Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila

doi:10.1523/JNEUROSCI.23-33-10495.2003

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Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila

Journal Article•DOI•

Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila

Martin Schwaerzel, Maria Monastirioti, Henrike Scholz, Florence Friggi-Grelin, Serge Birman, Martin Heisenberg - Show less +2 more

19 Nov 2003-The Journal of Neuroscience (Society for Neuroscience)-Vol. 23, Iss: 33, pp 10495-10502

TL;DR: The results suggest that in associative conditioning, different memories are formed of the same odor under different circumstances, and that they are linked to the respective motivational systems by their specific modulatory pathways.

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Abstract: The catecholamines play a major role in the regulation of behavior. Here we investigate, in the fly Drosophila melanogaster, the role of dopamine and octopamine (the presumed arthropod homolog of norepinephrine) during the formation of appetitive and aversive olfactory memories. We find that for the formation of both types of memories, cAMP signaling is necessary and sufficient within the same subpopulation of mushroom-body intrinsic neurons. On the other hand, memory formation can be distinguished by the requirement for different catecholamines, dopamine for aversive and octopamine for appetitive conditioning. Our results suggest that in associative conditioning, different memories are formed of the same odor under different circumstances, and that they are linked to the respective motivational systems by their specific modulatory pathways.

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Journal Article•DOI•

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

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Yoshinori Aso¹, Daisuke Hattori¹, Yang Yu¹, Rebecca M. Johnston¹, Nirmala Iyer¹, Teri T.B. Ngo¹, Heather Dionne¹, Larry F. Abbott², Richard Axel¹, Hiromu Tanimoto³, Gerald M. Rubin¹ - Show less +7 more•Institutions (3)

Howard Hughes Medical Institute¹, Columbia University², Max Planck Society³

23 Dec 2014-eLife

TL;DR: 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.

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Abstract: 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.

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813 citations

Cites background or methods from "Dopamine and Octopamine Differentia..."

...In accord with this model, DAN activity is required during learning (Schwaerzel et al., 2003; Aso et al., 2010, 2012; Burke et al., 2012; Liu et al., 2012) and exogenous activation of DAN subpopulations can serve as an US in associative learning paradigms (Schroll et al., 2006; Claridge-Chang et…...
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...In accord with this model, DAN activity is required during learning (Schwaerzel et al., 2003; Aso et al., 2010, 2012; Burke et al., 2012; Liu et al., 2012) and exogenous activation of DAN subpopulations can serve as an US in associative learning paradigms (Schroll et al....
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...…been shown to project axon terminals to specific regions within the MB lobes and transmit information about reward and punishment to the MB to guide learning (Schwaerzel et al., 2003; Claridge-Chang et al., 2009; Mao and Davis, 2009; Aso et al., 2010, 2012; Burke et al., 2012; Liu et al., 2012)....
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...Two clusters of dopaminergic neurons (PPL1 and PAM) have previously been shown to project axon terminals to specific regions within the MB lobes and transmit information about reward and punishment to the MB to guide learning (Schwaerzel et al., 2003; Claridge-Chang et al., 2009; Mao and Davis, 2009; Aso et al., 2010, 2012; Burke et al., 2012; Liu et al., 2012)....
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Journal Article•DOI•

Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans

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Yun Zhang¹, Hang Lu¹, Cornelia I. Bargmann¹•Institutions (1)

Howard Hughes Medical Institute¹

10 Nov 2005-Nature

TL;DR: It is shown that C. elegans modifies its olfactory preferences after exposure to pathogenic bacteria, avoiding odours from the pathogen and increasing its attraction to odour from familiar nonpathogenic bacteria.

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Abstract: Food can be hazardous, either through toxicity or through bacterial infections that follow the ingestion of a tainted food source. Because learning about food quality enhances survival, one of the most robust forms of olfactory learning is conditioned avoidance of tastes associated with visceral malaise. The nematode Caenorhabditis elegans feeds on bacteria but is susceptible to infection by pathogenic bacteria in its natural environment. Here we show that C. elegans modifies its olfactory preferences after exposure to pathogenic bacteria, avoiding odours from the pathogen and increasing its attraction to odours from familiar nonpathogenic bacteria. Particular bacteria elicit specific changes in olfactory preferences that are suggestive of associative learning. Exposure to pathogenic bacteria increases serotonin in ADF chemosensory neurons by transcriptional and post-transcriptional mechanisms. Serotonin functions through MOD-1, a serotonin-gated chloride channel expressed in sensory interneurons, to promote aversive learning. An increase in serotonin may represent the negative reinforcing stimulus in pathogenic infection.

