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

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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Predictive olfactory learning in Drosophila

Scientific Reports ◽

10.1038/s41598-021-85841-y ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Chang Zhao ◽

Yves F. Widmer ◽

Sören Diegelmann ◽

Mihai A. Petrovici ◽

Simon G. Sprecher ◽

...

Keyword(s):

Synaptic Plasticity ◽

Dopaminergic Neurons ◽

Mushroom Body ◽

Trace Conditioning ◽

Fruit Fly ◽

Olfactory Learning ◽

Shock Strength ◽

Behavioral Experiments ◽

Kenyon Cells ◽

Output Neurons

AbstractOlfactory learning and conditioning in the fruit fly is typically modelled by correlation-based associative synaptic plasticity. It was shown that the conditioning of an odor-evoked response by a shock depends on the connections from Kenyon cells (KC) to mushroom body output neurons (MBONs). Although on the behavioral level conditioning is recognized to be predictive, it remains unclear how MBONs form predictions of aversive or appetitive values (valences) of odors on the circuit level. We present behavioral experiments that are not well explained by associative plasticity between conditioned and unconditioned stimuli, and we suggest two alternative models for how predictions can be formed. In error-driven predictive plasticity, dopaminergic neurons (DANs) represent the error between the predictive odor value and the shock strength. In target-driven predictive plasticity, the DANs represent the target for the predictive MBON activity. Predictive plasticity in KC-to-MBON synapses can also explain trace-conditioning, the valence-dependent sign switch in plasticity, and the observed novelty-familiarity representation. The model offers a framework to dissect MBON circuits and interpret DAN activity during olfactory learning.

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Selective dendritic localization of mRNA in Drosophila mushroom body output neurons

eLife ◽

10.7554/elife.62770 ◽

2021 ◽

Vol 10 ◽

Author(s):

Jessica Mitchell ◽

Carlas S Smith ◽

Josh Titlow ◽

Nils Otto ◽

Pieter van Velde ◽

...

Keyword(s):

Single Molecule ◽

Nicotinic Acetylcholine Receptors ◽

Neuronal Plasticity ◽

Mushroom Body ◽

Acetylcholine Receptors ◽

Behavioural Change ◽

Before And After ◽

Specific Mrnas ◽

Output Neurons ◽

Subcellular Resolution

Memory-relevant neuronal plasticity is believed to require local translation of new proteins at synapses. Understanding this process requires the visualization of the relevant mRNAs within these neuronal compartments. Here we used single-molecule fluorescence in situ hybridization (smFISH) to localize mRNAs at subcellular resolution in the adult Drosophila brain. mRNAs for subunits of nicotinic acetylcholine receptors and kinases could be detected within the dendrites of co-labelled Mushroom Body Output Neurons (MBONs) and their relative abundance showed cell-specificity. Moreover, aversive olfactory learning produced a transient increase in the level of CaMKII mRNA within the dendritic compartments of the 52a MBONs. Localization of specific mRNAs in MBONs before and after learning represents a critical step towards deciphering the role of dendritic translation in the neuronal plasticity underlying behavioural change in Drosophila.

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Author response: Extrinsic activin signaling cooperates with an intrinsic temporal program to increase mushroom body neuronal diversity

10.7554/elife.58880.sa2 ◽

2020 ◽

Author(s):

Anthony M Rossi ◽

Claude Desplan

Keyword(s):

Mushroom Body ◽

Author Response ◽

Neuronal Diversity ◽

Activin Signaling ◽

Temporal Program

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Long-term memory requires sequential protein synthesis in three subsets of mushroom body output neurons in Drosophila

Scientific Reports ◽

10.1038/s41598-017-07600-2 ◽

2017 ◽

Vol 7 (1) ◽

Cited By ~ 13

Author(s):

Jie-Kai Wu ◽

Chu-Yi Tai ◽

Kuan-Lin Feng ◽

Shiu-Ling Chen ◽

Chun-Chao Chen ◽

...

