Homeostatic and non-homeostatic controls of feeding behavior: Distinct vs. common neural systems

Understanding the neurobiological controls of feeding behavior is critical in light of the growing obesity pandemic, a phenomenon largely based on excessive caloric consumption. Feeding behavior and its underlying biological substrates are frequently divided in the literature into two separate categories: [1] homeostatic processes involving energy intake based on caloric and other metabolic deficits, and [2] non-homeostatic processes that involve feeding driven by environmental and cognitive factors. The present review summarizes both historic and recent research examining the homeostatic regulation of feeding with specific emphasis on hypothalamic and hindbrain circuitry that monitor and regulate various metabolic signals. Regarding non-homeostatic controls, we highlight higher-order brain structures that integrate feeding-relevant external, interoceptive, and cognitive factors, including sensory cortical processing, learned associations in the hippocampus, and reward-based processing in the nucleus accumbens and interconnected mesolimbic circuitry. Finally, the current review focuses on recent evidence that challenges the traditional view that distinct neural systems regulate homeostatic vs. non-homeostatic controls of feeding behavior. Specifically, we highlight several feeding-related endocrine systems that act on both lower- and higher-order substrates, present evidence for the modulation of learned and cognitive feeding-relevant behaviors by lower-order brain regions, and highlight data showing that apparent homeostatic-based feeding behavior is modulated by higher-order brain regions. Our concluding perspective is that the classic dissociation between homeostatic and non-homeostatic constructs in relation to feeding behavior is limited with regards to understanding the complex integrated neurobiological systems that control energy balance.