A subset of broadly responsive Type III taste cells contribute to the detection of bitter, sweet and umami stimuli

Taste receptor cells use multiple signaling pathways to detect chemicals in potential food items. These cells are functionally grouped into different types: Type I cells act as support cells and have glial-like properties; Type II cells detect bitter, sweet, and umami taste stimuli; and Type III cells detect sour and salty stimuli. We have identified a new population of taste cells that are broadly tuned to multiple taste stimuli including bitter, sweet, sour, and umami. The goal of this study was to characterize these broadly responsive (BR) taste cells. We used an IP(3)R3-KO mouse (does not release calcium (Ca2+) from internal stores in Type II cells when stimulated with bitter, sweet, or umami stimuli) to characterize the BR cells without any potentially confounding input from Type II cells. Using live cell Ca(2+)imaging in isolated taste cells from the IP(3)R3-KO mouse, we found that BR cells are a subset of Type III cells that respond to sour stimuli but also use a PLC beta signaling pathway to respond to bitter, sweet, and umami stimuli. Unlike Type II cells, individual BR cells are broadly tuned and respond to multiple stimuli across different taste modalities. Live cell imaging in a PLC beta 3-KO mouse confirmed that BR cells use this signaling pathway to respond to bitter, sweet, and umami stimuli. Short term behavioral assays revealed that BR cells make significant contributions to taste driven behaviors and found that loss of either PLC beta 3 in BR cells or IP(3)R3 in Type II cells caused similar behavioral deficits to bitter, sweet, and umami stimuli. Analysis of c-Fos activity in the nucleus of the solitary tract (NTS) also demonstrated that functional Type II and BR cells are required for normal stimulus induced expression. Author summary We use our taste system to decide if we are going to consume or reject a potential food item. This is critical for survival, as we need energy to live but also need to avoid potentially toxic compounds. Therefore, it is important to understand how the taste cells in our mouth detect the chemicals in food and send a message to our brain. Signals from the taste cells form a code that conveys information about the nature of the potential food item to the brain. How this taste coding works is not well understood. Currently, it is thought that taste cells are primarily selective for each taste stimuli and only detect either bitter, sweet, sour, salt, or umami (amino acids) compounds. Our study describes a new population of taste cells that can detect multiple types of stimuli, including chemicals from different taste qualities. Thus, taste cells can be either selective or generally responsive to stimuli which is similar to the cells in the brain that process taste information. The presence of these broadly responsive taste cells provides new insight into how taste information is sent to the brain for processing.