Chizuko Yamamoto, Hajime Nagai, Kayo Takahashi, Seiji Nakagawa, Masahiko Yamaguchi, Mitsuo Tonoike, and Takashi Yamamoto
Red berries of a tropical plant called miracle fruit, Richadella dulcifica, reduce the sour and aversive taste of acids and add sweet and palatable taste. To elucidate the brain mechanism of this unique action of miracle fruit, we recorded taste-elicited magnetic fields of the human cerebral cortex. The initial taste responses were localized in the fronto-parietal opercular/insular cortex reported as the primary taste area. The mean latency of the response to citric acid after chewing miracle fruit was essentially the same as that for sucrose and was 250–300 ms longer than that for citric acid.
Since it is known that stimulation with acids after the action of miracle fruit induces both sweetness and sourness responses in the primate taste nerves, the present results suggest that the sourness component of citric acid is greatly diminished at the level of subcortical relays, and mostly sweetness information reaches the cortical primary taste area. We propose the idea that the qualitative aspect of taste is processed in the primary taste area and the affective aspect is represented by the pattern of activation among the different cortical areas.
Introduction
Miracle fruit, red berries of a native shrub, Richadella dulcifica, in tropical West Africa, contains a taste-modifying protein, miraculin which has the unusual property of reducing sour taste of acids and adding sweet taste e.g.: the taste of lemon changes into that of orange.
One explanation for the taste modifications by miracle fruit is that this dramatic effect comes from the addition of sweetness to sourness, resulting in the suppression of sourness in the central nervous system rather than direct suppression of sourness at the receptor level. The sweetness could be induced by the interaction of the sugar component of this glycoprotein to sweet receptors on taste cells as a result of conformational changes of the cell membrane by acid stimulation.
As supportive evidence of this notion showed that the taste nerves of the monkey actually conveyed both acid and sugar information in response to acids after treatment of the tongue with miraculin. Another one showed single fiber analyses of the chorda tympani nerve in chimpanzees that a subset of fibers responsive exclusively to sweeteners but not to acids responded to acids as well as to sweeteners after miraculin.
Methods
A total of 28 subjects who are neurologically healthy volunteers aged from 22 to 35 years: 10 males and 18 females. 7 males and 12 females were right handed, and 3 males and 6 females were left-handed participated in the pilot study and received screening tests where they were examined for several aspects concerning suitability as subjects including adequate patience in the shielded room, good compatibility of the tongue with the flow chamber, good evoked MEG responses and long lasting and remarkable taste-modifying action of miracle fruit.
They were informed about the nature of the experiment on taste stimuli used were 0.05 M citric acid and 0.5 M sucrose. At these concentrations, all the subjects reported that the citric acid was sour and unpleasant and that the sucrose was sweet and pleasant. These solutions were made just before the experiment by dissolving the reagent grade chemicals into distilled water. The solutions and water were used at room temperature (24 ± 1 °C).
To analyze the taste-modifying action, responses to citric acid were recorded after chewing one or two pieces of miracle fruit berries for 3 min. Miracle fruit.
Soon after each session, the subjects were asked to describe each stimulus, and we confirmed that they described citric acid as sour, sucrose as sweet, citric acid after miracle fruit as mostly sweet with slight sourness toward the end of the session, and water as tasteless.
Results
Reliable and reproducible data were obtained in 7 subjects. They were 5 males and 2 females; 3 males and 1 female were right handed, and 2 males and 1 female were left-handed. For the assessment of validity of the response patterns, averaged responses in the same subject to citric acid, sucrose, citric acid after miracle fruit and water from all the 24 recording points were superimposed on the same graphs.
Sucrose, and citric acid after miracle fruit induced responses with longer latencies than that of citric acid. Water evoked essentially no response. To further assess the validity of the above findings across subjects, representative averaged responses obtained from a prescribed electrode in each subject were examined by exhibiting superimposed traces. The time courses and the magnitudes of responses were very similar among the 7 subjects for each of the 3 stimulations.
The results show that the first ECD was obtained in the frontal lobe in 4 subjects and in the parietal lobe in 3 subjects. It is noted here that ‘frontal lobe’ is more anterior than our ‘frontal lobe’. Although there seemed to be a tendency for activation to sucrose and citric acid after miracle fruit to be located more anteriorly and for activation to citric acid to be found posteriorly, further analysis is needed to provide clear evidence for chemotopy in the PTA. Besides the PTA, other areas of the cortex were also activated by taste stimuli, i.e., ECDs were estimated outside the taste areas. These areas included the superior temporal sulcus, central sulcus, lingual gyrus, middle temporal sulcus, cuneus, angular gyrus, parahippocampal gyrus and supramarginal gyrus. The cortical areas activated differed depending on the kind of taste stimuli and among the subjects. However, no apparent difference was detected between the left and right hemispheres for these activated areas.
Discussion
Studies in non-human primates have suggested the existence of two taste areas (PTA and STA) in the cerebral cortex: the PTA is in the transitional zone of the frontal operculum and the anterior insular cortex and the STA is in the caudolateral OFC includes the somatosensory area 3 in the PTA and precentral opercular area and areas 1–2 in the STA.
Non-invasive recordings from the human brain have shown taste-elicited activation in two areas corresponding to the PTA and the STA. In addition to these areas, other brain areas including the inferior part of the insula and the anteromedial temporal lobe are also shown to be activated by taste stimuli.
The most interesting and unexpected finding in the present study was that the response latency to citric acid after miracle fruit was essentially the same as that to sucrose. As for the peripheral mechanism of taste-modifying action of miracle fruits, miraculin stimulates sweet receptors under acidic conditions, i.e., acid information is not converted to sweet information, but both acid and sweet information are conveyed through the taste nerves to the brain.
Also after miracle fruit treatment when citric acid is reported to taste sweet in humans, sour taste is recovered by treatment of the tongue with an anti-sweet agent, gymnemic acid. Considering these findings, we expected to record two components of responses in the PTA corresponding to an early response to sour information and a late response to sweet information. If the sour component were to disappear as a result of processing exclusively in the cortex, the early acid responses should have been obtained in the PTA.
The present results, however, showed that mainly the late response was detected, suggesting that the sour component signal in the taste nerves diminishes while being processed through the brainstem to the PTA. To confirm and extend the mixture effect of sweetness and sourness suggested for the action of miracle fruit, a further study should be done on the mixture effect of different tastes under well controlled design with the MEG technique in humans.
These findings also suggest that simple reception of ascending neural inputs for PTA neurons may be sufficient to induce simple and rapid sensation of the taste quality because the taste information, even in part, has been processed or modified through the subcortical taste pathway.
The experience of taste is similar to the experience of pain in the sense that both sensory and affective components are involved.
Alternatively, activation of various parts of the brain may reflect the involvement of chemical systems influencing widespread areas of the brain by taste stimulation. It is well known that dopaminergic fibers from the ventral tegmental area project widely to various parts of the forebrain including the cerebral cortex.
In conclusion, comparing sweet and sour information conveyed by the taste nerves in response to citric acid after chewing miracle fruit, the present MEG study strongly suggests that only sweet information is processed by the primary taste area. Citric acid after miracle fruit was very similar to sucrose in terms of the response latency and the across-region response pattern of the cerebral cortex possibly representing the affective aspect of taste.
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