual appetitive memory was impaired at restrictive temperature by blocking the subsets of glutamate or acetylcholine MBONs labeled by MB434B, MB011B, MB210B, MB542B and MB052B compared to +/Shi and GAL4/+ controls. (D) No appetitive visual memory impairment was found at the permissive temperature compared to +/Shi. (E) Sugar attraction in untrained flies was not impaired at the restrictive temperature compared to +/Shi. (F) Rendering of MBONs implicated in appetitive visual memory. MBONs grouped by square brackets represent cases where the available set of driver lines do not allow assigning an effect to a single cell type, but only to the bracketed set. (G) Circuit diagram for appetitive visual memory. Glutamatergic MBONs (MBON-β′2mp and MBON-γ5β′2a) mediate visual appetitive memory. PAM neurons innervating these compartments of the MB lobes (see Figure 1A) are thought to convey the sucrose reward signal (Vogt et al., 2014). MBON-γ4>γ1γ2 feeds forward onto the dendrites of MBON-γ1pedc>α/β, a neuron required for aversive odor and aversive visual memory. Cholinergic V2 cluster neurons also appear to play a role.


Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila.

Aso Y, Sitaraman D, Ichinose T, Kaun KR, Vogt K, Belliart-Guérin G, Plaçais PY, Robie AA, Yamagata N, Schnaitmann C, Rowell WJ, Johnston RM, Ngo TT, Chen N, Korff W, Nitabach MN, Heberlein U, Preat T, Branson KM, Tanimoto H, Rubin GM - Elife (2014)

Expression patterns of split-GAL4s that caused appetitive visual memory phenotypes.(A–E) Expression patterns of the indicated split-GAL4 drivers as assessed with pJFRC2-10XUAS-IVS-mCD8::GFP (VK00005). Full confocal stacks of these images are available at www.janelia.org/split-gal4.DOI:http://dx.doi.org/10.7554/eLife.04580.025
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Related In: Results  -  Collection

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fig9s1: Expression patterns of split-GAL4s that caused appetitive visual memory phenotypes.(A–E) Expression patterns of the indicated split-GAL4 drivers as assessed with pJFRC2-10XUAS-IVS-mCD8::GFP (VK00005). Full confocal stacks of these images are available at www.janelia.org/split-gal4.DOI:http://dx.doi.org/10.7554/eLife.04580.025
Mentions: (A) Diagram of the training protocol used for appetitive visual conditioning. Starved flies were trained with sugar and the PI calculated in the same manner as in aversive visual conditioning (see Figure 8A). Flies were trained and tested at the restrictive temperature. (B) Screening for MBONs required for aversive visual conditioning. pJFRC100-20XUAS-TTS-Shibire-ts1-p10 (VK00005) was used to block synaptic transmission. MBONs have been grouped by neurotransmitter and color-coded. The bottom and top of each box represents the first and third quartile, and the line inside the box is the median. The whiskers represent the 10th and 90th percentiles. The gray rectangle spanning the horizontal axis indicates the interquartile range of the control. Statistical tests are described in methods: *, p < 0.05. Gray asterisks indicate lines that were not significantly different from GAL4/+ controls (MB083C, MB082C, MB018B and MB242A) or had altered color preference (MB298B). The relative expression levels produced by the split-GAL4 driver lines in each cell type (indicated in a gray scale) are based on imaging with pJFRC2-10XUAS-IVS-mCD8::GFP (VK00005). Images of the expression patterns of selected drivers are shown in Figure 9—figure supplement 1. (C) Visual appetitive memory was impaired at restrictive temperature by blocking the subsets of glutamate or acetylcholine MBONs labeled by MB434B, MB011B, MB210B, MB542B and MB052B compared to +/Shi and GAL4/+ controls. (D) No appetitive visual memory impairment was found at the permissive temperature compared to +/Shi. (E) Sugar attraction in untrained flies was not impaired at the restrictive temperature compared to +/Shi. (F) Rendering of MBONs implicated in appetitive visual memory. MBONs grouped by square brackets represent cases where the available set of driver lines do not allow assigning an effect to a single cell type, but only to the bracketed set. (G) Circuit diagram for appetitive visual memory. Glutamatergic MBONs (MBON-β′2mp and MBON-γ5β′2a) mediate visual appetitive memory. PAM neurons innervating these compartments of the MB lobes (see Figure 1A) are thought to convey the sucrose reward signal (Vogt et al., 2014). MBON-γ4>γ1γ2 feeds forward onto the dendrites of MBON-γ1pedc>α/β, a neuron required for aversive odor and aversive visual memory. Cholinergic V2 cluster neurons also appear to play a role.

Bottom Line: The behavioral effects of MBON perturbation are combinatorial, suggesting that the MBON ensemble collectively represents valence.We propose that local, stimulus-specific dopaminergic modulation selectively alters the balance within the MBON network for those stimuli.Our results suggest that valence encoded by the MBON ensemble biases memory-based action selection.

View Article: PubMed Central - PubMed

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

ABSTRACT
Animals discriminate stimuli, learn their predictive value and use this knowledge to modify their behavior. In Drosophila, the mushroom body (MB) plays a key role in these processes. Sensory stimuli are sparsely represented by ∼2000 Kenyon cells, which converge onto 34 output neurons (MBONs) of 21 types. We studied the role of MBONs in several associative learning tasks and in sleep regulation, revealing the extent to which information flow is segregated into distinct channels and suggesting possible roles for the multi-layered MBON network. We also show that optogenetic activation of MBONs can, depending on cell type, induce repulsion or attraction in flies. The behavioral effects of MBON perturbation are combinatorial, suggesting that the MBON ensemble collectively represents valence. We propose that local, stimulus-specific dopaminergic modulation selectively alters the balance within the MBON network for those stimuli. Our results suggest that valence encoded by the MBON ensemble biases memory-based action selection.

Show MeSH