Journal of Neuroscience, Vol 9, 3522-3528, Copyright © 1989 by Society for Neuroscience
Evidence for a novel mechanism of binding and release of stimuli in the primate taste bud
AI Farbman and G Hellekant
Department of Neurobiology and Physiology, Northwestern University, Evanston, Illinois 60208.
In previous work, we showed that thaumatin, an intensely sweet protein,
binds to certain formed elements in taste pores of Rhesus monkey foliate
papillae, namely, microvilli and small vesicles shed from microvilli, in
addition to amorphous secretions (Farbman et al., 1987). We suggested that
the taste bud responds to a thaumatin stimulus by shedding the small
vesicles containing fragments of microvillar membrane bearing the
stimulus-binding site complex. To examine this hypothesis further, we used
electron microscopy to examine taste pores of both vallate and foliate
papillae from Rhesus monkeys before or after stimulation with thaumatin or
sucrose. We also recorded the neural activity from the glossopharyngeal
nerve during stimulation with thaumatin, sucrose, citric acid, and NaCl.
The results indicate (1) with no stimulation, vesicles are found in pores
of foliate papilla taste buds much more frequently than in pores of vallate
papilla buds, (2) in both types of papillae, stimulation with sucrose has
no apparent effect on the number of pores containing vesicles, (3)
stimulation with thaumatin elicits release of vesicles into pores of both
foliate and vallate buds, (4) repeated stimulation of taste buds with
thaumatin results in a declining neural response, not seen after repeated
stimulation with sucrose, citric acid, or NaCl, and (5) stimulation with
thaumatin suppresses the neural response to sucrose, but the reverse does
not occur. The combined morphological and physiological data support our
original hypothesis that, in response to thaumatin stimulation, binding
sites on taste microvillar membranes may be shed as a stimulus-receptor
complex into the pore. Alternatively, the binding sites may in some way be
altered by the shedding of part of the membrane. The data suggest further
that the binding site for sucrose may be close to that for thaumatin
because it too is lost or altered after thaumatin stimulation. The reduced
neural response after repeated thaumatin stimulation indicates that cells
may have suffered a net loss of functional receptors or at least a loss in
functional capacity of the receptors. The data indicate that the cellular
mechanism for handling the protein sweetener, thaumatin, is strikingly
different from the adsorption-desorption response to saccharide sweeteners.