scholarly journals Suppression of GABAergic neurons through D2-like receptor secures efficient conditioning in Drosophila aversive olfactory learning

2019 ◽  
Vol 116 (11) ◽  
pp. 5118-5125 ◽  
Author(s):  
Mingmin Zhou ◽  
Nannan Chen ◽  
Jingsong Tian ◽  
Jianzhi Zeng ◽  
Yunpeng Zhang ◽  
...  
Keyword(s):  
Mushroom Body ◽  
Olfactory Learning ◽  
Gabaergic Inhibition ◽  
Synaptic Connections ◽  
Inhibitory System ◽  
Kenyon Cells ◽  
Synaptic Modification ◽  
In Vivo Functional Imaging ◽  
Negative Modulator

The GABAergic system serves as a vital negative modulator in cognitive functions, such as learning and memory, while the mechanisms governing this inhibitory system remain to be elucidated. In Drosophila, the GABAergic anterior paired lateral (APL) neurons mediate a negative feedback essential for odor discrimination; however, their activity is suppressed by learning via unknown mechanisms. In aversive olfactory learning, a group of dopaminergic (DA) neurons is activated on electric shock (ES) and modulates the Kenyon cells (KCs) in the mushroom body, the center of olfactory learning. Here we find that the same group of DA neurons also form functional synaptic connections with the APL neurons, thereby emitting a suppressive signal to the latter through Drosophila dopamine 2-like receptor (DD2R). Knockdown of either DD2R or its downstream molecules in the APL neurons results in impaired olfactory learning at the behavioral level. Results obtained from in vivo functional imaging experiments indicate that this DD2R-dependent DA-to-APL suppression occurs during odor-ES conditioning and discharges the GABAergic inhibition on the KCs specific to the conditioned odor. Moreover, the decrease in odor response of the APL neurons persists to the postconditioning phase, and this change is also absent in DD2R knockdown flies. Taken together, our findings show that DA-to-GABA suppression is essential for restraining the GABAergic inhibition during conditioning, as well as for inducing synaptic modification in this learning circuit. Such circuit mechanisms may play conserved roles in associative learning across species.

scholarly journals Predictive olfactory learning in Drosophila

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.

scholarly journals Predictive olfactory learning in Drosophila

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.

scholarly journals The anterior paired lateral neuron normalizes odour-evoked activity at the mushroom body calyx

2021 ◽  
Author(s):  
Luigi Prisco ◽  
Stephan Hubertus Deimel ◽  
Hanna Yeliseyeva ◽  
Andre Fiala ◽  
Gaia Tavosanis
Keyword(s):  
Mushroom Body ◽  
Activity Patterns ◽  
Sensory Information ◽  
Input Circuit ◽  
Projection Neurons ◽  
Neuronal Populations ◽  
Kenyon Cells ◽  
Presynaptic Boutons ◽  
Evoked Activity

To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral neuron (APL) in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic Kenyon cells (KCs). Combining EM data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the Kenyon cells requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.

scholarly journals The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Luigi Prisco ◽  
Stephan Hubertus Deimel ◽  
Hanna Yeliseyeva ◽  
André Fiala ◽  
Gaia Tavosanis
Keyword(s):  
Mushroom Body ◽  
Activity Patterns ◽  
Sensory Information ◽  
Input Circuit ◽  
Projection Neurons ◽  
Neuronal Populations ◽  
Kenyon Cells ◽  
Presynaptic Boutons ◽  
Evoked Activity

To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral neuron (APL) in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic Kenyon cells (KCs). Combining EM data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the Kenyon cells requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.

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 ◽  
...  
Keyword(s):  
Synaptic Plasticity ◽  
Mushroom Body ◽  
Acetylcholine Receptors ◽  
Olfactory Learning ◽  
Muscarinic Acetylcholine Receptors ◽  
Projection Neurons ◽  
Kenyon Cell ◽  
Muscarinic Acetylcholine ◽  
Kenyon Cells ◽  
Output Neurons

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.

scholarly journals The neuronal architecture of the mushroom body provides a logic for associative learning

eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Yoshinori Aso ◽  
Daisuke Hattori ◽  
Yang Yu ◽  
Rebecca M Johnston ◽  
Nirmala A Iyer ◽  
...  
Keyword(s):  
Associative Learning ◽  
Learning And Memory ◽  
Mushroom Body ◽  
Dopaminergic Neuron ◽  
Olfactory Learning ◽  
Kenyon Cell ◽  
Feedforward Network ◽  
Kenyon Cells ◽  
Functional Logic ◽  
Dendritic Arbors

