Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Location of the Primary Gustatory Area in Humans and its Properties, Studied by Magnetoencephalography
1 National Institute of Advanced Industrial Science and Technology (AIST), 2 Faculty of Medical and Pharmaceutical Sciences, Kumamoto University, 3 Kobe Shoin Women’s University
Correspondence to be sent to: Tatsu Kobayakawa, e-mail: kobayakawa-tatsu{at}aist.go.jp
Key words: brain, fMRI, humans, MEG, primary gustatory area, taste
The precise location of the primary gustatory area (PGA) in humans has not been
determined conclusively, regardless of intensive studies with various non-invasive brain
imaging. Analysis of brain function by fMRI and PET is based on changes in the regional
cerebral blood flow (rCBF) several seconds after electrical neural activity. Thus, these
techniques are not suitable for the location of the PGA, the cortical area activated at
the shortest latency after gustatory stimulation, though most studies have localized the
putative PGA in the middle dorsal insula and the frontal operculum (Small et al., 1999
, 2003;
O'Doherty et al.,
2001;
De Araujo et al., 2003) by
analogy to the PGA in monkeys. However, the anatomical structure of the human brain does
not always present in the location corresponding to that of the monkey; for example, the
human primary visual area is located on the medial surface of the occipital lobe, whereas
that of subhuman primates is on the lateral surface. Thus, it is possible that the human
PGA and monkey PGA reside in different locations.
Börnstein (1940) investigated
three patients with hematoma at the base of the postcentral gyrus caused by gunshot
wounds. The patients with hematoma close to the lateral sulcus showed ageusia or
hypogeusia. The patient with hematoma dorsal to the lateral sulcus showed parageusia.
Penfield and Jasper (1954) evoked
gustatory sensation by electrical stimulation of the dorsal middle-posterior insula and
fronto-parietal operculum inside the lateral sulcus during the brain surgery and found
the foci of gustatory aura in similar regions.
Hausser-Hauw and Bancaud (1987)
reported two foci related to gustatory hallucination: one at the dorsomedial region of
the temporal lobe and one at the parietal lobe superior to the lateral sulcus. The
parietal focus causes gustatory hallucination only in contrast to the temporal focus
generally inducing both olfactory and gustatory hallucinations. The parietal lobe is,
therefore, considered to be a taste-specific area. Although
Faurion et al. (1999) and
Zald and Pardo (2000) reported
activity in the Rolandic operculum, which partially overlaps with the parietal lobe, few
fMRI and PET studies have reported activity in the parietal lobe. A clear discrepancy is
noted between most fMRI and PET results and clinical observations.
MEG, on the other hand, can measure brain activity with a time resolution of 1 ms.
Additionally, MEG can locate the active area with high spatial resolution when the number
of cortical areas activated within a given latency is limited.
Suk et al. (1991) reported
that the regions activated by electrical stimuli at the index finger and little finger
were 5.8 mm apart in the primary somatosensory cortex and clearly statistically
distinguishable. Likewise,
Pantev et al. (1995)
reported that areas activated by pure tones of 500 Hz and 1 kHz were 6 mm apart in the
primary auditory cortex. These reports demonstrate that MEG can locate activated areas in
the primary sensory cortex with both high temporal and spatial resolutions.
Kobayakawa et al. (1996,
1999) developed a gustatory stimulus presentation device characterized by a short rise
time of the taste stimulus avoiding tactile component to measure gustatory evoked
magnetic fields (GEMfs). The taste delivery system has previously been described in
detail (Kobayakawa et al.,
1996). Deionized water was always presented to participant’s tongue and
short duration taste stimuli were inserted repeatedly in the constant water flow with the
two fluids separated by air bulbs. The participant covered a small hole opened in the
wall of a tube with the tip of his/her tongue and the air and liquid did not leak into
participant’s mouth. The stimulation area was approximately the same as the
filter-paper disk, clinically used to evaluate the gustatory function (Tomita and Ikeda, 2002). Solutions of 1 M NaCl
and 3 mM saccharin were used as tastants. The earliest activation was most frequently
found at the transition area between the posterior insula and parietal operculum (area G
in humans), followed by the bottom of the central sulcus (CS). The average latency of
activation in area G was 155 ms and 267 ms for NaCl and saccharin, respectively and the
difference between these latencies was significant. No activation was observed at the CS
for saccharin stimulation. Following area G and the CS, late activation was found in
several cortical regions, e.g. the hippocampus, parahippocampal gyrus, superior temporal
sulcus, intra-parietal sulcus, frontal operculum and anterior insula. These last two
regions were denominated as the putative PGA by fMRI and PET studies.
Kaneda et al. (2004) also
discovered the first cortical activation in area G with the average latency of 327 ms
after the presentation of isohumulones-enriched decarbonated beer. The results also show
that the activity latency in area G varies with different taste stimuli, probably because
of the different transduction mechanisms in taste receptors.
Mizoguchi et al. (2002)
recorded gustatory-evoked potentials (GEPs) together with GEMfs using the aforementioned
taste delivery system. Each participant received a total of 240 stimulus presentations in
six sessions. Three components—P1, N1 and P2—were observed in GEPs. ECD
corresponding to P1 was localized in area G in all participants and no significant GEPs
activity was detected preceding the P1, suggesting the presence of no cortical activity
other than that detected by MEG.
Findings based on MEG at a high temporal resolution and clinical studies indicates that area G in humans and the CS are the most likely candidates for the PGA in humans. The mid-frontal operculum and anterior insula, reported as the putative PGA by fMRI and PET studies, are more likely to be high-order gustatory regions, because they were activated with longer latencies in MEG experiments.
The reason is still unclear as to why the activation of the parietal region has rarely been observed by PET or fMRI studies. Frequent repetition of stimuli with short duration, e.g. quick reverse of checker pattern in vision experiments, is probably required to observe rCBF changes in the primary sensory cortices. In gustation, however, long-lasting stimuli have been used in PET and fMRI studies. The present authors, therefore, attempted to examine whether fMRI detects cortical activation by repetitive stimulations of the tongue tip with NaCl by using a computer-controlled stimulator and found the activation of area G in nine out of eleven participants in individual analysis. The results indicate that changes in the rCBF in area G in humans are observable in fMRI study, if repetitive applications of stimuli with short duration were used.
Besides, the present authors also presented four concentrations of NaCl (30 mM, 100
mM, 300 mM and 1 M) to six healthy volunteers under the same stimulus and recording
condition as previously. Participants were asked to rate the perceived intensity with
fingers (from 0 to 5), a few seconds after the taste detection. They found significant
differences in the ECD amplitudes in area G across concentrations [F(3,15)
= 8.99, P < 0.001, one-way ANOVA], but non-significant difference
in the latency [F(3,15) = 0.60, n.s.], as shown in the onset
latency of GEMfs (Saito et al.,
1998). They also observed significant differences in the perceived
intensities across concentrations [F(3,15) = 10.7, P <
0.001]. When the value was plotted against log concentration, the linearity was,
however, better with the ECD amplitude (R2 = 0.976) than with
perceived intensity (R2 = 0.878).
In this paper, we have demonstrated that the transition area between the posterior insula and parietal operculum and the CS was the most likely candidate for the PGA in humans and that the activation latency differs among tastants and amplitudes reflect concentrations.
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