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705 citations

Journal Article•DOI•

Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae.

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Christian Schroll¹, Thomas Riemensperger¹, Daniel Bucher¹, Julia Ehmer¹, Thomas Völler¹, Karen Erbguth¹, Bertram Gerber¹, Thomas Hendel¹, Georg Nagel¹, Erich Buchner¹, André Fiala¹ - Show less +7 more•Institutions (1)

University of Würzburg¹

05 Sep 2006-Current Biology

TL;DR: It is demonstrated that antagonistic modulatory subsystems are sufficient to substitute for aversive and appetitive reinforcement during classical conditioning and that distinct neuronal populations can be activated simply by illuminating the animals with blue light.

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631 citations

Cites background from "Dopamine and Octopamine Differentia..."

...In adult Drosophila, dopaminergic neurons respond to a punishing electric shock stimulus [28], and blocking synaptic transmission from dopaminergic neurons during olfactory learning impairs aversive but not appetitive memory formation [3]....
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...On the other hand, octopamine has been shown to be a necessary transmitter for appetitive olfactory learning in adult Drosophila and crickets [3, 4]....
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Journal Article•DOI•

Tyramine and octopamine: ruling behavior and metabolism.

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Thomas Roeder¹•Institutions (1)

University of Marburg¹

01 Jan 2005-Annual Review of Entomology

TL;DR: Progress made on all levels of OA and TA research has enabled researchers to understand better the molecular events underlying the control of complex behaviors, and these events represent promising targets for new insecticides.

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Abstract: Octopamine (OA) and tyramine (TA) are the invertebrate counterparts of the vertebrate adrenergic transmitters They are decarboxylation products of the amino acid tyrosine, with TA as the biological precursor of OA Nevertheless, both compounds are independent neurotransmitters that act through G protein-coupled receptors OA modulates a plethora of behaviors and peripheral and sense organs, enabling the insect to respond correctly to external stimuli Because these two phenolamines are the only biogenic amines whose physiological significance is presumably restricted to invertebrates, pharmacologists have focused their attention on the corresponding receptors, which are still believed to represent promising targets for new insecticides Recent progress made on all levels of OA and TA research has enabled researchers to understand better the molecular events underlying the control of complex behaviors

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630 citations

Journal Article•DOI•

Remote Control of Behavior through Genetically Targeted Photostimulation of Neurons

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Susana Q. Lima¹, Gero Miesenböck¹•Institutions (1)

Yale University¹

08 Apr 2005-Cell

TL;DR: Encodable phototriggers provide noninvasive control interfaces for studying the connectivity and dynamics of neural circuits, for assigning behavioral content to neurons and their activity patterns, and, potentially, for restoring information corrupted by injury or disease.

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584 citations

Cites background from "Dopamine and Octopamine Differentia..."

...…et al., 1997), learning (Quinn and Greenspan, 984), and sleep and wakefulness (Hendricks et al., 000; Shaw et al., 2000), as well as attempts to identify he neural symbols representing reward and punishent (Schwaerzel et al., 2003), expectation, and cateories of generalization (Liu et al., 1999)....
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References

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Open Access

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Journal Article•DOI•

The Molecular Biology of Memory Storage: A Dialogue Between Genes and Synapses

[...]

Eric R. Kandel¹•Institutions (1)

Howard Hughes Medical Institute¹

02 Nov 2001-Science

TL;DR: This book aims to investigate elementary forms of learning and memory at a cellular molecular level—as specific molecular activities within identified nerve cells withinidentified nerve cells.

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Abstract: One of the most remarkable aspects of an animal's behavior is the ability to modify that behavior by learning, an ability that reaches its highest form in human beings. For me, learning and memory have proven to be endlessly fascinating mental processes because they address one of the fundamental features of human activity: our ability to acquire new ideas from experience and to retain these ideas over time in memory. Moreover, unlike other mental processes such as thought, language, and consciousness, learning seemed from the outset to be readily accessible to cellular and molecular analysis. I, therefore, have been curious to know: What changes in the brain when we learn? And, once something is learned, how is that information retained in the brain? I have tried to address these questions through a reductionist approach that would allow me to investigate elementary forms of learning and memory at a cellular molecular level-as specific molecular activities within identified nerve cells.

