Glossopharyngeal nerve transection impairs unconditioned avoidance of diverse bitter stimuli in rats.

Abstract

There is growing evidence of heterogeneity among responses to bitter stimuli at the peripheral, central and behavioral levels. For instance, the glossopharyngeal (GL) nerve and neurons receiving its projections are more responsive to bitter stimuli than the chorda tympani (CT) nerve, and this is particularly true for some bitter stimuli like PROP & cycloheximide that stimulate the GL to a far greater extent. Given this information, we hypothesized that cutting the GL would have a greater effect on behavioral avoidance of cycloheximide and PROP than quinine and denatonium, which also stimulate the CT, albeit to a lesser degree than salts and acids. Forty male SD rats were divided into 4 surgery groups: bilateral GL transection (GLX), chorda tympani transection (CTX), SHAM surgery, and combined transection (CTX + GLX). Post-surgical avoidance functions were generated for the 4 bitter stimuli using a brief-access test. GLX significantly compromised avoidance compared to both CTX and SHAM groups for all stimuli (p < .02), while CTX and SHAM groups did not differ. Contrary to our hypothesis, GLX had a greater effect on quinine than cycloheximide (mean shift of 1.02 vs. 0.27 log10 units). Moreover, combined CTX + GLX transection shifted the concentration-response function further than GLX alone for every stimulus except cycloheximide (p’s < .03), suggesting that the GSP nerve is capable of maintaining avoidance of this stimulus to a large degree. This hypothesis is supported by reports of cycloheximide-responsive cells with GSP-innervated receptive fields in the NST and PBN.

Mouse parabrachial neurons signal a relationship between bitter taste and nociceptive stimuli

“…Notably, glossopharyngeal fibers show robust firing to lingual presence of cycloheximide (Danilova and Hellekant, 2003), which was presently identified as a key predictor of nociceptive-active, bitter-class PbN neurons. That glossopharyngeal nerve input may drive bitter activity in these units further supports their involvement in protective coding, as severing the glossopharyngeal nerve impairs rejective, but not discriminative, rat oral behavioral responses to bitter stimuli (St. John and Spector, 1998;Geran and Travers, 2011). In closing, the present data reveal that neural messages associated with bitterness and oral pain are partly relayed to PbN neurons dually linked to gustatory and trigeminal processing.…”

Bitter Taste Stimuli Induce Differential Neural Codes in Mouse Brain

“…Such discrimination would support selection of plants of reduced toxicity or signal highly toxic vegetation requiring countermeasures for edibility, such as the co-ingestion of earth performed by certain plant-eating animals to presumably absorb and neutralize bitter toxins in plants [62], [69]. Neural distinctions among the tastes of “bitter” stimuli, as observed presently, may reflect the conservation of a trait supporting perceptual distinctions used in the wild to discriminate chemical toxicity [53]. Although denatonium and SOA are synthetic chemicals that from an evolutionary perspective co-opt bitter taste receptors, the naturally occurring bitters quinine, an alkaloid in vegetation, and cycloheximide, produced by bacteria in soil, were found here to induce differential taste codes in mice, corresponding to a roughly tenfold difference in the toxicities of these chemicals (mouse oral LD 50 : cycloheximide, 0.1 g/kg [70]; quinine, 1.2 g/kg [71]).…”

“…On the other hand, oral delivery of cycloheximide or SOA induces strong activity in rodent IX but a relatively low or null response in VII [13], [17], [19], [49]–[52]. Thus, unlike quinine and denatonium, SOA and cycloheximide tend to show high, but possibly not exclusive [53], affinity for receptors innervated by IX. Speculatively, TBCs supplied by VII and IX may express different repertoires of bitter taste receptors.…”

Differential neural representation of oral ethanol by central taste-sensitive neurons in ethanol-preferring and genetically heterogeneous rats

“…It is possible that the oral stimulation technique used did not effectively bathe taste receptors on the posterior tongue innervated by the IXth nerve. This nerve is implicated in oral reflexive behaviors (Travers et al 1987) and importantly contributes to unconditioned avoidance responses to bitter stimuli in oral sensory behavioral paradigms (Geran and Travers 2011). The IXth nerve drives a unique population of NTS units, some selective toward bitter tastants (Geran and Travers 2006), and it would be worthwhile to investigate how afferent input from IX would contribute to ethanol taste representations in W and P rats.…”