Chem. Senses 24: 201-209,
1999
© Oxford University Press
Spatio-temporal Analysis of Cortical Activity Evoked by Gustatory Stimulation in Humans
Human Informatics Department, National Institute of Bioscience and Human-Technology, Higashi1-1, Tsukuba 1 Department of Physiology, Kumamoto University School of Medicine, Kumamoto 2 Sapporo Breweries Ltd, Shizuoka 3 Institute of Psychology, University of Tsukuba, Tsukuba, Japan
Correspondence to be sent to: Tatsu Kobayakawa, National Institute of Bioscience Human-Technology (NIBH), Higashi 1-1, Tsukuba 305-8566, Japan. e-mail:kobayakawa{at}nibh.go.jp
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Gustatory activated regions in the cerebral cortex have not been identified precisely in humans. In this study we recorded the magnetic fields from the brain in response to two tastants, 1 M NaCl and 3 mM saccharin. We estimated the location of areas activated sequentially after the onset of stimulation with magnetic source imaging. We investigated the primary gustatory area (area G) precisely, and found it at the transition between the parietal operculum and the insular cortex. The central sulcus was activated less frequently than area G but with almost the same latency in cases of NaCl stimulation. Following area G, we found activation in several cortical regions, e.g. both the frontal operculum and the anterior part of the insula, the hippocampus, the parahippocampal gyrus and the superior temporal sulcus.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The gustatory-related regions of the cerebral cortex in human beings have been the subject of argument for a long time (since Penfield and Boldrey, 1937
). Although
intensive electrophysiological experiments on gustatory areas have been made on subhuman
primates (for reviews see Ogawa, 1994; Rolls, 1989),
research on human beings has been limited to clinical observation of patients with
brain damage (e.g. Motta, 1959). In most cases, damage is not confined
to a pinpoint place in the brain but instead involves a wide area, which makes clinical study
difficult. Thus little has been discovered about the location and function of gustatory cortex in
the human brain to date.
Recent development of imaging techniques has yielded various non-invasive methods, e.g.
functional magnetic resonance imaging (fMRI), positron emission tomography (PET) and
magnetoencephalography (MEG), and allows us to measure the cerebral activities of living
human subjects without surgical invasion. Among these methods, PET and fMRI have
insufficient temporal resolution to trace the cortical flow of taste information. Kinomura et
al. (1994) revealed many gustatory-related regions in human cerebral
cortex with PET. MEG, on the other hand, has good temporal resolution, and can give a good
estimation of the location of the activity much more precisely than electroencephalography
(EEG), because the magnetic field generated from living brain is free from distortion by the
skull. However, a pulse-like presentation of a pure tastant free from tactile stimulation is
indispensable in the measurement of gustatory-related cerebral activities by MEG or EEG.
Because of the difficulty in building such a stimulator, only a few reports have been made of
gustatory evoked potentials (Funakoshi and Kawamura, 1971; Kobal, 1985; Prescott, 1989; Plattig,
1991) in a long history of EEG measurement.
We devised a tactile-free taste delivery system with a rise time of 20 ms or less (Kobayakawa et al., 1996a). By integrating both the taste stimulator and a
64-channel whole-head SQUID MEG measurement system, we measured the magnetic fields
evoked by gustatory stimulation inshort latencies (e.g. <200 ms for NaCl and <400 ms
for saccharin), and located the source of the first peak, i.e. the primary gustatory area (area G), at
the transition between the operculum and insular cortex (Kobayakawa et al.,
1996b). However, we could not determine the precise location; that is, it is not clear
whether the area is at the transition between the frontal operculum and insula, as in macaque
monkeys (Ogawa et al., 1985), or between the parietal
operculum and insula. On the other hand, it is known that the oral representation region in the
primary somatosensory area (SI) is activated as fast as area G in monkeys when peripheral taste
nerves are stimulated electrically (Ogawa et al., 1985), though
only area G has previously been found to contribute to the gustatory evoked magnetic fields
(GEMs). Further, we noticed a lack of the previously defined first peak of GEMs in a few cases
with an increased number of subjects and recording sessions.
