Sour Sensing from the Tongue to the Brain

• Published in: Cell Vol. 179; no. 2; pp. 392 - 402.e15
• Main Authors: Zhang, Jin, Jin, Hao, Zhang, Wenyi, Ding, Cheng, O’Keeffe, Sean, Ye, Mingyu, Zuker, Charles S.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 03.10.2019
• Subjects: Acids - pharmacology; Afferent Pathways - cytology; Afferent Pathways - metabolism; Afferent Pathways - physiology; Animals; brain; Brain - cytology; Brain - metabolism; Brain - physiology; brain circuits; Female; fermentation; ganglia; gravity; innate behaviors; ion channels; Male; Membrane Proteins - genetics; Membrane Proteins - metabolism; Mice; Mice, Inbred C57BL; otopetrin; sensory coding; sour; sourness; Taste; Taste Buds - drug effects; Taste Buds - metabolism; Taste Buds - physiology; Taste Perception; taste receptors; tongue; brain circuits; sour; sensory coding; innate behaviors; otopetrin; taste
• ISSN: 0092-8674; 1097-4172; 1097-4172
• DOI: 10.1016/j.cell.2019.08.031

The ability to sense sour provides an important sensory signal to prevent the ingestion of unripe, spoiled, or fermented foods. Taste and somatosensory receptors in the oral cavity trigger aversive behaviors in response to acid stimuli. Here, we show that the ion channel Otopetrin-1, a proton-selective channel normally involved in the sensation of gravity in the vestibular system, is essential for sour sensing in the taste system. We demonstrate that knockout of Otop1 eliminates acid responses from sour-sensing taste receptor cells (TRCs). In addition, we show that mice engineered to express otopetrin-1 in sweet TRCs have sweet cells that also respond to sour stimuli. Next, we genetically identified the taste ganglion neurons mediating each of the five basic taste qualities and demonstrate that sour taste uses its own dedicated labeled line from TRCs in the tongue to finely tuned taste neurons in the brain to trigger aversive behaviors. [Display omitted] •OTOP1 is the mammalian sour taste receptor•Expression of OTOP1 in sweet taste cells allows them to respond to sour stimuli•Neurons mediating the five basic tastes (sweet, bitter, salty, umami, and sour) are genetically distinct from each other•The circuit mediating responses to sour is hardwired to evoke behavioral aversion to acid stimuli The detection of sour is mediated by the Otop1 proton channel present in sour-sensing taste receptor cells. These taste cells are selectively wired to dedicated neurons and brain circuits triggering innately aversive reactions to acid stimuli.