Gustatory hallucinations. Are these taste distortions similar to auditory neuropathy?
Gustatory hallucinations are relatively common distortions which occur spontaneously in the oral cavity in the absence of any food or beverage. They occur in most patients who suffer a loss of taste acuity following several common events such as a viral-type illness, systemic allergic rhinitis or head injury. These distortions, called phantageusias, can occur in as many as 60% of people who lose taste acuity. These distortions are commonly persistent and extremely disturbing since they are constant and can be considered a type of oral pain.
These patients commonly are evaluated by otolaryngologists once the dentists determine that there are no oral abnormalities present in these patients. However, otolaryngologists are usually baffled by these patients since they also find no oral pathology but find the patient extremely disturbed by this persistent symptom.
These distortions have several characteristics – chemical, very salty, bitter or metallic labeled torquegeusia, rotten or fecal-like labeled cacogeusia, or a mixture of both torquegeusic and cacogeusic characteristics. The majority of patients with these symptoms characterize these distortions as torquegeusia.
Most otolaryngologists, in their quest to help these patients in the absence of any oral pathology, will perform a computerized tomography (CT) scan or magnetic resonance imaging (MRI) of the brain which is almost uniformly within normal limits. Neurologists may perform an electroencephalogram which also almost uniformly is within normal limits. At this point most otolaryngologists and other physicians remain baffled by the presence of this symptom and their lack of techniques to help these patients. At this point they may refer these patients to a neurologist, who also may be unable to help these patients, or they simply give up and suggest that the patient may have to learn to live with the symptom. Some otolaryngologists may perceive that these symptoms are psychological in nature and refer patients to psychiatrists who are also usually baffled by these patients’ symptom. Some physicians consider this symptom a reflection of some type of pain or seizure disorder. Treatment is usually related to use of drugs such as analgesics or antiepileptic medications which are of little to no value.
At The Taste and Smell Clinic in Washington, DC we have evaluated these patients over the past 40 years (1). We have initially evaluated these patients clinically with measurements of taste acuity since most patients state that associated with their distortion is a loss of ability to taste salt, sweet, sour or bitter tastants. This may seem inconsistent to the patient since the loss of acuity is associated with their persistent distortion. Measurements of taste acuity by use of sophisticated but clinically useful tests using a forced-choice, three stimuli, staircase drop technique usually finds a generalized loss of taste by which an abnormality to taste receptor function is determined (1). These tests are available to all physicians with instructions for their use (1).
Based upon these sensory losses the physicians may be confused by the patient’s complaint of taste distortion in the presence of the loss of taste acuity.
In order to understand this apparent incongruity we utilized a technique called functional magnetic resonance imaging (fMRI) (2). By this technique we asked patients to imagine (think of) their taste distortion while in the MRI scanner which is imaging their active brain function. This technique uniformly demonstrated extreme robust brain activation, not only in the brain regions involved with taste function, but also over most of the brain itself which again may seem incongruous since patients may exhibit a loss of taste acuity.
In order to understand these results more fully we next performed tests of brain neurochemistry using magnetic resonance spectroscopy (MRS) by which biochemical measurements of several brain neurotransmitters could be measured quantitatively (3). Use of this technique demonstrated low levels of the neurotransmitter gamma-aminobutyric acid (GABA) in the same brain region in which this extremely robust brain activation was measured by fMRI (3).
Use of this technique by MRS demonstrated a neural mechanism responsible for these hallucinations since brain GABA is a normal inhibitory neurotransmitter which in its absence may allow brain signals, which are normally repressed, to be perceived by the patient and recognized as taste distortions or hallucinations.
Auditory neuropathy is a term used to describe a type of hearing impairment caused by abnormal neural coding of sound stimuli despite preservation of sensory transduction and amplification by outer hair cells of the ear (4). This term was coined for a type of hearing impairment affecting speech comprehension beyond changes in audibility (4). Patients with this condition report that “they can hear but they cannot understand” speech (4). This type of impairment has been reported to be caused by damage to the sensory inner hair cells of the ear – the receptors used by the ear to “hear sounds”. This type of sensory abnormality may be similar to the receptor abnormality presumed to occur in patients with phantageusia. Indeed, patients with auditory neuropathy also report a decrease in auditory acuity (4) which has been measured in these patients and which is similar to the loss of taste acuity measured in patients with phantageusia (1).
Whereas treatment for auditory neuropathy is currently unknown treatment for phantageusia, based on fMRI and MRS studies are present.
Based upon the decreased brain GABA levels, we initially treated these patients with GABAergic drugs (5). The treatment increased brain GABA levels as measured by MRS and inhibited the presence of these gustatory hallucinations as measured by fMRI (3). We next hypothesized that repetitive transcranial magnetic stimulation (rTMS) of brain might have a similar effect. We used this technique and found that in most patients, this procedure also increased brain GABA (5) and inhibited the gustatory hallucinations (5). On occasion, this treatment was associated with an increase in taste acuity (5).
While the detailed neural mechanisms related to auditory neuropathy are not well understood they have been reported to involve presynaptic loading of synaptic vesicles, Ca2+ influx, or synaptic vesicle exocytosis (4). In our studies, increased brain GABA by use of rTMS inhibited gustatory hallucinations in 80% of patients (6). However, the specific brain correlates of this initiation or treatment of these phantageusias have not yet been determined.