Neural correlates of water reward in thirsty Drosophila

By Suewei Lin, D. Owald, Vikram Chandra, Clifford B. Talbot, Wolf Huetteroth, S. Waddell. 2014

206 citations recorded by the source corpus.

Drinking water is innately rewarding to thirsty animals. In addition, the consumed value can be assigned to behavioral actions and predictive sensory cues by associative learning. Here we show that thirst converts water avoidance into water-seeking in naive Drosophila melanogaster. Thirst also permitted flies to learn olfactory cues paired with water reward. Water learning required water taste and <40 water-responsive dopaminergic neurons that innervate a restricted zone of the mushroom body γ lobe. These water learning neurons are different from those that are critical for conveying the reinforcing effects of sugar. Naive water-seeking behavior in thirsty flies did not require water taste but relied on another subset of water-responsive dopaminergic neurons that target the mushroom body β′ lobe. Furthermore, these naive water-approach neurons were not required for learned water-seeking. Our results therefore demonstrate that naive water-seeking, learned water-seeking and water learning use separable neural circuitry in the brain of thirsty flies.

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): “A large body of previous work has established that the KCs, MBONs and DANs innervating individual compartments are differentially involved in forming memories with different valence—that is, appetitive and aversive memories—and with different stabilities (Schwaerzel et al., 2003; Zars et al., 2000; ”
Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “Metabolic states, such as thirst and hunger, have been shown to gate appetitive reinforcement by water and sugar rewards (Burke et al., 2012; Huetteroth et al., 2015; Lin et al., 2014), permitting state-dependent formation of olfactory associations only in motivated animals.”
Distinct dopamine neurons mediate reward signals for short- and long-term memories (2014, background): “It would be interesting to compare neuronal representations of different rewarding stimuli, such as ethanol (51) and water (41, 52).”
Spaced Training Forms Complementary Long-Term Memories of Opposite Valence in Drosophila (2019, unknown): “, 2012), water (Lin et al., 2014; Shyu et al., 2017) and alcohol reward (Scaplen et al.”
Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila (2015, unknown): “This matches well with the picture developed from recent behavioral studies indicating the different compartments are related to distinct motivational drives (Burke et al., 2012; Huetteroth et al., 2015; Krashes et al., 2009; Lin et al., 2014b; Liu et al., 2012; Musso et al., 2015; Yamagata et al., ”
Dissecting neural pathways for forgetting in Drosophila olfactory aversive memory (2015, methodology): “This suggests that NP2397 labeled multiple subsets of PAM-DANs, which included but were not limited to PAM-β′1.”
Do the right thing: neural network mechanisms of memory formation, expression and update in Drosophila (2018, background): “For example, a memory of a water reward is preferentially expressed when flies are thirsty, but not hungry, while a previously sugarassociated cue is approached when flies are hungry, but not thirsty [55].”
Sweet Taste and Nutrient Value Subdivide Rewarding Dopaminergic Neurons in Drosophila (2015, methodology): “Our initial examination of oambP-GAL4 revealed expression in approximately 55 rewarding dopaminergic neurons (and w12 tyrosine hydroxylase (TH)-negative neurons) in the protocerebral anterior medial (PAM) cell cluster that innervate the horizontal mushroom body lobes (Figures 1C–1E, S1A, S1C, and S1”
A Higher Brain Circuit for Immediate Integration of Conflicting Sensory Information in Drosophila. (2015, result): “Independent support for a role of this MB region in modulation of innate behaviors comes from a study showing that blocking of b02 PAM cluster neurons converted the innate behavior of naive thirsty flies from water preference into water avoidance [34].”
Neuronal mechanisms underlying innate and learned olfactory processing in Drosophila. (2019, background): “caloric value of food) that entrain memories of 241 different stability [64-66,68].”
Postsynaptic plasticity of cholinergic synapses underlies the induction and expression of appetitive and familiarity memories in Drosophila (2022, background): “In vertebrates, typically, postsynaptic long- term changes (Korte and Schmitz, 2016; Kandel et al., 2014; Lüscher and Malenka, 2011) are mediated via NMDA- sensitive glutamate receptors (NMDAR) that induce (‘induction’; Nicoll, 2017) an expression phase (‘expression’; Nicoll, 2017) through changed…”
Activity of Defined Mushroom Body Output Neurons Underlies Learned Olfactory Behavior in Drosophila (2015, background): “One half of GRASP is driven by R48B04LexA (Figure S1A) (Lin et al., 2014) and the other by VT1211-GAL4.”