The nucleus accumbens shell: a neural hub at the interface of homeostatic and hedonic feeding.

ABSTRACT

Feeding behavior is a complex physiological process regulated by the interplay between homeostatic and hedonic feeding circuits. Among the neural structures involved, the nucleus accumbens (NAc) has emerged as a pivotal region at the interface of these two circuits. The NAc comprises distinct subregions and in this review, we focus mainly on the NAc shell (NAcSh). Homeostatic feeding circuits, primarily found in the hypothalamus, ensure the organism's balance in energy and nutrient requirements. These circuits monitor peripheral signals, such as insulin, leptin, and ghrelin, and modulate satiety and hunger states. The NAcSh receives input from these homeostatic circuits, integrating information regarding the organism's metabolic needs. Conversely, so-called hedonic feeding circuits involve all other non-hunger and -satiety processes, i.e., the sensory information, associative learning, reward, motivation and pleasure associated with food consumption. The NAcSh is interconnected with hedonics-related structures like the ventral tegmental area and prefrontal cortex and plays a key role in encoding hedonic information related to palatable food seeking or consumption. In sum, the NAcSh acts as a crucial hub in feeding behavior, integrating signals from both homeostatic and hedonic circuits, to facilitate behavioral output via its downstream projections. Moreover, the NAcSh's involvement extends beyond simple integration, as it directly impacts actions related to food consumption. In this review, we first focus on delineating the inputs targeting the NAcSh; we then present NAcSh output projections to downstream structures. Finally we discuss how the NAcSh regulates feeding behavior and can be seen as a neural hub integrating homeostatic and hedonic feeding signals, via a functionally diverse set of projection neuron subpopulations.