Taste in chimpanzees. III: Labeled-line coding in sweet taste

Abstract

In peripheral taste the coding mechanism remains an enigma. Among coding theories the "across-fiber pattern" argues that activity across fibers codes for taste, whereas the "labeled line" claims that activity in a particular set of fibers underlies a taste quality. We showed previously that chimpanzee chorda tympani taste fibers grouped according to human taste qualities into an S-cluster, responding predominantly to sweet stimuli, a Q-cluster, sensitive to bitter tastants, and an N-cluster, stimulated by salts. The analysis showed that information in the S-line suffices to distinguish stimuli of one taste quality from the others. However, one condition for the labeled line remained: that blockage of activity in a particular line must cause blockage of one taste quality, but of no other, or its onset give rise to the sensation of a taste quality. Here we studied this requirement with gymnemic acids and miraculin. In humans and chimpanzees, gymnemic acids suppress the sweet taste of all sweeteners whereas miraculin adds a sweet taste quality to sour stimuli. Gymnemic acids also abolish miraculin-induced sweet taste. We found that gymnemic acids practically abolished the response to every sweetener in the chimpanzee S-cluster. Equally important, they had no effect on the responses of the Q- and N-clusters. After miraculin, the S-cluster fibers responded to acids as well as to sweeteners, although they had not responded to acids before miraculin. Gymnemic acids abolished this miraculin-induced response to acids and responses to sweeteners in the S-fibers. These results link the sweet taste quality to activity in fibers of the S-cluster. Thus the S-cluster fibers satisfy the definition of the labeled-line theory: "that activity in a particular fiber type represents a specific taste quality."