Identification of conserved circuit logic in temperature navigation behavior in fish and fly

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Temperature affects the physiological processes of all organisms. A failure to assess its value, valence, and rate of change can have a variety of consequences from tissue damage to failure of the entire system. Thus, most organisms have evolved strategies to maintain their body temperature within a specific narrow range. Regardless of the specific strategy adopted, the nervous system plays an important role in detecting temperature changes, evaluating them in the current context and state of the animal, and directing both physiological and behavioral changes. The evolutionary relationship between the function of the nervous system in temperature regulation between different species remains unclear. Through the work of a PhD student funded by the previous funding period of this SPP, we have significantly advanced our understanding of the role of the nervous system in temperature homeostasis in ectotherms as compared to endotherms. Through novel behavioral assays, we have found that fish and flies use highly similar strategies to navigate temperature gradients to remain in or return to a preferred temperature range (‘homeostatic navigation’). We further showed that fish achieve thermoregulation through a neural network connecting the preoptic area of the hypothalamus (PoA) to brain areas enabling spatial navigation. PoA drives reorientation when thermal conditions are worsening and conveys this information for instructing future motor actions to the navigation-controlling habenula (Hb) - interpeduncular nucleus (IPN) circuit. These results suggest a conserved function of the PoA in thermoregulation acting through species- specific neural networks. Furthermore, we propose that homeostatic navigation arose from an ancient chemotaxis navigation circuit that was subsequently extended to serve in other sensory modalities. In the next funding period, we want to (i) identify the functional equivalents of the PoA and the Hb in the fly by combining state-of-the-art in vivo imaging and optogenetic manipulation during homeostatic navigation, (ii) characterize the role of serotonergic signaling in homeostatic navigation in fish and fly (feedback and feedforward modulation), and (iii) address the role of homeostatic setpoints in triggering temperature navigation by changing the temperature setpoint of fish and flies though developmental temperature, exogenous pyrogens, and hunger states. Finally, we will use these new data to update and refine the general and species-specific contribution of neuron types and circuit motives in a computational circuit model. Together the expected results will show how joint homeostatic needs are processed by functionally equivalent brain regions or neurons and which role the homeostatic setpoint plays in triggering behavior to improve survival chances of evolutionary distinct species.