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

By Yoshinori Aso, Divya Sitaraman, Toshiharu Ichinose, K. Kaun, K. Vogt, Ghislain Belliart-Guérin, P. Plaçais, Alice Robie, Nobuhiro Yamagata, C. Schnaitmann and 11 more. 2014

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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. DOI: http://dx.doi.org/10.7554/eLife.04580.001

Subfields: Cellular and Molecular Neuroscience, Ecology, Evolution, Behavior and Systematics, Genetics, Neuroscience

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Citations in the corpus

A Comprehensive Survey of Continual Learning: Theory, Method and Application (2023, background): “, a memory center in fruit fly) coordinating multiple parallel compartments to process the sequentially-arrived experiences [23], [24], [78], [310], [421], corresponding to the use of modular networks in continual learning [15], [353], [430].”
Dopaminergic neurons write and update memories with cell-type-specific rules (2016, methodology): “Previously we described the anatomy of the adult MB and defined 20 types of dopaminergic neurons (DANs) that each innervate distinct MB compartments (Aso et al., 2014a, 2014b).”
Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, neutral): “The MBONs, as the only known efferent pathways of the mushroom body, must translate KC odor representations into adaptive behavioral responses (Aso et al., 2014a; Tanaka et al., 2008).”
Neuronal mechanisms underlying innate and learned olfactory processing in Drosophila. (2019, background): “The current working 209 hypothesis in the field is that memories are read out by MB output neurons (MBONs), which 210 are activated by KCs and bias the fly towards approach or avoidance [74-76].”
A Higher Brain Circuit for Immediate Integration of Conflicting Sensory Information in Drosophila. (2015, methodology): “Activation of the here-identified MBONs triggered arousal and hence interrupted the fly’s sleep pattern significantly [20].”
Cell Type-Specific Transcriptome Analysis in the Drosophila Mushroom Body Reveals Memory-Related Changes in Gene Expression (2016, positive): “The MB contains both intrinsic neurons (termed Kenyon cells or KCs) and extrinsic neurons (comprising output neurons (MBONs), neurons postsynaptic to the KCs, and several types of modulatory neuron) (Aso et al., 2014a; Tanaka et al., 2008).”