Metaplastic neuronal state transition regulates species-specific interoceptive processing in Drosophila

Interoceptive processing, which involves the sensing and integration of internal physiological states, is fundamental to maintaining homeostasis. However, how species-specific interoceptive features arise from the underlying biophysical properties of neural circuit physiology remains unclear. We investigate the biophysical basis of species-specific interoception by examining protein-hunger dopamine neurons (DA-WED) in two Drosophila species with divergent dietary ecologies. We find that DA-WED neurons in D. melanogaster exhibit weak persistence of internal states, enabling flexible behavioral transitions during nutrient stress. In contrast, D. sechellia shows strong state persistence, locking neurons into a "preferred" configuration during protein deprivation. This divergence is supported by distinct intrinsic membrane properties, including protein deprivation-induced rebound spikes unique to D. sechellia. Analysis of synaptic dynamics and cardiomyocyte electrophysiology reveals species-specific physiological regulations coordinating central and peripheral systems. Behavioral assays confirm corresponding differences in protein consumption strategies, directly linking neural state geometry to ecologically relevant feeding behavior. Our findings establish metaplastic regulation of neural state transitions as a fundamental mechanism through which ecological specialization shapes interoceptive processing and brain-body coordination.