scholarly journals Inhibitory muscarinic acetylcholine receptors enhance aversive olfactory learning in adult Drosophila

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Noa Bielopolski ◽  
Hoger Amin ◽  
Anthi A Apostolopoulou ◽  
Eyal Rozenfeld ◽  
Hadas Lerner ◽  
...  

Olfactory associative learning in Drosophila is mediated by synaptic plasticity between the Kenyon cells of the mushroom body and their output neurons. Both Kenyon cells and their inputs from projection neurons 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), particularly in the gamma subtype of Kenyon cells. mAChR-A inhibits odor responses and is localized in Kenyon cell dendrites. Moreover, mAChR-A knockdown impairs the learning-associated depression of odor responses in a mushroom body output neuron. Our results suggest that mAChR-A function in Kenyon cell dendrites is required for synaptic plasticity between Kenyon cells and their output neurons.

2018 ◽  
Author(s):  
Noa Bielopolski ◽  
Hoger Amin ◽  
Anthi A. Apostolopoulou ◽  
Eyal Rozenfeld ◽  
Hadas Lerner ◽  
...  

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.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Chang Zhao ◽  
Yves F. Widmer ◽  
Sören Diegelmann ◽  
Mihai A. Petrovici ◽  
Simon G. Sprecher ◽  
...  

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.


2019 ◽  
Author(s):  
Chang Zhao ◽  
Yves F Widmer ◽  
Soeren Diegelmann ◽  
Mihai Petrovici ◽  
Simon G Sprecher ◽  
...  

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.


Author(s):  
Jürgen Rybak ◽  
Randolf Menzel

The mushroom body (MB) in the insect brain is composed of a large number of densely packed neurons called Kenyon cells (KCs) (Drosophila, 2200; honeybee, 170,000). In most insect species, the MB consists of two caplike dorsal structures, the calyces, which contain the dendrites of KCs, and two to four lobes formed by collaterals of branching KC axons. Although the MB receives input and provides output throughout its whole structure, the neuropil part of the calyx receives predominantly multimodal input from sensory projection neurons (PNs) of second or a higher order, and the lobes send output neurons to many other parts of the brain, including recurrent neurons to the MB calyx. Widely branching, supposedly modulatory neurons (serotonergic, octopaminergic) innervate the MB at all levels (calyx, peduncle, and lobes), including the somata of KCs in the calyx (dopamine).


2013 ◽  
Vol 126 (3) ◽  
pp. 360-371 ◽  
Author(s):  
Abu Syed Md Anisuzzaman ◽  
Junsuke Uwada ◽  
Takayoshi Masuoka ◽  
Hatsumi Yoshiki ◽  
Matomo Nishio ◽  
...  

2005 ◽  
Vol 94 (5) ◽  
pp. 3303-3313 ◽  
Author(s):  
Paul Szyszka ◽  
Mathias Ditzen ◽  
Alexander Galkin ◽  
C. Giovanni Galizia ◽  
Randolf Menzel

We explored the transformations accompanying the transmission of odor information from the first-order processing area, the antennal lobe, to the mushroom body, a higher-order integration center in the insect brain. Using Ca2+ imaging, we recorded activity in the dendrites of the projection neurons that connect the antennal lobe with the mushroom body. Next, we recorded the presynaptic terminals of these projection neurons. Finally, we characterized their postsynaptic partners, the intrinsic neurons of the mushroom body, the clawed Kenyon cells. We found fundamental differences in odor coding between the antennal lobe and the mushroom body. Odors evoked combinatorial activity patterns at all three processing stages, but the spatial patterns became progressively sparser along this path. Projection neuron dendrites and boutons showed similar response profiles, but the boutons were more narrowly tuned to odors. The transmission from projection neuron boutons to Kenyon cells was accompanied by a further sparsening of the population code. Activated Kenyon cells were highly odor specific. Furthermore, the onset of Kenyon cell responses to projection neurons occurred within the first 200 ms and complex temporal patterns were transformed into brief phasic responses. Thus two types of transformations occurred within the MB: sparsening of a combinatorial code, mediated by pre- and postsynaptic processing within the mushroom body microcircuits, and temporal sharpening of postsynaptic Kenyon cell responses, probably involving a broader loop of inhibitory recurrent neurons.


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