Different classes of input and output neurons reveal new features in microglomeruli of the adult Drosophila mushroom body calyx

We reconstructed, from a whole CNS EM volume, the synaptic map of input and output neurons that underlie food intake behavior of Drosophila larvae. Input neurons originate from enteric, pharyngeal and external sensory organs and converge onto seven distinct sensory synaptic compartments within the CNS. Output neurons consist of feeding motor, serotonergic modulatory and neuroendocrine neurons. Monosynaptic connections from a set of sensory synaptic compartments cover the motor, modulatory and neuroendocrine targets in overlapping domains. Polysynaptic routes are superimposed on top of monosynaptic connections, resulting in divergent sensory paths that converge on common outputs. A completely different set of sensory compartments is connected to the mushroom body calyx. The mushroom body output neurons are connected to interneurons that directly target the feeding output neurons. Our results illustrate a circuit architecture in which monosynaptic and multisynaptic connections from sensory inputs traverse onto output neurons via a series of converging paths.

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The connectome of the adult Drosophila mushroom body: implications for function

10.1101/2020.08.29.273276 ◽

2020 ◽

Cited By ~ 3

Author(s):

Feng Li ◽

Jack Lindsey ◽

Elizabeth C. Marin ◽

Nils Otto ◽

Marisa Dreher ◽

...

Keyword(s):

Dopaminergic Neurons ◽

Mushroom Body ◽

Experimental Studies ◽

Central Complex ◽

Sensory Inputs ◽

Descending Neurons ◽

Sensory Modalities ◽

Output Neurons ◽

Transfer Of Information ◽

Adult Drosophila

AbstractMaking inferences about the computations performed by neuronal circuits from synapse-level connectivity maps is an emerging opportunity in neuroscience. The mushroom body (MB) is well positioned for developing and testing such an approach due to its conserved neuronal architecture, recently completed dense connectome, and extensive prior experimental studies of its roles in learning, memory and activity regulation. Here we identify new components of the MB circuit in Drosophila, including extensive visual input and MB output neurons (MBONs) with direct connections to descending neurons. We find unexpected structure in sensory inputs, in the transfer of information about different sensory modalities to MBONs, and in the modulation of that transfer by dopaminergic neurons (DANs). We provide insights into the circuitry used to integrate MB outputs, connectivity between the MB and the central complex and inputs to DANs, including feedback from MBONs. Our results provide a foundation for further theoretical and experimental work.

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Inhibitory muscarinic acetylcholine receptors enhance aversive olfactory conditioning in adult Drosophila

10.1101/382440 ◽

2018 ◽

Cited By ~ 1

Author(s):

Noa Bielopolski ◽

Hoger Amin ◽

Anthi A. Apostolopoulou ◽

Eyal Rozenfeld ◽

Hadas Lerner ◽

...

Keyword(s):

Mushroom Body ◽

Acetylcholine Receptors ◽

Physiological Function ◽

Muscarinic Acetylcholine Receptors ◽

Kenyon Cell ◽

Olfactory Conditioning ◽

Muscarinic Acetylcholine ◽

Kenyon Cells ◽

Output Neurons ◽

Adult Drosophila

AbstractOlfactory associative learning inDrosophilais mediated by synaptic plasticity between the Kenyon cells of the mushroom body and their output neurons. Both Kenyon cells and their inputs are cholinergic, yet little is known about the physiological function of muscarinic acetylcholine receptors in learning in adult flies. Here we show that aversive olfactory learning in adult flies requires type A muscarinic acetylcholine receptors (mAChR-A) specifically in the gamma subtype of Kenyon cells. Surprisingly, mAChR-A inhibits odor responses in both Kenyon cell dendrites and axons. Moreover, mAChR-A knockdown impairs the learning-associated depression of odor responses in a mushroom body output neuron. Our results suggest that mAChR-A is required at Kenyon cell presynaptic terminals to depress the synapses between Kenyon cells and their output neurons, and may suggest a role for the recently discovered axo-axonal synapses between Kenyon cells.

