Distinct internal states interact to shape food choice by modulating sensorimotor processing at global and local scales

Abstract

When deciding what to eat, animals evaluate sensory information about food quality alongside multiple ongoing internal states. How internal states interact to alter sensorimotor processing and shape decisions such as food choice remains poorly understood. Here, we use pan-neuronal volumetric activity imaging in the Drosophila brain to investigate the neuronal basis of internal state dependent nutrient appetites. We created a functional atlas of the ventral fly brain and find that metabolic state shapes sensorimotor processing across large sections of the neuropil. Reproductive state, in contrast, acts locally to define how sensory information is translated into feeding motor output. Thereby, these two states synergistically modulate protein-specific food intake and thus food choice. Finally, using a novel computational strategy, we identify driver lines innervating state-modulated regions and show that the newly identified borboleta region is sufficient to direct food choice towards protein-rich food. We therefore identify a generalizable principle by which distinct internal states are integrated to shape decision-making and propose a strategy to uncover and functionally validate how internal states shape behavior.