Exploration and exploitation are flexibly balanced during local search in flies

Abstract

After finding food, a foraging animal must decide whether to continue feeding, or to explore the environment for potentially better options. One strategy to negotiate this tradeoff is to perform local searches around the food but repeatedly return to feed. We studied this behavior in flies and used genetic tools to uncover the underlying mechanisms. Over time, flies gradually expand their search, shifting from primarily exploiting food sources to exploring the environment, a change that is likely driven by increases in satiety. We found that flies search patterns preserve these dynamics even as the overall scale of the search is modulated by starvation-induced changes in metabolic state. In contrast, search induced by optogenetic activation of sugar sensing neurons does not show these dynamics. We asked what navigational strategies underlie local search. Using a generative model, we found that a change in locomotor pattern after food consumption could account for repeated returns to the food, but failed to capture relatively direct, long return trajectories. Alternative strategies, such as path integration or sensory taxis could allow flies to return from larger distances. We tested this by individually silencing the flys head direction system, olfaction and hygrosensation, and found that the only substantial effect was from perturbing hygrosensation, which reduced the number of long exploratory trips. Our study illustrates that local search is composed of multiple behavioral features that evolve over time based on both internal and external factors, providing a path towards uncovering the underlying neural mechanisms.