Ultrastructure of mouse vallate taste buds: III. Patterns of synaptic connectivity.

Abstract

We have used serial high voltage electron micrographs and computer-generated, three-dimensional reconstructions to study morphological relationships and patterns of synaptic connectivity in taste buds from the circumvallate papillae of the mouse. The intragemmal arborizations of 40 sensory nerve fibers were examined from 7 taste buds that were sectioned serially. We identified the synaptic connections from taste cells onto the reconstructed nerve fibers and classified the presynaptic taste cells based on previously established ultrastructural criteria. From these data we were able to extract the following information for the reconstructed nerve fibers: (1) the morphology of intragemmal nerve fibers and their arborizations within the taste bud, (2) the total number of synaptic connections from taste bud cells onto the nerve fibers, and (3) the taste cell types associated with each of the synapses. Fifty-six synapses were studied. Synapses were often found to be located at either the branch points or terminations of nerve fiber processes. The maximum number of taste cells observed to synapse onto a single nerve fiber was 5. Several nerve fibers had no apparent synapses. Dark cells (type I), intermediate cells, and light cells (type II) all formed synaptic connections with sensory nerve fibers. In no cases did dark cells and light cells synapse onto the same sensory nerve fiber. Our observation that any given nerve fiber receives its synaptic input from morphologically similar taste cells provides evidence for specificity in taste bud synaptic connections. We speculate that the observed pattern of synaptic connections is related to taste bud function. Since all of the synapses onto a given nerve fiber are from morphologically similar taste cells, we postulate that there is a correlation between taste cell morphology and sensory responsiveness. Intracellular electrophysiological studies on taste cells, in which responses to focally applied chemical stimuli are followed by characterization of the ultrastructural features of the same taste cells, will prove or disprove this hypothesis.