Recently, a taste phenotype termed thermal taster status has been described¹. Thermal taster status refers to the fact that, in some individuals, thermal stimulation of the tongue elicits a phantom taste. Little is known regarding the mechanism behind this, but behavioural data² has led to the hypothesis of cross-wiring between taste and temperature receptors co-innervating papillae on the tongue. Here, we use fMRI to perform the first study to determine whether cortical areas respond to the perception of phantom taste.

21 subjects were screened for thermal taster status (8 male, 26± 4yrs). 9 subjects (3 male, 27± 4yrs) were classified as thermal tasters (TTs) and took part in the fMRI study.

Thermal Taster screening was performed using an intra-oral thermode (Medoc Pathway) to deliver warming and cooling thermal stimuli to the anterior tongue tip^1,2, Fig1. Subjects were asked whether they perceived a taste during heating and/or cooling thermal stimulation, and if so, to describe the taste quality (sweet, salty, bitter, sour, umami, ‘metallic’, etc.), and using a rollerball to indicate the time point(s) they perceived the taste and to rate its intensity on a general Labelled Magnitude Scale (gLMS). Thermal tasters were classified as those who perceived a taste during warming or cooling.

fMRI Protocol:

Subjects were scanned during blocks of warming trials followed by cooling trials (Fig. 1), with 10 repetitions of each trial. During fMRI, subjects indicated using a rollerball, the time point(s) they perceived a taste and its intensity for each warming/cooling trial on a gLMS. A control task was employed to model confounding effects (e.g., due to motor activation) of the rollerball rating in which subjects were not exposed to any thermal stimuli, but were instructed to rate using the rollerball.

fMRI Data Acquisition and Analysis:

fMRI data was acquired on a Philips 3T Achieva scanner with 32-channel receive coil using 36 transverse dual-echo GE-EPI images (TE: 20/45ms, TR: 2.5s, 3x3x3mm3, SENSE 2), and an MPRAGE image was collected to aid registration of functional maps to MNI space. Weighted fMRI data were slice timing corrected, realigned, normalised to MNI space, and spatially smoothed (6 mm) and temporally filtered using SPM12. A GLM was formed for each subject to identify cortical activation to phantom taste. For each individual, the onset and duration of the phantom taste was determined from the continuous rollerball taste intensity ratings collected during the fMRI acquisition. This rollerball time series was convolved with a canonical haemodynamic response function, and motion parameters included as covariates of no interest. Thermal tasters who responded to warming or cooling trials were pooled, with maps combined at the 2^nd level random effects group (RFX) analysis

During thermal stimulation of the tongue, the intensity of the “phantom” taste reported was between weak and strong on the gLMS, with an average intensity rating of above moderate. TTs reported perceiving tastes during warming trials, cooling trials or both, with sweet taste reported being most often perceived during warming trials, and sweet/minty during cooling trials, Fig 2. Behavioural rollerball data collected during the fMRI session indicated consistency in onset of the perceived phantom taste across the 10 repetition, Fig 3. RFX maps from thermal tasters showed that phantom taste perceived during thermal stimulation of the tongue activated taste areas including anterior insula [(-36, 16, 4), T=5.12, P<0.001], frontal operculum [(-48, 14, 8), T=5.52, P<0.001] and ACC [(4, 26, 44), T=4.83, P<0.001], Fig. 4. Maps in response to the control task, to assess rollerball movements, were limited to a small region of somatosensory areas with no activation in taste areas.Behaviourally thermal tasters have been shown to be more sensitive to pure taste stimuli at supra-threshold levels², and the temperature of warm and cold stimuli³ compared with thermal non-tasters (TnTs). The mechanism for this increase in sensitivity in TTs has been hypothesised to be due to a temperature sensitive chemosensory pathway¹. A hypothesis supported by the discovery that the TRPM5 cation channel, which responds to sweet, bitter and umami tastes is also heat activated and highly temperature sensitive⁴. We demonstrate that thermal stimulation applied to the anterior of the tongue can elicit a clear “phantom” taste response in thermal tasters generating a cortical response in primary gustatory cortex. Recently, fMRI studies have shown a heightened cortical response in TTs compared with TnT to taste, aroma flavour and trigeminal stimuli^5,6, again supporting a mechanism of entwined gustatory and trigeminal nerves in thermal tasters.