Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Taste Damage: Previously Unsuspected Consequences
Department of Surgery, Yale University School of Medicine, New Haven, CT 06520-8041, USA
Correspondence to be sent to: Linda M. Bartoshuk, e-mail: linda.bartoshuk{at}yale.edu
Key words: burning mouth syndrome, dysgeusia, inhibition, phantoms, PROP
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Inhibition within the taste system |
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Taste damage, taste intensification and taste phantoms
Studies using anesthesia provide insights into oral phantoms. The chorda tympani nerve
is accessible for anesthesia at two sites. First, the chorda tympani leaves the tongue
with the lingual nerve (CN V) and the two travel through the pterygomandibular space. The
inferior alveolar nerve, which conveys pain from the lower teeth, passes through the same
space; thus dental anesthesia abolishes taste and touch as well as pain. Secondly, the
chorda tympani passes through the middle ear after separating from the lingual nerve, so
injection of an anesthetic just under the skin near the ear drum anesthetizes taste but
not touch. Using both procedures, we showed that anesthesia of the chorda tympani
intensifies tastes evoked from the contralateral rear of the tongue, the area innervated
by the glossopharyngeal nerve (Lehman et
al., 1995
;
Yanagisawa et al., 1998).
This finding supports the earlier evidence of
Halpern and Nelson (1965) for central
inhibitory connections between the chorda tympani and glossopharyngeal nerves. This
inhibition acts as a constancy mechanism: when one nerve is damaged, its input to the
central nervous system (CNS) is reduced, releasing inhibition on other taste structures
and thus compensating for the loss of input from the damage.
During our anesthesia experiments, about half of the subjects developed taste
phantoms typically localized to the contralateral rear of the tongue (Yanagisawa et al., 1998). This
suggested that clinical taste phantoms (i.e. dysgeusia) might be the result of localized
taste damage. Indeed, we have found taste damage in patients reporting taste phantoms
(Bartoshuk et al., 2002).
Taste damage, oral pain intensification and oral pain phantoms: burning mouth syndrome (BMS)
Anesthesia of the chorda tympani intensifies the burn of capsaicin on the
contralateral anterior tongue (Tie et
al., 1999), indicating that taste input normally inhibits trigeminal
input centrally. Taste inhibition could protect eating behavior in an animal suffering
pain from tongue damage; it could also aid animals in eating plants defended by natural
mechanisms such as capsaicin or thorns.
The intensification of oral burn is related to the genetic ability to taste PROP
(6-n-propylthiouracil). Some individuals (nontasters) are ‘taste
blind’ to PROP, while to others (tasters) PROP tastes bitter. The development of
new psychophysical procedures (Hall et
al., 1975;
Marks et al., 1988;
Bartoshuk et al., 2004) has
permitted quantification of this bitterness. Tasters are further subdivided into
supertasters (those perceiving the most intense bitter) and medium tasters (those
perceiving less intense bitter) (Bartoshuk et
al., 1994). Anesthesia of the chorda tympani produced the greatest
intensification of contralateral oral burn from supertasters (Tie et al., 1999).
We suspect that interactions between taste and oral pain are responsible for BMS
(Grushka, 1987). Patients with BMS
report intense oral pain in the absence of visible pathology. In a series of BMS
patients, we found severe taste damage. In addition, the intensity of the peak oral pain
correlated with the density of fungiform papillae; that is, patients with BMS were
primarily supertasters (Grushka and Bartoshuk,
2000). According to Grushka, interactions between taste and pain may extend
to other facial pain. For example, patients with atypical odontalgia (pain appearing to
originate from healthy teeth) showed taste damage (Grushka et al., 2002).
GABA (gamma-aminobutyric acid) and taste inhibition
Grushka et al. (1998)
discovered that the majority of BMS patients experienced relief using clonazepam, an
agonist to the inhibitory neurotransmitter GABA, which is found in taste pathways
(Davis, 1993;
Wang and Bradley, 1993;
Smith and Li, 2000). If BMS results
because taste damage produces a loss of the inhibition normally exerted on central
structures mediating oral pain, then a GABA agonist might be expected to counter that
loss of inhibition and thus relieve the oral pain phantom.
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Does taste inhibition operate more generally than previously understood? |
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TopInhibition within the taste...Does taste inhibition operate...References |
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Taste input may inhibit a variety of activities incompatible with eating (Bartoshuk and Snyder, 2002
). The first evidence
for this idea came from a study showing that women with pregnancy hyperemesis show taste
damage (Sipiora et al.,
2000). Interestingly, many folk remedies for the nausea of pregnancy involve
taste. For example, ginger combats nausea systemically (Smith et al., 2004), but when consumed as a folk
remedy, the patient benefits from stimulation of taste as well. Clonazepam has also been
associated with anti-nausea effects (Shindo
et al., 1995).
Berger’s clinical insights have played an important role in the development of
these ideas. She noted that nausea, cough and hiccups are among the clinical problems
afflicting cancer patients at the end of life. Cancer patients typically undergo
therapies that damage taste (Duffy et
al., 2002). Taste stimulation (e.g. eating ginger, sucking a lemon,
eating candies) is anecdotally associated with the treatment of these symptoms and GABA
agonists have therapeutic value (Dicpinigaitis
et al., 2000;
Smith and Busracamwongs, 2003). Given
that taste is also thought to play a role in preparing the gastrointestinal tract for the
arrival of food (e.g. cephalic phase responses) (Teff, 2000), damage to taste may have gastrointestinal
consequences.
The evidence above suggests ways to harness the inhibition produced by the taste system for clinical benefit either by stimulating taste or potentiating central inhibition with clonazepam or other GABA agonists. The role of PROP status may also be important clinically; nontasters may produce less inhibition.
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TopInhibition within the taste...Does taste inhibition operate...References |
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