Layered reward signaling through octopamine and dopamine in Drosophila

By Christopher J. Burke, Wolf Huetteroth, D. Owald, E. Perisse, M. Krashes, Gaurav Das, Daryl M. Gohl, Marion Silies, Sarah J Certel, S. Waddell. 2012

552 citations recorded by the source corpus.

Dopamine is synonymous with reward and motivation in mammals. However, only recently has dopamine been linked to motivated behaviour and rewarding reinforcement in fruitflies. Instead, octopamine has historically been considered to be the signal for reward in insects. Here we show, using temporal control of neural function in Drosophila, that only short-term appetitive memory is reinforced by octopamine. Moreover, octopamine-dependent memory formation requires signalling through dopamine neurons. Part of the octopamine signal requires the α-adrenergic-like OAMB receptor in an identified subset of mushroom-body-targeted dopamine neurons. Octopamine triggers an increase in intracellular calcium in these dopamine neurons, and their direct activation can substitute for sugar to form appetitive memory, even in flies lacking octopamine. Analysis of the β-adrenergic-like OCTβ2R receptor reveals that octopamine-dependent reinforcement also requires an interaction with dopamine neurons that control appetitive motivation. These data indicate that sweet taste engages a distributed octopamine signal that reinforces memory through discrete subsets of mushroom-body-targeted dopamine neurons. In addition, they reconcile previous findings with octopamine and dopamine and suggest that reinforcement systems in flies are more similar to mammals than previously thought.

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, neutral): “…Blum et al., 2009; Krashes et al., 2009; Claridge-Chang et al., 2009; Aso et al., 2010; Sejourne et al., 2011; Trannoy et al., 2011; Liu et al., 2012; Burke et al., 2012; Aso et al., 2012; Placais et al., 2013; Pai et al., 2013, Aso et al., 2014b; Lin et al., 2014; Bouzaiane et al., 2015; Ichinose…”
Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “The mushroom body lobes are also richly innervated by dopaminergic neurons (DANs) thought to convey the contextual signals that impart meaning to an odor (Aso et al., 2012; Burke et al., 2012; Claridge-Chang et al., 2009; Liu et al., 2012; Mao and Davis, 2009; Waddell, 2013; Yamagata et al., 2015).”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, background): “…associative memory Recent studies of dopamine signaling have implicated distinct sites of memory formation within the MB lobes (summarized in Figure 1A) (Schroll et al., 2006; Claridge-Chang et al., 2009; Aso et al., 2010, 2012; Burke et al., 2012; Liu et al., 2012; Perisse et al., 2013).”
The neuronal architecture of the mushroom body provides a logic for associative learning (2014, methodology): “In classical learning paradigms, different DAN types respond to different unconditioned stimuli (US) (Riemensperger et al., 2005; Mao and Davis, 2009; Burke et al., 2012; Liu et al., 2012).”
Spaced Training Forms Complementary Long-Term Memories of Opposite Valence in Drosophila (2019, unknown): “3 provide reinforcement signals that modulate connections between MB Kenyon Cells (KCs) and MB output neurons (MBONs), whose dendrites occupy the same MB compartment (Claridge-Chang et al., 2009; Aso et al., 2010; Burke et al., 2012; Liu et al., 2012; Lin et al., 2014).”
Distinct dopamine neurons mediate reward signals for short- and long-term memories (2014, background): “The PAM cluster neurons have presynaptic terminals in the MB (18, 19).”
Pain-relief learning in flies, rats, and man: basic research and applied perspectives (2014, background): “distinct from those mediating punishment (Schwaerzel et al. 2003; Burke et al. 2012; Liu et al. 2012), such that distinct sets of Kenyon cell output synapses are likely to be modulated to accommodate conditioned approach.”
Different Kenyon Cell Populations Drive Learned Approach and Avoidance in Drosophila (2013, methodology): “Transgenic flies were raised commercially (BestGene).”
Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning (2019, background): “Aversive electric shock and sugar rewards evoke distributed patterns of activity across the DAN population (Burke et al., 2012; Cohn et al., 2015; Liu et al., 2012; Mao and Davis, 2009), implying that these naturalistic reinforcers likewise instruct coordinated bidirectional plasticity across differ”
Competing dopamine neurons drive oviposition choice for ethanol in Drosophila (2013, background): “Because innate olfactory preference for ethanol is octopamine-dependent, and a subset of octopaminergic neurons mediates PAM neuron activation required for appetitive memory, octopamine may play a role in the olfactory response (46, 47).”
Drosophila Learn Opposing Components of a Compound Food Stimulus (2014, background): “Since octopamine only provides shortterm sweet-taste reinforcement [9], we hypothesized that persistent nutrient-dependentmemorymust be independently formed in Tbh flies.”