Activity of Defined Mushroom Body Output Neurons Underlies Learned Olfactory Behavior in Drosophila

By D. Owald, Johannes Felsenberg, Clifford B. Talbot, Gaurav Das, E. Perisse, Wolf Huetteroth, S. Waddell. 2015

325 citations recorded by the source corpus.

Summary During olfactory learning in fruit flies, dopaminergic neurons assign value to odor representations in the mushroom body Kenyon cells. Here we identify a class of downstream glutamatergic mushroom body output neurons (MBONs) called M4/6, or MBON-β2β′2a, MBON-β′2mp, and MBON-γ5β′2a, whose dendritic fields overlap with dopaminergic neuron projections in the tips of the β, β′, and γ lobes. This anatomy and their odor tuning suggests that M4/6 neurons pool odor-driven Kenyon cell synaptic outputs. Like that of mushroom body neurons, M4/6 output is required for expression of appetitive and aversive memory performance. Moreover, appetitive and aversive olfactory conditioning bidirectionally alters the relative odor-drive of M4β′ neurons (MBON-β′2mp). Direct block of M4/6 neurons in naive flies mimics appetitive conditioning, being sufficient to convert odor-driven avoidance into approach, while optogenetically activating these neurons induces avoidance behavior. We therefore propose that drive to the M4/6 neurons reflects odor-directed behavioral choice.

Subfields: Cellular and Molecular Neuroscience, Genetics, Insect Science

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “DOI: 10.7554/eLife.16135.001”
Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “MBON axons converge on a small number of target neuropils, where their concerted activity has been proposed to bias an animal's innate and learned olfactory preferences (Aso et al., 2014b; Hige et al., 2015; Owald et al., 2015).”
Cell Type-Specific Transcriptome Analysis in the Drosophila Mushroom Body Reveals Memory-Related Changes in Gene Expression (2016, unknown): “We further hypothesize that the genes identified so far represent only a fraction of the genes involved in LTM.”
Origins of Cell-Type-Specific Olfactory Processing in the Drosophila Mushroom Body Circuit. (2017, unknown): “These MB output neurons encode valence and bias the behavior toward attraction or aversion in various learning tasks (Aso et al., 2014b; Owald et al., 2015).”
The Drosophila Mushroom Body: From Architecture to Algorithm in a Learning Circuit. (2020, methodology): “This neuron receives input from KCs and feeds it back to the KCs, providing the adaptive inhibition posited by the Marr-Albus model (Inada et al. 2017, Papadopoulou et al. 2011).”
A Complete Electron Microscopy Volume of the Brain of Adult Drosophila melanogaster (2017, background): “KC-MBON synapses are modulated by rewarding or punishing signals from dopaminergic afferent neurons (DANs; Aso et al., 2012; Burke et al., 2012; Liu et al., 2012); this plasticity underlies olfactory memory formation (Hige et al., 2015; Owald et al., 2015; Sejourne et al., 2011).”
Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila (2015, unknown): “As part of this process, stimulus-specific sensory information must be transformed into a format useful for motor output, where more abstract information such as the valence of stimuli are more relevant (Aso et al., 2014b; Hige et al., 2015; Owald et al., 2015).”
Postsynaptic plasticity of cholinergic synapses underlies the induction and expression of appetitive and familiarity memories in Drosophila (2022, methodology): “…of both familiarity learning and appetitive conditioning, odor exposure induces increased α2 subunit dynamics (Figures 6 and 7) accompanying postsynaptic depression (Owald et al., 2015; Hattori et al., 2017; Figure 7), while not or mildly affecting α5 subunits (for familiarity learning).”