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 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 Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Chang-Hui Tsao ◽  
Chien-Chun Chen ◽  
Chen-Han Lin ◽  
Hao-Yu Yang ◽  
Suewei Lin
Keyword(s):  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
Energy State ◽  
Fruit Fly ◽  
Mushroom Bodies ◽  
Kenyon Cells ◽  
Control Food ◽  
Seeking Behavior ◽  
Output Neurons ◽  
Food Seeking

The fruit fly can evaluate its energy state and decide whether to pursue food-related cues. Here, we reveal that the mushroom body (MB) integrates hunger and satiety signals to control food-seeking behavior. We have discovered five pathways in the MB essential for hungry flies to locate and approach food. Blocking the MB-intrinsic Kenyon cells (KCs) and the MB output neurons (MBONs) in these pathways impairs food-seeking behavior. Starvation bi-directionally modulates MBON responses to a food odor, suggesting that hunger and satiety controls occur at the KC-to-MBON synapses. These controls are mediated by six types of dopaminergic neurons (DANs). By manipulating these DANs, we could inhibit food-seeking behavior in hungry flies or promote food seeking in fed flies. Finally, we show that the DANs potentially receive multiple inputs of hunger and satiety signals. This work demonstrates an information-rich central circuit in the fly brain that controls hunger-driven food-seeking behavior.

scholarly journals Input connectivity reveals additional heterogeneity of dopaminergic reinforcement in Drosophila

2020 ◽  
Author(s):  
Nils Otto ◽  
Markus W. Pleijzier ◽  
Isabel C. Morgan ◽  
Amelia J. Edmondson-Stait ◽  
Konrad J. Heinz ◽  
...  
Keyword(s):  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
List Type ◽  
Behavioral Experiments ◽  
State Dependent ◽  
Memory Extinction ◽  
Level Function ◽  
Output Neurons ◽  
Functional Relevance ◽  
Dendritic Branches

SummaryDifferent types of Drosophila dopaminergic neurons (DANs) reinforce memories of unique valence and provide state-dependent motivational control [1]. Prior studies suggest that the compartment architecture of the mushroom body (MB) is the relevant resolution for distinct DAN functions [2, 3]. Here we used a recent electron microscope volume of the fly brain [4] to reconstruct the fine anatomy of individual DANs within three MB compartments. We find the 20 DANs of the γ5 compartment, at least some of which provide reward teaching signals, can be clustered into 5 anatomical subtypes that innervate different regions within γ5. Reconstructing 821 upstream neurons reveals input selectivity, supporting the functional relevance of DAN sub-classification. Only one PAM-γ5 DAN subtype γ5(fb) receives direct recurrent input from γ5β’2a mushroom body output neurons (MBONs) and behavioral experiments distinguish a role for these DANs in memory revaluation from those reinforcing sugar memory. Other DAN subtypes receive major, and potentially reinforcing, inputs from putative gustatory interneurons or lateral horn neurons, which can also relay indirect feedback from MBONs. We similarly reconstructed the single aversively reinforcing PPL1-γ1pedc DAN. The γ1pedc DAN inputs mostly differ from those of γ5 DANs and they cluster onto distinct dendritic branches, presumably separating its established roles in aversive reinforcement and appetitive motivation [5, 6]. Tracing also identified neurons that provide broad input to γ5, β’2a and γ1pedc DANs suggesting that distributed DAN populations can be coordinately regulated. These connectomic and behavioral analyses therefore reveal further complexity of dopaminergic reinforcement circuits between and within MB compartments.HighlightsNanoscale anatomy reveals additional subtypes of rewarding dopaminergic neurons.Connectomics reveals extensive input specificity to subtypes of dopaminergic neurons.Axon morphology implies dopaminergic neurons provide subcompartment-level function.Unique dopaminergic subtypes serve aversive memory extinction and sugar learning.

scholarly journals Differential Conditioning Produces Merged Long-term Memory in Drosophila

2021 ◽  
Author(s):  
Bohan Zhao ◽  
Jiameng Sun ◽  
Qian Li ◽  
Yi Zhong
Keyword(s):  
Conditioned Stimulus ◽  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
Differential Conditioning ◽  
Long Term Memory ◽  
Single Trial ◽  
Kenyon Cells ◽  
Output Neurons ◽  
New Protein

AbstractMultiple spaced trials of aversive differential conditioning can produce two independent longterm memories (LTMs) of opposite valence. One is an aversive memory for avoiding the conditioned stimulus (CS+), and the other is a safety memory for approaching the non-conditioned stimulus (CS−). Here, we show that a single trial of aversive differential conditioning yields one merged LTM (mLTM) for avoiding both CS+ and CS−. Such mLTM can be detected after sequential exposures to the shock-paired CS+ and unpaired CS−, and be retrieved by either CS+ or CS−. The formation of mLTM relies on triggering aversive-reinforcing dopaminergic neurons and subsequent new protein synthesis. Expressing mLTM involves αβ Kenyon cells and corresponding approach-directing mushroom body output neurons (MBONs), in which similar-amplitude long-term depression of responses to CS+ and CS− seems to signal the mLTM. Our results suggest that animals can develop distinct strategies for occasional and repeated threatening experiences.

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 Differential conditioning produces merged long-term memory in Drosophila

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Bohan Zhao ◽  
JIameng Sun ◽  
Qian Li ◽  
Yi Zhong
Keyword(s):  
Conditioned Stimulus ◽  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
Differential Conditioning ◽  
Long Term Memory ◽  
Single Trial ◽  
Kenyon Cells ◽  
Output Neurons ◽  
New Protein

Multiple spaced trials of aversive differential conditioning can produce two independent long-term memories (LTMs) of opposite valence. One is an aversive memory for avoiding the conditioned stimulus (CS+), and the other is a safety memory for approaching the non-conditioned stimulus (CS-). Here, we show that a single trial of aversive differential conditioning yields one merged LTM (mLTM) for avoiding both CS+ and CS-. Such mLTM can be detected after sequential exposures to the shock-paired CS+ and unpaired CS-, and be retrieved by either CS+ or CS-. The formation of mLTM relies on triggering aversive-reinforcing dopaminergic neurons and subsequent new protein synthesis. Expressing mLTM involves αβ Kenyon cells and corresponding approach-directing mushroom body output neurons (MBONs), in which similar-amplitude long-term depression of responses to CS+ and CS- seems to signal the mLTM. Our results suggest that animals can develop distinct strategies for occasional and repeated threatening experiences.

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

2020 ◽  
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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