We identified the neurons comprising the Drosophila mushroom body (MB), an associative center in invertebrate brains, and provide a comprehensive map describing their potential connections. Each of the 21 MB output neuron (MBON) types elaborates segregated dendritic arbors along the parallel axons of ∼2000 Kenyon cells, forming 15 compartments that collectively tile the MB lobes. MBON axons project to five discrete neuropils outside of the MB and three MBON types form a feedforward network in the lobes. Each of the 20 dopaminergic neuron (DAN) types projects axons to one, or at most two, of the MBON compartments. Convergence of DAN axons on compartmentalized Kenyon cell–MBON synapses creates a highly ordered unit that can support learning to impose valence on sensory representations. The elucidation of the complement of neurons of the MB provides a comprehensive anatomical substrate from which one can infer a functional logic of associative olfactory learning and memory.

scholarly journals Mechanisms underlying homeostatic plasticity in theDrosophilamushroom body in vivo

2020 ◽  
Vol 117 (28) ◽  
pp. 16606-16615 ◽  
Author(s):  
Anthi A. Apostolopoulou ◽  
Andrew C. Lin
Keyword(s):  
Mushroom Body ◽  
Feedback Inhibition ◽  
Homeostatic Plasticity ◽  
Projection Neurons ◽  
Kenyon Cell ◽  
Network Function ◽  
Kenyon Cells ◽  
Central Brain ◽  
Artificial Activation

Neural network function requires an appropriate balance of excitation and inhibition to be maintained by homeostatic plasticity. However, little is known about homeostatic mechanisms in the intact central brain in vivo. Here, we study homeostatic plasticity in theDrosophilamushroom body, where Kenyon cells receive feedforward excitation from olfactory projection neurons and feedback inhibition from the anterior paired lateral neuron (APL). We show that prolonged (4-d) artificial activation of the inhibitory APL causes increased Kenyon cell odor responses after the artificial inhibition is removed, suggesting that the mushroom body compensates for excess inhibition. In contrast, there is little compensation for lack of inhibition (blockade of APL). The compensation occurs through a combination of increased excitation of Kenyon cells and decreased activation of APL, with differing relative contributions for different Kenyon cell subtypes. Our findings establish the fly mushroom body as a model for homeostatic plasticity in vivo.

scholarly journals Learning with naturalistic odor representations in a dynamic model of the Drosophila olfactory system

2019 ◽  
Author(s):  
Ann Kennedy
Keyword(s):  
Associative Learning ◽  
Dynamic Model ◽  
Olfactory System ◽  
Mushroom Body ◽  
Sparse Representations ◽  
Olfactory Learning ◽  
Associative Memories ◽  
Kenyon Cells ◽  
Output Neurons ◽  
Odor Receptors

AbstractMany odor receptors in the insect olfactory system are broadly tuned, yet insects can form associative memories that are odor-specific. The key site of associative olfactory learning in insects, the mushroom body, contains a population of Kenyon Cells (KCs) that form sparse representations of odor identity and enable associative learning of odors by mushroom body output neurons (MBONs). This architecture is well suited to odor-specific associative learning if KC responses to odors are uncorrelated with each other, however it is unclear whether this hold for actual KC representations of natural odors. We introduce a dynamic model of the Drosophila olfactory system that predicts the responses of KCs to a panel of 110 natural and monomolecular odors, and examine the generalization properties of associative learning in model MBONs. While model KC representations of odors are often quite correlated, we identify mechanisms by which odor-specific associative learning is still possible.

scholarly journals Reciprocal synapses between mushroom body and dopamine neurons form a positive feedback loop required for learning

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Isaac Cervantes-Sandoval ◽  
Anna Phan ◽  
Molee Chakraborty ◽  
Ronald L Davis
Keyword(s):  
Nicotinic Acetylcholine Receptors ◽  
Positive Feedback ◽  
Mushroom Body ◽  
Acetylcholine Receptors ◽  
Critical Role ◽  
Olfactory Learning ◽  
Dopamine Neurons ◽  
Olfactory Conditioning ◽  
Kenyon Cells ◽  
Presynaptic Calcium

Current thought envisions dopamine neurons conveying the reinforcing effect of the unconditioned stimulus during associative learning to the axons of Drosophila mushroom body Kenyon cells for normal olfactory learning. Here, we show using functional GFP reconstitution experiments that Kenyon cells and dopamine neurons from axoaxonic reciprocal synapses. The dopamine neurons receive cholinergic input via nicotinic acetylcholine receptors from the Kenyon cells; knocking down these receptors impairs olfactory learning revealing the importance of these receptors at the synapse. Blocking the synaptic output of Kenyon cells during olfactory conditioning reduces presynaptic calcium transients in dopamine neurons, a finding consistent with reciprocal communication. Moreover, silencing Kenyon cells decreases the normal chronic activity of the dopamine neurons. Our results reveal a new and critical role for positive feedback onto dopamine neurons through reciprocal connections with Kenyon cells for normal olfactory learning.

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