Recent Advances in Neural Circuits for Taste Perception in Hunger

Abstract

Feeding is essential for survival and taste greatly influences our feeding behaviors. Palatable tastes such as sweet trigger feeding as a symbol of a calorie-rich diet containing sugar or proteins, while unpalatable tastes such as bitter terminate further consumption as a warning against ingestion of harmful substances. Therefore, taste is considered a criterion to distinguish whether food is edible. However, perception of taste is also modulated by physiological changes associated with internal states such as hunger or satiety. Empirically, during hunger state, humans find ordinary food more attractive and feel less aversion to food they usually dislike. Although functional magnetic resonance imaging studies performed in primates and in humans have indicated that some brain areas show state-dependent response to tastes, the mechanisms of how the brain senses tastes during different internal states are poorly understood. Recently, using newly developed molecular and genetic tools as well as in vivo imaging, researchers have identified many specific neuronal populations or neural circuits regulating feeding behaviors and taste perception process in the central nervous system. These studies could help us understand the interplay between homeostatic regulation of energy and taste perception to guide proper feeding behaviors.

Keywords: appetitive and consummatory behaviors; hunger; neural circuit; satiety; taste.

Figure 1

Neural regulation of taste perception in hunger state. AgRP neurons, which are firstly activated under hunger conditions, induce food seeking and consequent consummatory behaviors. (1) AgRP neurons inhibit the InsCtx via AgRP-PVT-BLA-InsCtx circuits to enhance the anticipatory response toward food cue in the appetitive feeding process. (2) After the start of eating, taste is detected by the tongue and perceived by the gustatory cortex (the InsCtx and the OFC) through rNTS, PBN, and VPMpc. (3) The InsCtx encodes the positive or negative valence of taste by interacting with the BLA or the central amygdala to continue or stop feeding. The OFC integrates taste and other sensory information as well as the reward value by projecting to the BLA. (4) Excitatory Vglut2-expressing neurons in the lateral hypothalamus also receives inhibitory inputs from AgRP neurons to induce feeding in hunger state. Vglut2 neurons in the LH project to the LS or to the LHb to modulate palatable or aversive taste preference, respectively. The aforementioned regions largely interact with the midbrain mesolimbic system to construct reward learning for the regulation of feeding behavior. BLA, the basolateral amygdala, CeA: the central nucleus of the amygdala, InsCtx: the insular cortex; LHb, the lateral habenula; LS, the lateral septum; VPMpc, the ventral posteromedial of the thalamus; OFC, the orbitofrontal cortex; PBN, the parabrachial nucleus; rNTS, the rostral part of the nucleus tractus solitarius.

Figure 2

The role of the internal state and taste in feeding. Hunger motivates animals to initiate food seeking and to promote the taste and reward value prediction in the appetitive feeding process. While palatable taste leads to food consumption, aversive taste mediates rejection. This process also contributes to the positive or negative reinforcement toward food. Hunger enhances the preference toward palatable taste while reducing the aversion toward aversive taste to promote consummatory feeding and also inhibits the termination of feeding until satiety.