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

By Martin Schwaerzel, M. Monastirioti, Henrike Scholz, Florence Friggi-Grelin, S. Birman, Martin Heisenberg. 2003

893 citations recorded by the source corpus.

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.

Subfields: Cellular and Molecular Neuroscience, Ecology, Evolution, Behavior and Systematics, Genetics

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “DOI: 10.7554/eLife.16135.001”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, methodology): “…encoded by the rutabaga gene, are required specifically in the KCs for memory formation (Livingstone et al., 1984; Zars et al., 2000; Schwaerzel et al., 2003; Kim et al., 2007; McGuire et al., 2003; Gervasi et al., 2010; Qin et al., 2012) and rutabaga was shown to be required for…”
The neuronal architecture of the mushroom body provides a logic for associative learning (2014, methodology): “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…”
Dopamine Is Required for Learning and Forgetting in Drosophila (2012, neutral): “, 2005), addiction (Lüscher and Malenka, 2011), and learning (Schwaerzel et al., 2003; Claridge-Chang et al., 2009; Wise, 2004).”
WRITING MEMORIES WITH LIGHT-ADDRESSABLE REINFORCEMENT CIRCUITRY (2009, background): “The high efficacy of dopaminergic instruction, combined with the absence of short-term memory when dopaminergic synapses are blocked during training (Schwaerzel et al., 2003), argues that signaling from dopaminergic neurons is the primary means by which aversive odor associations are stored.”
Event Timing in Associative Learning: From Biochemical Reaction Dynamics to Behavioural Observations (2012, background): “In the Drosophila brain, individual odours activate small, specific groups of Kenyon cells increasing their intracellular Ca concentration [22–24]; whereas shock induces a dopaminergic reinforcement signal, which is also delivered to the Kenyon cells [25–29].”
Dynamics of learning-related cAMP signaling and stimulus integration in the Drosophila olfactory pathway. (2009, neutral): “They also may receive information about punishment and reward via dopaminergic and octopaminergic interneurons, respectively (Han et al., 1996, 1998; Schwaerzel et al., 2003; Schroll et al., 2006).”
Activity of Defined Mushroom Body Output Neurons Underlies Learned Olfactory Behavior in Drosophila (2015, background): “Value can be assigned to these odor representations during learning by the action of reinforcing dopaminergic neuronswhose presynaptic terminals are confined to discrete zones along the lobes of the MB (Schwaerzel et al., 2003; Riemensperger et al., 2005; Claridge-Chang et al., 2009; Aso et al., 201”
γ neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila (2012, neutral): “MBs integrate olfactory conditioned stimulus (CS) inputs with neuromodulatory reinforcement (unconditioned stimuli, US) [1, 2], which for aversive learning is thought to rely on dopaminergic (DA) signaling [3–6] to DopR, a D1-like dopamine receptor expressed in MBs [7, 8].”
Drosophila Learn Opposing Components of a Compound Food Stimulus (2014, background): “During Drosophila olfactory learning, distinct subsets of dopaminergic neurons appear to assign either positive or negative value to odor representations in mushroom body neurons [4–9].”
Reward signal in a recurrent circuit drives appetitive long-term memory formation (2015, neutral): “…reward signals are conveyed by PAM cluster neurons to a brain structure called mushroom body (MB), where the convergence of the reward and the odor is assumed to take place (Schwaerzel et al., 2003; Krashes et al., 2007; Trannoy et al., 2011; Cervantes-Sandoval et al., 2013; Huang et al., 2013).”
Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila (2015, neutral): “…al., 2014; Tomchik and Davis, 2009; Wang et al., 2008; Yu et al., 2006, but see Zhang and Roman, 2013), signals in MBONs decrease in some cases (Owald et al., 2015; Séjourné et al., 2011) and increase in others (Bouzaiane et al., 2015; Owald et al., 2015; Pai et al., 2013; Plaçais et al., 2013).”
Rapid Consolidation to a radish and Protein Synthesis-Dependent Long-Term Memory after Single-Session Appetitive Olfactory Conditioning in Drosophila (2008, background): “MB neurons are required during and after training to acquire and stabilize memory (Krashes et al., 2007), whereas MB neuron output is only required to retrieve the memory (Dubnau et al., 2001; McGuire et al., 2001; Schwaerzel et al., 2003; Krashes et al., 2007).”
Olfactory memory formation in Drosophila: from molecular to systems neuroscience. (2005, methodology): “Another recently introduced variation of this assay is the replacement of the electric shock US with an appetitive US: sucrose for a hungry fly (Schwaerzel et al. 2003).”