Functional Organization Of Chemical Senses: Central Neural Processing

The sense of taste regulates feeding behavior and guides in the selection of food. Humans perceive 5 basic tastes: sweet, umami (savory taste or amino acids), bitter, sour, and salty, although other taste modalities may be added, including CO2. Taste reception is orchestrated by distinct populations of selectively tuned cells clustered to form taste buds in the tongue, mouth, and gastrointestinal tract, which express specific receptors for different gustatory stimuli. Sweet, umami, and bitter are detected by 2 distinct families of G-protein–coupled receptors. By contrast, sour and salty are sensed by ion channels. The polycystic kidney disease channel has been proposed as the acid-sensing machinery detecting the sour taste. CO2 is also detected by sour-sensing cells; however, the taste of carbonation is separated from sour detection. Thus,CO2 taste machinery does not perceive sour taste despite being detected by the same cells. Even though different tastes act on different sets of taste cells, there is significant cell–cell communication within taste buds. Despite a growing literature on the peripheral mechanisms for taste, knowledge of the central neural processing of taste is still largely incomplete. In this study, we investigated the cortical representation of taste-related neural responses, the neural mechanisms underlying the perception of taste and the chemotopic organization of taste modalities in the human primary taste cortex (insula). Furthermore, we studied the interference between perceptual mechanisms of different tastants, and in particular the effect of CO2 on the brain processing of sweet stimuli, analyzing its differential effect on sucrose and artificial sweeteners. We used an experimental setting with Magnetic Resonance echo planar blood oxygenation-level-dependent experiments, while gustatory stimuli were delivered by computer controlled automatic injectors. We found a detailed chemotopic representation in the human insula where each taste, including CO2, that could be considered a sixth taste, has its own cortical representation. Our study demonstrated that the interference between different tastants can act as a powerful modulator of the perceptual processes of taste. The presence of CO2 produced a strong overall decrease in the neural processing of sweetness-related signals, while reducing the neural processing of sucrose more than artificial sweeteners. The analysis of the functional organization of the insular cortex unveiled essential steps allowing the perception of taste and regulating feeding and dietary behaviors.