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3,609 citations

"Dopamine and Octopamine Differentia..." refers background in this paper

...Appetitive and aversive olfactory memories are localized to the same neuropil Associative behavioral adaptations are mediated by the plasticity of synapses within neural circuits (Kandel, 2001)....
[...]
...One of the central tenets of cellular learning models is that cAMP signaling is involved in synaptic plasticity and associative memory formation (Yin and Tully, 1996; Kandel, 2001; Roman and Davis, 2001; Antonov et al., 2003)....
[...]
...One of the central tenets of cellular learning models is that cAMP signaling is involved in synaptic plasticity and associative memory formation (Yin and Tully, 1996; Kandel, 2001; Roman and Davis, 2001; Antonov et al., 2003)....
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...This presynaptic aspect of synaptic and behavioral plasticity has been documented for a variety of organisms throughout the animal kingdom using different kinds of reinforcers (Yin and Tully, 1996; Kandel, 2001)....
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...In many species, including Aplysia, mouse, and Drosophila, the type-1 AC has been shown to be critical in synaptic plasticity (Lechner and Byrne, 1998; Villacres et al., 1998; Kandel, 2001; Antonov et al., 2003)....
[...]

Journal Article•DOI•

Mushroom body memoir: From maps to models

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Martin Heisenberg¹•Institutions (1)

University of Würzburg¹

01 Apr 2003-Nature Reviews Neuroscience

TL;DR: Genetic intervention in the fly Drosophila melanogaster has provided strong evidence that the mushroom bodies of the insect brain act as the seat of a memory trace for odours, and the development of a circuit model that addresses this function might allow the mushrooms to throw light on the basic operating principles of the brain.

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Abstract: Genetic intervention in the fly Drosophila melanogaster has provided strong evidence that the mushroom bodies of the insect brain act as the seat of a memory trace for odours. This localization gives the mushroom bodies a place in a network model of olfactory memory that is based on the functional anatomy of the olfactory system. In the model, complex odour mixtures are assumed to be represented by activated sets of intrinsic mushroom body neurons. Conditioning renders an extrinsic mushroom-body output neuron specifically responsive to such a set. Mushroom bodies have a second, less understood function in the organization of the motor output. The development of a circuit model that also addresses this function might allow the mushroom bodies to throw light on the basic operating principles of the brain.

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1,189 citations

"Dopamine and Octopamine Differentia..." refers background or result in this paper

...These findings confirm and extend previous work, concluding that output synapses of Kenyon cells are the site of olfactory memory (summarized in Heisenberg, 2003)....
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...Based on the functional anatomy of the olfactory pathway, odors are assumed to be represented in the MBs by specific sets of Kenyon cells (Heisenberg, 2003)....
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Journal Article•DOI•

Classical conditioning and retention in normal and mutant Drosophila melanogaster.

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Tim Tully¹, William G. Quinn¹•Institutions (1)

Princeton University¹

01 Sep 1985-Journal of Comparative Physiology A-neuroethology Sensory Neural and Behavioral Physiology

TL;DR: By changing the conditioned discrimination paradigm of Quinn et al. (1974) from an instrumental procedure to a classical (Pavlovian) one, strong learning in type flies is demonstrated and conditioned avoidance still was measurable at least three hours after training.

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Abstract: By changing the conditioned discrimination paradigm of Quinn et al. (1974) from an instrumental procedure to a classical (Pavlovian) one, we have demonstrated strong learning in type flies. About 150 flies were sequestered in a closed chamber and trained by explosing them sequentially to two odors in air currents. Flies received twelve electric shock pulses in the presence of the first odor (CS+) but not in the presence of the second odor (CS−). To test for conditioned avoidance responses, flies were transported to a Tmaze choice point, between converging currents of the two odors. Typically, 95% of trained flies avoided the shock-associated odor (CS+).

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1,112 citations

"Dopamine and Octopamine Differentia..." refers methods in this paper

...To make the comparison as stringent as possible, sugar reward learning (Tempel et al., 1983) was adapted to the apparatus of Tully and Quinn (1985), which originally was designed for aversive electric shock learning....
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...Pavlovian training procedures in a T-maze apparatus were applied according to the procedure of Tully and Quinn (1985)....
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Journal Article•DOI•

Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons.