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The connectome of the adult Drosophila mushroom body provides insights into function

eLife ◽

10.7554/elife.62576 ◽

2020 ◽

Vol 9 ◽

Cited By ~ 4

Author(s):

Feng Li ◽

Jack W Lindsey ◽

Elizabeth C Marin ◽

Nils Otto ◽

Marisa Dreher ◽

...

Keyword(s):

Dopaminergic Neurons ◽

Mushroom Body ◽

Experimental Studies ◽

Central Complex ◽

Sensory Inputs ◽

Descending Neurons ◽

Sensory Modalities ◽

Output Neurons ◽

Transfer Of Information ◽

Adult Drosophila

Making inferences about the computations performed by neuronal circuits from synapse-level connectivity maps is an emerging opportunity in neuroscience. The mushroom body (MB) is well positioned for developing and testing such an approach due to its conserved neuronal architecture, recently completed dense connectome, and extensive prior experimental studies of its roles in learning, memory and activity regulation. Here we identify new components of the MB circuit in Drosophila, including extensive visual input and MB output neurons (MBONs) with direct connections to descending neurons. We find unexpected structure in sensory inputs, in the transfer of information about different sensory modalities to MBONs, and in the modulation of that transfer by dopaminergic neurons (DANs). We provide insights into the circuitry used to integrate MB outputs, connectivity between the MB and the central complex and inputs to DANs, including feedback from MBONs. Our results provide a foundation for further theoretical and experimental work.

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Octopaminergic neurons have multiple targets in Drosophila larval mushroom body calyx and regulate behavioral odor discrimination

10.1101/295659 ◽

2018 ◽

Author(s):

J Y Hilary Wong ◽

Bo Angela Wan ◽

Tom Bland ◽

Marcella Montagnese ◽

Alex McLachlan ◽

...

Keyword(s):

Mushroom Body ◽

Inhibitory Neuron ◽

Odor Discrimination ◽

Learning Ability ◽

Projection Neurons ◽

Input Region ◽

Output Neurons ◽

Mushroom Body Calyx ◽

Intrinsic Neurons ◽

Selection Of

AbstractDiscrimination of sensory signals is essential for an organism to form and retrieve memories of relevance in a given behavioural context. Sensory representations are modified dynamically by changes in behavioral state, facilitating context-dependent selection of behavior, through signals carried by noradrenergic input in mammals, or octopamine (OA) in insects. To understand the circuit mechanisms of this signaling, we characterized the function of two OA neurons, sVUM1 neurons, that originate in the subesophageal zone (SEZ) and target the input region of the memory center, the mushroom body (MB) calyx, in larval Drosophila. We find that sVUM1 neurons target multiple neurons, including olfactory projection neurons (PNs), the inhibitory neuron APL, and a pair of extrinsic output neurons, but relatively few mushroom body intrinsic neurons, Kenyon cells. PN terminals carried the OA receptor Oamb, a Drosophila α1-adrenergic receptor ortholog. Using an odor discrimination learning paradigm, we showed that optogenetic activation of OA neurons compromised discrimination of similar odors but not learning ability. Our results suggest that sVUM1 neurons modify odor representations via multiple extrinsic inputs at the sensory input area to the MB olfactory learning circuit.

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Faculty Opinions recommendation of Synaptic organization in the adult Drosophila mushroom body calyx.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1448971.926076 ◽

2010 ◽

Author(s):

Kevan A Martin ◽

Nuno Miguel MaÇarico Amorim da Costa

Keyword(s):

Mushroom Body ◽

Synaptic Organization ◽

Mushroom Body Calyx ◽

Adult Drosophila

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The Neurophysiology of Autonomic Dysfunction in SCI: Plasticity in the Input and Output Neurons

10.21236/ada623381 ◽

2014 ◽

Cited By ~ 1

Author(s):

Keith Tansey

Keyword(s):

Autonomic Dysfunction ◽

Input And Output ◽

Output Neurons

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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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