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 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 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 Reward signaling in a recurrent circuit of dopaminergic neurons and Kenyon cells

2018 ◽  
Author(s):  
Radostina Lyutova ◽  
Maximilian Pfeuffer ◽  
Dennis Segebarth ◽  
Jens Habenstein ◽  
Mareike Selcho ◽  
...  
Keyword(s):  
Learning And Memory ◽  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
Olfactory Learning ◽  
Mushroom Bodies ◽  
Neuronal Circuitry ◽  
Sustained Activity ◽  
Kenyon Cells ◽  
Reward Information ◽  
The Brain

1.AbstractDopaminergic neurons in the brain of theDrosophilalarva play a key role in mediating reward information to the mushroom bodies during appetitive olfactory learning and memory. Using optogenetic activation of Kenyon cells we provide evidence that a functional recurrent signaling loop exists between Kenyon cells and dopaminergic neurons of the primary protocerebral anterior (pPAM) cluster. An optogenetic activation of Kenyon cells paired with an odor is sufficient to induce appetitive memory, while a simultaneous impairment of the dopaminergic pPAM neurons abolishes memory expression. Thus, dopaminergic pPAM neurons mediate reward information to the Kenyon cells, but in turn receive feedback from Kenyon cells. We further show that the activation of recurrent signaling routes within mushroom body circuitry increases the persistence of an odor-sugar memory. Our results suggest that sustained activity in a neuronal circuitry is a conserved mechanism in insects and vertebrates to consolidate memories.

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 Inhibitory muscarinic acetylcholine receptors enhance aversive olfactory conditioning in adult Drosophila

2018 ◽  
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.

scholarly journals Roles for Drosophila mushroom body neurons in olfactory learning and memory

2006 ◽  
Vol 13 (5) ◽  
pp. 659-668 ◽  
Author(s):  
D.-B. G. Akalal ◽  
C. F. Wilson ◽  
L. Zong ◽  
N. K. Tanaka ◽  
K. Ito ◽  
...  
Keyword(s):  
Learning And Memory ◽  
Mushroom Body ◽  
Olfactory Learning

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 Pheromone components affect motivation and induce persistent modulation of associative learning and memory in honey bees

2020 ◽  
Vol 3 (1) ◽  
Author(s):  
David Baracchi ◽  
Amélie Cabirol ◽  
Jean-Marc Devaud ◽  
Albrecht Haase ◽  
Patrizia d’Ettorre ◽  
...  
Keyword(s):  
Associative Learning ◽  
Learning And Memory ◽  
Honey Bees ◽  
Animal Communication ◽  
Animal Cognition ◽  
Olfactory Learning ◽  
Olfactory Conditioning ◽  
Appetitive Motivation ◽  
Pheromone Components ◽  
Chemical Messengers

AbstractSince their discovery in insects, pheromones are considered as ubiquitous and stereotyped chemical messengers acting in intraspecific animal communication. Here we studied the effect of pheromones in a different context as we investigated their capacity to induce persistent modulations of associative learning and memory. We used honey bees, Apis mellifera, and combined olfactory conditioning and pheromone preexposure with disruption of neural activity and two-photon imaging of olfactory brain circuits, to characterize the effect of pheromones on olfactory learning and memory. Geraniol, an attractive pheromone component, and 2-heptanone, an aversive pheromone, improved and impaired, respectively, olfactory learning and memory via a durable modulation of appetitive motivation, which left odor processing unaffected. Consistently, interfering with aminergic circuits mediating appetitive motivation rescued or diminished the cognitive effects induced by pheromone components. We thus show that these chemical messengers act as important modulators of motivational processes and influence thereby animal cognition.

scholarly journals Sparsening and Temporal Sharpening of Olfactory Representations in the Honeybee Mushroom Bodies

2005 ◽  
Vol 94 (5) ◽  
pp. 3303-3313 ◽  
Author(s):  
Paul Szyszka ◽  
Mathias Ditzen ◽  
Alexander Galkin ◽  
C. Giovanni Galizia ◽  
Randolf Menzel
Keyword(s):  
Mushroom Body ◽  
Antennal Lobe ◽  
Activity Patterns ◽  
Projection Neuron ◽  
Insect Brain ◽  
Projection Neurons ◽  
Similar Response ◽  
Kenyon Cell ◽  
Cell Responses ◽  
Kenyon Cells

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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