Taste Bud Connectome: Implications for Taste Information Processing

Abstract

Taste buds contain 3 types of morphologically identifiable mature cells, 2 of which mediate transduction of specific taste qualities: Type III cells transduce sour while Type II cells transduce either sweet, bitter or umami. A long-standing controversy is whether the nerve fibers innervating these cells are wired specifically, in a labeled-line fashion, or non-specifically, leading to broad responsiveness across taste qualities, the so-called across-fiber system of encoding. Using serial blockface scanning electron microscopy through 5 circumvallate mouse taste buds, we reconstructed the patterns of connectivity of nerve fibers as well as the degree of potential interaction between the two types of taste transducing cells. Type II and Type III cells share few points of contact with one another, and display no morphologically identifiable synapses, suggesting limited direct interaction between these cell types. Of the 127 nerve fibers that make synaptic contacts with taste cells in the sampling volume, about 70% (n=91) synapse with only one taste cell. Of the remaining 36 fibers, 4 synapse with both Type II and Type III cells, the remainder synapsing exclusively with multiple Type II taste cells or multiple Type III cells. Since Type II and Type III cells transduce different taste qualities, the few mixed fibers do not follow a labeled-line organization according to taste quality information and show that connectional specificity in taste buds is not absolute. Significance StatementTaste buds, the sensory end organs for the sense of taste, contain multiple types of sensory cells, with each responding to one of the primary tastes: salt, sweet, sour, bitter and umami. A long-standing question is whether each type of taste cell is wired specifically to a unique set of nerve fibers conveying a "labeled-line" message to the brain. Using serial sections, we determined the neural connectivity in mouse circumvallate taste buds. The majority of individual nerve fibers connect to a single type of taste cell, but 3.1% of the fibers branch to receive input from taste cells known to have different specificities. Thus taste cannot entirely be carried along nerve fibers dedicated to single taste qualities.