Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Nerve–Target Interactions in the Gustatory System Following Unilateral Chorda Tympani Nerve Section
Department of Psychology, University of Virginia, Charlottesville, Virginia, VA 22904, USA
Correspondence to be sent to: Dr David L. Hill, e-mail: dh2t{at}virginia.edu
Key words: anterograde, fluorescent tracers, nucleus of the solitary tract, regeneration, retrograde, sodium restriction, taste bud.
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Introduction |
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 Top Introduction AcknowledgementsReferences |
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Although much effort has been directed at examining the morphological characteristics of denervated and regenerated taste buds, relatively little is known about the physiology of reinnervated taste cells (Vintschgau and Hönigschmied, 1876
;
Guth, 1957;
Fujimoto and Murray, 1970;
Cheal and Oakley, 1977;
Whitehead et al., 1987).
Over 25 years ago, Oakley (Cheal et al.,
1977) and colleagues found that some chorda tympani fibers reinnervated
fungiform papillae on the gerbil’s anterior tongue in <2 weeks post-sectioning.
Studies that examined recovery of taste function following nerve damage (Cain et al., 1996;
Cheal et al., 1977;
Ninomiya, 1998;
Yasumatsu et al., 2003)
indicate that regenerated taste nerves generally recover normal function after
progressing through a transitional period. Only relatively recently has the impact of
environment on the adult regenerating taste system been explored.
Regenerating taste receptor cells in adult rats are susceptible to dietary influences
(Hill and Phillips, 1994). Sectioning
the chorda tympani unilaterally in rats fed a sodium-restricted diet at adulthood
resulted in a regenerated nerve that had attenuated responses to sodium salts. Responses
to other stimuli were unaffected. In addition, there were other, novel effects. In the
same rat, the contralateral, uncut nerve was supersensitive to sodium salts. The
supersensitivity developed progressively following an initial subnormal response.
Moreover, these remarkable changes happened in the absence of reinnervation. Although the
mechanism underlying these large, dynamic functional changes are not clearly identified,
increasing evidence suggests a novel and important interaction exists with the immune
system (Phillips and Hill, 1996;
Hendricks et al., 2002;
McCluskey and Hill, 2002;
McCluskey, 2003). We hypothesize that
the immune system may be activated during phagocytosis of neural and taste receptor cell
debris following nerve section in sodium-replete rats. The activated immune cells may
then play a role in maintaining normal function. We further hypothesized, from published
reports (Chandra and Dayton, 1982;
Pimentel and Cook, 1987;
Latshaw, 1991), that
sodium-restricted rats are immunocompromised and may fail to maintain normal taste
function on the intact side of the tongue following unilateral nerve section. In summary,
there is emerging evidence that the immune system has a significant role in the biology
of adult taste buds and may be similar to roles demonstrated in other sensory receptors
(Warchol, 1997;
Warchol, 1999;
Warchol et al., 2001).
In addition to providing an excellent model for functional studies of taste receptor
cell plasticity, the regenerating taste system provides an excellent model in which to
study the plasticity of gustatory neuron/target matching. We explored the hypothesis that
the altered taste function produced by combining unilateral chorda tympani nerve section
with sodium restriction in adult rats also produces alterations in peripheral innervation
(Shuler et al., 2004). For
both sodium-restricted and sodium-replete rats, section-induced morphological alterations
occurred on both the regenerated and the intact side of the tongue. Namely, fewer than
normal numbers of geniculate ganglion neurons per taste bud volume innervated single
fungiform papillae on the regenerated side, and greater than normal numbers of neurons
per taste bud volume innervated single papillae on the intact, contralateral side. The
effect on the regenerated side of the tongue was primarily due to a 20% decrease
in geniculate ganglion cells available to innervate taste buds, while the effects on the
intact side were due primarily to a decrease in taste bud volumes and not to a change in
numbers of innervating neurons. The percentage of ganglion cells lost following chorda
tympani section is similar to that found in other sensory systems (Aldskogius et al., 1985;
Ardvidsson et al., 1986).
Unlike our functional data, there were no diet-dependent effects on the numbers of
innervating neurons or on neuron/target relationships. Therefore, our hypothesis that
altered function translates into altered patterns of innervation was not supported.
Instead, unilateral nerve section produced alterations on both the regenerated and intact
sides of the tongue, regardless of the diet.
The gustatory neurons sustaining profound structural and functional changes
peripherally following nerve section also have a central limb. Previous work showed that
changes in the nucleus of the solitary tract (NTS) following nerve damage include
long-term transganglionic degeneration (Barry and
Frank, 1992;
Whitehead et al., 1995;
Barry, 1999), incomplete recovery of
acetylcholinesterase staining (Barry and Frank,
1992), and relatively specific functional changes (Barry, 1999). The transganglionic degeneration occurred
within 2 days after chorda tympani nerve section, peaked at 8 days and continued as long
as 161 days post-section, without loss of cell soma of the chorda tympani nerve (i.e.
ganglion cells;
Whitehead et al., 1995).
Although these are pioneering studies, none examined (i) the amount of terminal field
remaining after nerve section; (ii) the anatomical and functional plasticity of other
gustatory nerves; (iii) the compensatory or aberrant synaptic changes induced by
peripheral nerve damage; or (iv) the influence of environment on central plasticity. To
address some of these questions, we examined the terminal field volume of the chorda
tympani nerve in the NTS of rats sustaining unilateral chorda tympani nerve section
and/or dietary sodium restriction (Cheon and Hill,
2003). The terminal field of the chorda tympani decreased dramatically after
7 days post nerve section. The total terminal field was ~33% of the control field
volume at 14 days postsection and 25% of controls at 60+ days. Although there
was a decrease in volume throughout the dorsal to ventral extent of the field, the
largest effect occurred in the dorsal zone. This was also the zone that appeared most
susceptible to environmental effects during development in rat (King and Hill, 1991;
Krimm and Hill, 1997;
Pittman and Contreras, 2002). Our
early results also showed that there is no large-scale effect in the contralateral NTS
and there were no diet-related effects.
In summary, there is a dramatic amount of plasticity in the peripheral and central gustatory system induced by unilateral chorda tympani nerve sectioning and/or dietary sodium restriction at adulthood. Neurobiological effects not only occur on the sectioned side of the gustatory system, but also occur on the intact side in some experimental conditions. These experimental procedures will be useful to uncover the underlying cellular/molecular mechanism involved in matching neurons with their peripheral and central targets.
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Acknowledgements |
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TopIntroductionAcknowledgementsReferences |
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Supported by grant no. DC03576.
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