In the present study, therefore, the aim of the investigation was threefold. We attempted (i) to
clarify the contribution of SI to the first peak of GEMs by increasing the number of subjects and
sessions to see if the afferent projection to SI from the thalamic gustatory area is the same in
humans as in monkeys (Ogawa et al., 1985); (ii) to determine
whether area G was anterior to the central sulcus or posterior to it; and (iii) to examine the
sequence of activation of the gustatory-related cortical regions revealed by PET after area G to
trace the possible flow of taste information.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Subjects
Seven neurologically healthy volunteers (four males and three females, age 21-37 years) participated in the experiments. They were informed about the nature of the experiment, and agreed to become subjects. The study was conducted in accordance with the revised version of the Helsinki declaration and was approved by the National Institute of Bioscience and Human-Technology, Japan.
Stimulation
The taste delivery system has previously been described in detail (Kobayakawa et
al., 1996a), and is represented in Figure 1a. In
short, deionized water and tastants were driven through the system by compressed air. The small
amount of air that separated the tastant and water was released into the tube for as short a
duration as possible (90ms) to minimize the chance of the subject feeling a pressure difference
between the liquid and air. The water, tastants and air flows in the tube were switched by
solenoid valves which were controlled by a personal computer (Figure 1a,b).
Stimuli were presented to the tongue through a hole (3 x 9 mm) opened in
the wall of a Teflon tube. The subject took the tube in his/her mouth, then covered the hole with
the tip of his/her tongue. Liquid and air then flowed over the part of the tongue that covered the
hole (Figure 1c). Since the flow of the liquid and air generated a slight
negative pressure, the tip of the tongue was sucked slightly into the hole, hence air and the liquid
did not leak outside the tube. We used an optical sensor to measure the time at which the tastants
reaches the tongue, in order to obtain a trigger for averaging the GEMs. The tastants were
colored red, whereas air and water were uncolored. Black tape covered the Teflon tube close to
mouth, to prevent subjects from seeing changes in the color in the tube (Figure 1c).A light outside the shielded room was passed through the Teflon tube just before
the hole and the tastant was detected by a photo-transistor. The voltage generated by the
photo-transistor was converted into a digital signal by an A/D converter. The distance between
the measurement location and the hole on the tube was 6.5 cm. It took ~300 ± 2.9 ms
(mean ± SD) for the fluid to run that distance. The rise-time to 80% of the signal was
16.5 ± 1.49 ms.
|
Solutions of 1 M NaCl and of 3 mM saccharin were used as tastants. The fluid was presented at the central, front edge of the subject's tongue, the part known to have high sensitivity to these tastes. The stimulus duration was 400 ms and the inter-stimulus interval 30 s. The tastant and water were kept at 36°C, approximately the same temperature as that of the tongue. The flow rate of the water and stimuli was 200 ml/min. During the recording session, the subjects wore earplugs. They were instructed not to change their head positions, keep their eyes open and watch a fixation point in front of them. Before each recording, we accustomed each subject to this experimental condition. After each recording, subjects were asked about the quality of the taste. The averaged intensity was 2.85 for salty stimuli and 2.55 for sweet in seven subjects, and there was no significant difference. They were also asked about the somatic (i.e. tactile and thermal) sensation incidental to the taste stimulation; however, none of them reported any, which is consistent with the previous finding that there was no MEG response to water stimuli (Kobayakawa et al., 1996b
). We presented only one tastant to a given subject in each session. Each subject participated in one session per day, in order to avoid fatigue. The sessions for a given subject were separated by >2 days.
Recordings of magnetic fields
For measurement of magnetic fields, we used a 64-channel whole-head SQUID system (CTF Systems Inc., Canada; Figure 1b). The sampling rate for the MEG signal was 250 Hz and the low-pass filter was set at 40 Hz. Forty trials were presented to each subject per session. After the experiment, the signals from the optical sensor were used as a trigger for off-line averaging of the data. Trials contaminated by eye movement were rejected. The number of trials used for averaging was nearly 35. If the number of available trials was <30, the session was rejected. The number of sessions available for data processing was 23 (11 for NaCl and 12 for saccharin).
Three-dimensional MRI scans were obtained for all subjects (SIEMENS: 1.5 tesla for six
subjects, 1.0 tesla for one subject). For source modeling, MRI head shape data were used to
determine the fitting sphere for each subject's head. Estimation of equivalent dipoles
(ECDs) were carried out to minimize the estimation error, based on the
Grynszpan–Geselowitz equation (Grynszpan and Geselowitz, 1973; see
Kobayakawa et al., 1996b). The error E was calculated
using the following formula:
 |
where Xn is the magnitude of the neuromagnetic field at the nth sensor and Xn is the calculated magnitude at the same sensor based on the theoretical model. The goodness of fit was calculated as 1 – E. The locations as well as the strength of the ECDs in each subject were estimated from magnetic fields obtained from 64 sensors.
