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Thermosensation is critical for the survival of animals. However, mechanisms through which nutritional status modulates thermosensation remain unclear. Herein, we showed that hungry Drosophila exhibit a strong hot avoidance behavior (HAB) compared to food-sated flies. We identified that hot stimulus increases the activity of α′β′ mushroom body neurons (MBns), with weak activity in the sated state and strong activity in the hungry state. Furthermore, we showed that α′β′ MBn receives the same level of hot input from the mALT projection neurons via cholinergic transmission in sated and hungry states. Differences in α′β′ MBn activity between food-sated and hungry flies following heat stimuli are regulated by distinct Drosophila insulin-like peptides (Dilps). Dilp2 is secreted by insulin-producing cells (IPCs) and regulates HAB during satiety, whereas Dilp6 is secreted by the fat body and regulates HAB during the hungry state. We observed that Dilp2 induces PI3K/AKT signaling, whereas Dilp6 induces Ras/ERK signaling in α′β′ MBn to regulate HAB in different feeding conditions. Finally, we showed that the 2 α′β′-related MB output neurons (MBONs), MBON-α′3 and MBON-β′1, are necessary for the output of integrated hot avoidance information from α′β′ MBn. Our results demonstrate the presence of dual insulin modulation pathways in α′β′ MBn, which are important for suitable behavioral responses in Drosophila during thermoregulation under different feeding states.

Thirst and hunger are fundamental survival drives that modulate various aspects of animal behavior through specific neural circuits. Previous studies have demonstrated that dopaminergic neurons (DANs) innervating the mushroom body (MB) in the Drosophila brain play essential roles in innate and learned thirst- and hunger-dependent behaviors, with most experiments focusing on acute water or food deprivation. However, it is unclear whether acute water or food deprivation alters dopamine production and neural activity in MB-innervating DANs. We genetically expressed green fluorescent protein (GFP) in MB-innervating DANs using broadly and specifically labeled GAL4 lines under satiety, thirst, and hunger states. The brains were immunostained with anti-tyrosine hydroxylase (TH) to assess dopamine biosynthesis. Additionally, the transcriptional reporter of intracellular Ca (TRIC) was expressed in these DANs using the same GAL4 lines to monitor neural activity under different internal states. Normalized anti-TH and TRIC signals in specific MB compartments were compared between the satiety and thirst groups and between the satiety and hunger groups using unpaired two-tailed t-tests. Neither TH levels nor neural activity in the 13 subtypes of MB-innervating DANs exhibited significant differences during the satiety, thirst, and hunger conditions. This study suggests that 16-hour water deprivation or 24-hour food deprivation does not significantly alter dopamine production and neural activity in MB-innervating DANs. These findings offer insights into the independence of baseline dopaminergic activity from internal states in thirst- or hunger-related behaviors.