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The Journal of Neuroscience, October 3, 2007, 27(40):10840-10848; doi:10.1523/JNEUROSCI.1863-07.2007

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Cellular/Molecular
Breadth of Tuning and Taste Coding in Mammalian Taste Buds

Seth M. Tomchik,¹ Stephanie Berg,¹ Joung Woul Kim,¹ Nirupa Chaudhari,^1,2 and Stephen D. Roper^1,2

¹Department of Physiology and Biophysics and ²Program in Neurosciences, University of Miami Miller School of Medicine, Miami, Florida 33136

Correspondence should be addressed to Dr. Stephen D. Roper, Department of Physiology and Biophysics (4065 Rosenstiel Medical Science Building), University of Miami Miller School of Medicine, 1600 N.W. 10th Avenue, Miami, FL 33136. Email: sroper{at}med.miami.edu

A longstanding question in taste research concerns taste coding and, in particular, how broadly are individual taste bud cells tuned to taste qualities (sweet, bitter, umami, salty, and sour). Taste bud cells express G-protein-coupled receptors for sweet, bitter, or umami tastes but not in combination. However, responses to multiple taste qualities have been recorded in individual taste cells. We and others have shown previously there are two classes of taste bud cells directly involved in gustatory signaling: "receptor" (type II) cells that detect and transduce sweet, bitter, and umami compounds, and "presynaptic" (type III) cells. We hypothesize that receptor cells transmit their signals to presynaptic cells. This communication between taste cells could represent a potential convergence of taste information in the taste bud, resulting in taste cells that would respond broadly to multiple taste stimuli. We tested this hypothesis using calcium imaging in a lingual slice preparation. Here, we show that receptor cells are indeed narrowly tuned: 82% responded to only one taste stimulus. In contrast, presynaptic cells are broadly tuned: 83% responded to two or more different taste qualities. Receptor cells responded to bitter, sweet, or umami stimuli but rarely to sour or salty stimuli. Presynaptic cells responded to all taste qualities, including sour and salty. These data further elaborate functional differences between receptor cells and presynaptic cells, provide strong evidence for communication within the taste bud, and resolve the paradox of broad taste cell tuning despite mutually exclusive receptor expression.

Key words: taste bud; cell type; taste processing; presynaptic cell; receptor cell; coding

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Received April 24, 2007; revised Aug. 5, 2007; accepted Aug. 8, 2007.

Correspondence should be addressed to Dr. Stephen D. Roper, Department of Physiology and Biophysics (4065 Rosenstiel Medical Science Building), University of Miami Miller School of Medicine, 1600 N.W. 10th Avenue, Miami, FL 33136. Email: sroper{at}med.miami.edu

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