Drosophila Learn Opposing Components of a Compound Food Stimulus

By Gaurav Das, M. Klappenbach, Eleftheria Vrontou, E. Perisse, Christopher M. Clark, Christopher J. Burke, S. Waddell. 2014

98 citations recorded by the source corpus.

Summary Dopaminergic neurons provide value signals in mammals and insects [1–3]. 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]. However, it is not known how flies evaluate substances that have mixed valence. Here we show that flies form short-lived aversive olfactory memories when trained with odors and sugars that are contaminated with the common insect repellent DEET. This DEET-aversive learning required the MB-MP1 dopaminergic neurons that are also required for shock learning [7]. Moreover, differential conditioning with DEET versus shock suggests that formation of these distinct aversive olfactory memories relies on a common negatively reinforcing dopaminergic mechanism. Surprisingly, as time passed after training, the behavior of DEET-sugar-trained flies reversed from conditioned odor avoidance into odor approach. In addition, flies that were compromised for reward learning exhibited a more robust and longer-lived aversive-DEET memory. These data demonstrate that flies independently process the DEET and sugar components to form parallel aversive and appetitive olfactory memories, with distinct kinetics, that compete to guide learned behavior.

Subfields: Cellular and Molecular Neuroscience, Genetics, Insect Science

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “Punitive or rewarding stimuli such as electric shock, heat, cold, bitter taste and sugar generally activate a complex pattern of DANs (Riemensperger et al., 2005; Mao and Davis, 2009; ; Liu et al., 2012; Tomchik, 2013; Galili et al., 2014; Das et al., 2014; Kirkhart and Scott, 2015).”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, background): “This DAN also mediates aversive reinforcement of bitter taste (Das et al., 2014).”
The neuronal architecture of the mushroom body provides a logic for associative learning (2014, background): “Different populations of DANs are activated by USs of different valence; see Figure 1A of the accompanying paper (Aso et al., 2014) for summary (Riemensperger et al., 2005; Mao and Davis, 2009; Liu et al., 2012; Das et al., 2014).”
The Drosophila Mushroom Body: From Architecture to Algorithm in a Learning Circuit. (2020, background): “This novelty-assessing module has interesting parallels with Bloomfilters, data structures used in computer science that efficiently store and allow lookup for previously encountered patterns (Dasgupta et al. 2018).”
Reward signal in a recurrent circuit drives appetitive long-term memory formation (2015, unknown): “Interestingly, the induced LTM is undetectable immediately after conditioning but gradually develops with time (Das et al., 2014; Huetteroth et al., 2015; Yamagata et al., 2015).”
A connectome of a learning and memory center in the adult Drosophila brain (2017, background): “…coordination of parallel memory modules The organization of the MB into a set of compartments arranged in series along the KC axons is well suited for simultaneously storing multiple independent memories of a given sensory stimulus (Das et al., 2014; Kaun et al., 2011; Aso and Rubin, 2016).”
Spaced Training Forms Complementary Long-Term Memories of Opposite Valence in Drosophila (2019, unknown): “In contrast, flies simultaneously form parallel competing memories when trained with bitter tainted sugar and their performance switches from aversion to approach over time, as dictated by the superior persistence of the nutrient-dependent sugar memory (Das et al., 2014).”
Distinct dopamine neurons mediate reward signals for short- and long-term memories (2014, background): “1 H and I), similar to appetitive memory without a short-term component of mutants for TβH (36).”
Sweet Taste and Nutrient Value Subdivide Rewarding Dopaminergic Neurons in Drosophila (2015, background): “Nutrient-dependent LTM does not involve octopamine [4, 10] or sweet-taste-reinforcing dopaminergic neurons.”
Gustatory Learning and Processing in the Drosophila Mushroom Bodies (2015, background): “Previous studies of PPL1 neurons showed that they are necessary for shock-induced olfactory aversive conditioning and that they respond to temperature decreases (Tomchik, 2013) and the chemical repellent DEET (Das et al., 2014), suggesting that PPL1 encodes multiple types of aversive US.”