Keyword(s):

Protein Synthesis ◽

Mushroom Body ◽

Long Term Memory ◽

Term Memory ◽

Output Neurons

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Multimodal integration and stimulus categorization in putative mushroom body output neurons of the honeybee

Royal Society Open Science ◽

10.1098/rsos.171785 ◽

2018 ◽

Vol 5 (2) ◽

pp. 171785 ◽

Cited By ~ 23

Author(s):

Martin F. Strube-Bloss ◽

Wolfgang Rössler

Keyword(s):

Visual Information ◽

Mushroom Body ◽

Visual Cues ◽

Sensory Modality ◽

Sensory Information ◽

Insect Brain ◽

Pollinating Insects ◽

Output Neurons ◽

Electrophysiological Characterization ◽

Nonlinear Integration

Flowers attract pollinating insects like honeybees by sophisticated compositions of olfactory and visual cues. Using honeybees as a model to study olfactory–visual integration at the neuronal level, we focused on mushroom body (MB) output neurons (MBON). From a neuronal circuit perspective, MBONs represent a prominent level of sensory-modality convergence in the insect brain. We established an experimental design allowing electrophysiological characterization of olfactory, visual, as well as olfactory–visual induced activation of individual MBONs. Despite the obvious convergence of olfactory and visual pathways in the MB, we found numerous unimodal MBONs. However, a substantial proportion of MBONs (32%) responded to both modalities and thus integrated olfactory–visual information across MB input layers. In these neurons, representation of the olfactory–visual compound was significantly increased compared with that of single components, suggesting an additive, but nonlinear integration. Population analyses of olfactory–visual MBONs revealed three categories: (i) olfactory, (ii) visual and (iii) olfactory–visual compound stimuli. Interestingly, no significant differentiation was apparent regarding different stimulus qualities within these categories. We conclude that encoding of stimulus quality within a modality is largely completed at the level of MB input, and information at the MB output is integrated across modalities to efficiently categorize sensory information for downstream behavioural decision processing.

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Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1216336110 ◽

2013 ◽

Vol 110 (19) ◽

pp. 7898-7903 ◽

Cited By ~ 68

Author(s):

T.-P. Pai ◽

C.-C. Chen ◽

H.-H. Lin ◽

A.-L. Chin ◽

J. S.-Y. Lai ◽

...

Keyword(s):

Mushroom Body ◽

Memory Formation ◽

Long Term Memory ◽

Term Memory ◽

Output Neurons

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Predictive olfactory learning in Drosophila

10.1101/2019.12.29.890533 ◽

2019 ◽

Author(s):

Chang Zhao ◽

Yves F Widmer ◽

Soeren Diegelmann ◽

Mihai Petrovici ◽

Simon G Sprecher ◽

...

Keyword(s):

Synaptic Plasticity ◽

Dopaminergic Neurons ◽

Mushroom Body ◽

Trace Conditioning ◽

Fruit Fly ◽

Olfactory Learning ◽

Shock Strength ◽

Behavioral Experiments ◽

Kenyon Cells ◽

Output Neurons

AbstractOlfactory learning and conditioning in the fruit fly is typically modelled by correlation-based associative synaptic plasticity. It was shown that the conditioning of an odor-evoked response by a shock depends on the connections from Kenyon cells (KC) to mushroom body output neurons (MBONs). Although on the behavioral level conditioning is recognized to be predictive, it remains unclear how MBONs form predictions of aversive or appetitive values (valences) of odors on the circuit level. We present behavioral experiments that are not well explained by associative plasticity between conditioned and unconditioned stimuli, and we suggest two alternative models for how predictions can be formed. In error-driven predictive plasticity, dopaminergic neurons (DANs) represent the error between the predictive odor value and the shock strength. In target-driven predictive plasticity, the DANs represent the target for the predictive MBON activity. Predictive plasticity in KC-to-MBON synapses can also explain trace-conditioning, the valence-dependent sign switch in plasticity, and the observed novelty-familiarity representation. The model offer a framework to dissect MBON circuits and interpret DAN activity during olfactory learning.

Download Full-text