Synaptic Connections in Developing and Adult Rat Taste Buds

Abstract

Synaptic connections in rat taste buds closely resemble synapses found in the CNS. Taste bud synapses are characterized by parallel, apposed, thickened membranes that are separated by a cleft ranging from 16 to 30 nm. The putative synaptic vesicles are of two types: small, clear vesicles (40–70 nm) and large, dense-cored vesicles (90–120 nm). The small, clear vesicles predominate at most synapses. Most taste bud synapses fall into two structural types: small, macular synapses and ‘finger-like’ synapses (Kinnamon et al., 1985). The finger-like synapses are characterized by a rod-like postsynaptic process that protrudes into an invagination of the presynaptic taste cell. Virtually all adult synapses are afferent, from the gustatory receptor cell onto a process of a cranial nerve. It has been proposed, however, that subsurface cisternae of smooth endoplasmic reticulum located at the close appositions between taste cells and nerve processes may participate in efferent modulation of the taste cell (Ide and Munger, 1980; Clapp et al., 2004). Synapses in developing taste buds are more varied, including afferent, efferent, and neuroneuronal synapses. Most synapses in the CNS utilize a variety of proteins to translocate synaptic vesicles to the active zone of the presynaptic membrane, dock the vesicle, cause fusion of the vesicle membrane with the presynaptic membrane, and bring about exocytosis of the vesicle contents into the synaptic cleft. We are currently studying four synaptic proteins: SNAP-25, synaptobrevin, syntaxin and synaptotagmin. SNAP-25 and syntaxin are presynaptic membrane proteins, while synaptobrevin and synaptotagmin are synaptic vesicle proteins. SNAP-25, syntaxin and synaptobrevin (VAMP) are the three SNARE proteins (SNAP receptors) that form the core complex involved in synaptic vesicle docking and fusion (Sollner et al., 1993; Jahn and Sudhof, 1994). We have found that SNAP-25-like immuoreactivity (-LIR) is present in a small subset of taste cells (Yang et al., 2000). Approximately 92% of the taste cells we observed with synapses displayed SNAP-25-LIR. Syntaxin, another presynaptic membrane protein, is also expressed in taste cells with synapses (Yang et al., 2004a), as is synaptotagmin (unpublished observations). Using colloidal gold immunoelectron microscopy we have found that synaptobrevin-LIR is closely associated with vesicles at synapses from taste cells onto nerve processes. Based on their ultrastructural features we believe that most, if not all, of the taste cells with synapses in rat circumvallate taste buds are type III cells.