To accommodate complex and changing environmental conditions, animals have evolved mechanisms to modify behaviors that maximize survival. Behavior can be modified by prior experiences that alter internal states such as hunger and external cues such as food signals. Despite the importance of this ability to evaluate and respond to environmental changes, it remains incompletely understood how animals accomplish this essential task. Using the Caenorhabditis elegans model system, the goal of this dissertation is to reveal mechanisms that allow animals to interpret the world around them and respond appropriately. Advantages of using C. elegans include a simple body plan with a total of only 959 somatic cells, a complete nervous system wiring diagram and robust behavior readouts. Combining these advantages with powerful genetics and molecular manipulations, my dissertation presents mechanistic insight into how the nervous system generates flexible behaviors.

Chapter 1 introduces effects of environmental changes on neural circuits and how neuropeptides play an important role in linking food conditions with animal behavior responses. Insulin-like signaling is presented as an example of how conserved molecules play critical roles in modifying the nervous system. In Chapters 2 and 3, I use acute food experience paradigms to probe how prior experience modifies the nervous system resulting in altered animal behavior. Using acute food deprivation in Chapter 2, I show that internal state changes specifically and reversibly modify C.elegans behavioral responses to repellent signals. Lack of food status is sensed and relayed through multiple tissues using neuropeptides to modify downstream ASI chemosensory neurons altering repellent sensitivity. In Chapter 3, I show that transiently altering diet by changing food source modifies C. elegans behavioral responses to attractive signals. I also find that neuropeptide signals are used to relay diet changes modifying food-seeking behavior. In summary, my research links dietary changes with neuropeptide signals from multiple tissues modifying behaviors. Together, I have identified a role for neuropeptides and conserved signaling pathways in relaying changes in internal and external states. In sum, this dissertation unravels how prior experiences involving food signals modify the nervous system allowing animals to generate adaptive and appropriate behaviors.