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Toshihiro Kitamoto¹•Institutions (1)

Beckman Research Institute¹

01 May 2001-Journal of Neurobiology

TL;DR: These observations show that the GAL4/UAS system can be used to express shi(ts1) in a specific subset of neurons to cause temperature-dependent changes in behavior, and this method will be useful to study the functional significance of particular neuronal subsets in the behavior of intact animals.

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Abstract: Behavior is a manifestation of temporally and spatially defined neuronal activities. To understand how behavior is controlled by the nervous system, it is important to identify the neuronal substrates responsible for these activities, and to elucidate how they are integrated into a functional circuit. I introduce a novel and general method to conditionally perturb anatomically defined neurons in intact Drosophila. In this method, a temperature-sensitive allele of shibire (shi(ts1)) is overexpressed in neuronal subsets using the GAL4/UAS system. Because the shi gene product is essential for synaptic vesicle recycling, and shi(ts1) is semidominant, a simple temperature shift should lead to fast and reversible effects on synaptic transmission of shi(ts1) expressing neurons. When shi(ts1) expression was directed to cholinergic neurons, adult flies showed a dramatic response to the restrictive temperature, becoming motionless within 2 min at 30 degrees C. This temperature-induced paralysis was reversible. After being shifted back to the permissive temperature, they readily regained their activity and started to walk in 1 min. When shi(ts1) was expressed in photoreceptor cells, adults and larvae exhibited temperature-dependent blindness. These observations show that the GAL4/UAS system can be used to express shi(ts1) in a specific subset of neurons to cause temperature-dependent changes in behavior. Because this method allows perturbation of the neuronal activities rapidly and reversibly in a spatially and temporally restricted manner, it will be useful to study the functional significance of particular neuronal subsets in the behavior of intact animals.

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838 citations

"Dopamine and Octopamine Differentia..." refers background in this paper

...For temperaturedependent blockade of synaptic transmission, we used progeny of crosses between the homozygous parental lines UAS-shits1 (as virgin females) and the Gal4-lines 247-Gal4 (Zars et al., 2000b) and TH-Gal4 (FriggiGrelin et al., 2003) (as males)....
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...To test for the role of synaptic output from Kenyon cells in sugar memory, neurotransmitter release was blocked during either training or testing in 247-Gal4/UAS-shits1 flies....
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...In flies expressing the UAS-shits1 transgene either in the MBs (247-Gal4/UAS-shits1) or in the DA-positive cells (TH-Gal4/ UAS-shits1), the different temperatures used throughout the memory tests had no negative effect on the detection of relevant cues....
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...To block chemical synapses in these cells, the TH-Gal4 driver was combined with the UAS-shits1 effector gene above....
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...When trained at the restrictive and tested at the permissive temperature, TH-Gal4/UAS-shits1 flies showed very little electric shock memory, whereas control flies were not affected by this temperature regime (Fig....
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Journal Article•DOI•

Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli

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Jacques Mirenowicz¹, Wolfram Schultz¹•Institutions (1)

University of Fribourg¹

01 Feb 1996-Nature

TL;DR: Dopamine neurons preferentially report environmental stimuli with appetitive rather than aversive motivational value, and primary and conditioned non-noxious aversive stimuli either failed to activate dopamine neurons or induced weaker responses than appetitive stimuli.

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Abstract: Midbrain dopamine systems are crucially involved in motivational processes underlying the learning and execution of goal-directed behaviour. Dopamine neurons in monkeys are uniformly activated by unpredicted appetitive stimuli such as food and liquid rewards and conditioned, reward-predicting stimuli. By contrast, fully predicted stimuli are ineffective, and the omission of predicted reward depresses their activity. These characteristics follow associative-learning rules, suggesting that dopamine responses report an error in reward prediction. Accordingly, neural network models are efficiently trained using a dopamine-like reinforcement signal. However, it is unknown whether the responses to environmental stimuli concern specific motivational attributes or reflect more general stimulus salience. To resolve this, we have compared dopamine impulse responses to motivationally opposing appetitive and aversive stimuli. In contrast to appetitive events, primary and conditioned non-noxious aversive stimuli either failed to activate dopamine neurons or, in cases of close resemblance with appetitive stimuli, induced weaker responses than appetitive stimuli. Thus, dopamine neurons preferentially report environmental stimuli with appetitive rather than aversive motivational value.

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814 citations

"Dopamine and Octopamine Differentia..." refers background in this paper

...In the monkey, midbrain dopaminergic neurons have been described that carry the reinforcing properties of a US in appetitive but not aversive conditioning (Mirenowicz and Schultz, 1996)....
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