Nerve regeneration-induced recovery of quinine avoidance after complete gustatory deafferentation of the tongue

Abstract

The concentration-dependent decrease in quinine licking by rats is substantially attenuated by combined bilateral transection of the chorda tympani (CT) and glossopharyngeal (GL) nerves, but transection of either nerve alone produces marginal impairments at most. Here we tested whether regeneration of one or both of these nerves after combined transection would result in recovery of taste avoidance. Water-restricted rats were presented with a series of brief-access (5 s) taste trials (water and 0.003-3.0 mM quinine-HCl) in a 5-day test block of 40-min sessions both before nerve transection and starting 75-77 days after transection. Licking avoidance returned to presurgical levels when both nerves were allowed to regenerate. When only the GL was allowed to regenerate, performance did not differ from that of sham-transected animals. This suggests that even after considerable gustatory deafferentation, regeneration has the capacity to restore normal taste-guided behavior. Surprisingly, when only the CT was allowed to regenerate, avoidance behavior was severely impaired and was not different from that of rats in which regeneration of both nerves was prevented. Taking into account prior findings, it appears that the absence of the GL in the presence of an intact CT is fundamentally different from the absence of the GL in the presence of a regenerated CT with respect to some taste functions. This represents the first reported instance to our knowledge in which the capacity of a regenerated nerve to maintain taste-guided behavior was distinctly different from that of an intact nerve in a rodent model.

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

“…When both the GL and CT were cut simultaneously, avoidance threshold increased still further (by 1.8 log 10 units). This is somewhat larger than the within-subject shifts of 1.18 and 1.35 log 10 units reported for CTX + GLX rats with pre-surgical quinine experience (Geran, Garcea, & Spector, 2004; St John, Garcea, & Spector, 1994), suggesting that the remaining quinine avoidance with combined CT+GL transection, presumably due to GSP input, may be improved with presurgical conditioning. However, given that these are separate studies with differing parameters we cannot say for sure.…”

“…Taste pores in fungiform papillae were stained with methylene blue and counted under a light microscope to confirm CTX (see Parks & Whitehead, 1998; Spector, Schwartz, & Grill, 1990) while circumvallate tissue was embedded in paraffin, cut into 5 −10 um sections, mounted and stained using a hemoxylin/eosin procedure to confirm GLX (Guth, 1957; Spector & Grill, 1992). A taste bud was counted in the circumvallate papilla if there was a visible taste pore or a group of well-organized elongated cells very close to the trench, suggesting the apical taste pore was just out of the plane of section (Geran, Garcea, & Spector, 2004). …”

Rewiring the gustatory system: Specificity between nerve and taste bud field is critical for normal salt discrimination

“…Moreover, taste buds, which degenerate upon interruption of the nerve supply, reappear when a transected lingual taste nerve regenerates and reinnervates its native receptor field (Barry and Frank, 1992). Notably, for the most part, taste functions that are disrupted upon nerve transection, are restored once the nerve successfully reinnervates its normal epithelial region (Barry et al, 1993; Cain et al, 1996; St John et al, 1995; King et al, 2000; Kopka et al, 2000; Kopka and Spector, 2001; Yasumatsu et al, 2003; Geran et al, 2004). For the chorda tympani nerve (CT), this recovery of function occurs despite the seemingly permanent anatomical alterations in the gustatory system following regeneration including: decreases in the number of anterior tongue taste buds and their volume (Shuler et al, 2004), decreases in the number of myelinated fibers in the regenerated CT coupled with decreased number of cell bodies in the geniculate ganglion (Cain et al, 1996), and reduced volume and density of the CT terminal projection field in the nucleus of the solitary tract (Barry, 1999).…”

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

“…Moreover, when lingual taste nerves are cut, taste buds in the denervated oral region degenerate, either partially or completely, depending on the species, and the transected fibers regenerate to reinnervate their native receptor field (e.g., 8,9,12,13,19,23,39,55,58,60). Following reinnervation of the epithelium by the nerve fibers, the taste buds return and in the rodents examined, behavioral function is restored (e.g., 3,4,6,14,27,29,30,45). Such plasticity is indeed remarkable, but it is unclear whether the recovered function is dependent upon the tongue receptor field being reinnervated (the source of the input) or upon the nerve and the central circuits it supplies, or both.…”