Experimentally cross-wired lingual taste nerves can restore normal unconditioned gaping behavior in response to quinine stimulation

Abstract

Studies examining the effects of transection and regeneration of the glossopharyngeal (GL) and chorda tympani (CT) nerves on various taste-elicited behaviors in rats have demonstrated that the GL (but not the CT) nerve is essential for the maintenance of both an unconditioned protective reflex (gaping) and the neural activity observed in central gustatory structures in response to lingual application of a bitter substance. An unresolved issue, however, is whether recovery depends more on the taste nerve and the central circuits that it supplies and/or on the tongue receptor cell field being innervated. To address this question, we experimentally cross-wired these taste nerves, which, remarkably, can regenerate into parts of the tongue they normally do not innervate. We report that quinine-stimulated gaping behavior was fully restored, and neuronal activity, as assessed by Fos immunohistochemistry in the nucleus of the solitary tract and the parabrachial nucleus, was partially restored only if the posterior tongue (PT) taste receptor cell field was reinnervated; the particular taste nerve supplying the input was inconsequential to the recovery of function. Thus, PT taste receptor cells appear to play a privileged role in triggering unconditioned gaping to bitter tasting stimuli, regardless of which lingual gustatory nerve innervates them. Our findings demonstrate that even when a lingual gustatory nerve (the CT) forms connections with taste cells in a non-native receptor field (the PT), unconditioned taste rejection reflexes to quinine can be maintained. These findings underscore the extraordinary ability of the gustatory system to adapt to peripherally reorganized input for particular behaviors.

Necessity of the glossopharyngeal nerve in the maintenance of normal intake and ingestive bout size of corn oil by rats

“…Quinine-evoked gaping is normal in rats when the CT cross-reinnervates the posterior tongue in the absence of the GL but is severely suppressed when the GL crossreinnervates the anterior tongue in the absence of the CT. This suggests that the effects of GLX on certain quinine-evoked central nervous system and behavioral responses are due to the exceptional signal generated by the posterior tongue taste receptors, regardless of which nerve innervates them, upon application of this aversive stimulus (30). This conclusion is consistent with the dense expression of T2Rs in this oral taste receptor field (8).…”

Licking and gaping elicited by microstimulation of the nucleus of the solitary tract

“…In contrast, bilateral transections of the IXth nerve greatly attenuate the medial FLI and result in a profound reduction in gaping (19,33,34,57). Moreover, when the IXth nerve is allowed to regenerate, FLI and gaping recover in parallel (32,33). However, this correlation did not prove to be causal.…”

“…The preferential medial distribution of FLI is unique for bitter vs. other taste qualities (26,61) and is preserved with decerebration (60), a manipulation that also preserves gaping (18). In contrast, bilateral transections of the IXth nerve greatly attenuate the medial FLI and result in a profound reduction in gaping (19,33,34,57). Moreover, when the IXth nerve is allowed to regenerate, FLI and gaping recover in parallel (32,33).…”

“…In contrast, elimination of input from the IXth nerve has only minimal impact on operant behaviors involving bitter (and other) discriminations (51) but significantly reduces the number and abolishes the distinctive topographic pattern of bitterinduced Fos neurons of the NST (32)(33)(34). Despite minimal effects on operant behavior, IXth nerve transection profoundly impairs the unconditioned oral rejection reflex (gaping), a behavior preferentially elicited by bitter stimuli (19,33,57).…”

“…Despite minimal effects on operant behavior, IXth nerve transection profoundly impairs the unconditioned oral rejection reflex (gaping), a behavior preferentially elicited by bitter stimuli (19,33,57). These parallel behavioral and anatomic effects of IXth nerve cuts suggest the possibility that bitter-activated Fos neurons in the medial third of the NST have a preferential role in eliciting gaping.…”