The location of the head with respect to the sensors was determined by measuring the magnetic fields produced by small currents delivered to three coils attached to the scalp, located at the nasion and the two pre auricular points. When we obtained the subjects' MR image, oil-filled pellets were attached to the same landmarks as used in the MEG experiment. The positional information for the centers of three white balls in the subject's MR image, i.e. the images of the oily pellets, were used to align the MEG data with the participant's MR image. The coordinates of the dipole centers of gravity were overlaid on individual MRI slices to show the corresponding locations in the brain, after alignment.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Gustatory evoked magnetic fields
Figure 2 shows superimposed magnetic fields of 12 out of the 64 channels, and an isocontour map over the head, in response to two tastants. These 12 channels had remarkable changes in magnetic fields, at 370 ms after the onset of saccharin presentation and at 110 ms after NaCl. Both isocontour maps showed that the induced magnetic field was directed from the front to the back on the left side of the head and from the back to the front on the right side.
|
Contribution of activation in SI to the first peak of GEMs
In the present study, we detected the first peak of the GEMs regardless of the length of the latency and examined the cortical area which contributed to the production. In each hemisphere of seven subjects in 23 sessions, we chose the single latency of the first change in the GEMs at which we could estimate certain cortical regions clearly, i.e. the time of best fit (TOBF) for the earliest ECDs. In some sessions, two ECDs were estimated in one hemisphere at the first TOBF. Figure 3a,b shows the distributions of such TOBFs in 11 sessions for NaCl and 12 sessions for saccharin respectively.
|
We found that the total activations were most frequent at 75 and 125 ms for NaCl (Figure 3a). Area G was the most frequently activated at the first TOBF (12 of the 22 hemispheres examined), followed by the central sulcus (seven hemispheres), the hippocampus (three hemispheres), and the frontal operculum and the parahippocampal gyrus (one hemisphere respectively). Activation of both area G and the central sulcus clearly contributed to the fastest group of the TOBF.
On the other hand, we found that the total activations were most frequent at 225 and 275 ms for saccharin. Area G was the most frequently activated by saccharin (17 of the 24 hemispheres examined), followed by the inferior part of the insular cortex and the hippocampus (three hemispheres respectively), and the frontal operculum and the parieto-occipital sulcus (one hemisphere respectively). No activation in the central sulcus was observed for saccharin sessions. Activation of area G was seen at the shortest latency and no other cortical region was activated at that latency.
The average latency of TOBF for NaCl was 155 ± 45.0 ms, and for saccharin 267 ± 91.7 ms. The difference in latency of the two tastants was 112 ms.
Thus, area G was most frequently activated by two different tastants, NaCl and saccharin,
with the shortest latencies. The results confirm our previous finding (Kobayakawa et
al., 1996b) that the transition between the insular cortex and the
operculum was the primary gustatory area, or area G. The activation of SI was observed only in
response to NaCl. This area, therefore, might be related to coding of some aspect of taste for
NaCl.
Precise location of area G
Figure 4 illustrates the locations of ECDs in area G, estimated in four sessions (two saccharin on the upper line and two NaCl sessions in the lower) of one subject. Figure 4b shows coronal sections passing through the center of anterior and posterior commissure. Parts A and C of the figure are left and right sagittal sections passing through the neighborhood of the insular cortex respectively.
|
In each part of the figure, the center of the cross is the average location of the ECDs in the first period when the ECDs were estimated with >80% goodness of fit. The lengths of the bars from the center represent 1 SD in each direction. The length of the each bar is <5 mm in most cases, except in one case for NaCl, in which it is 12 mm, and the estimated ECD moved from the bottom of the central sulcus to area G during this period.
In Figure 4b, the central sulcus (white arrow) is seen above area G. Since the central sulcus runs on the lateral surface of the cortex in the dorso-posterior to ventro-anterior direction, the MRI findings indicate that area G is situated posterior to the central sulcus; that is, area G is at the transition between the parietal operculum and the insula in the human. When the anterior end of the lateral sulcus was set as 0 and its posterior end as 100%, the foot of the central sulcus was located at 43.6 ± 6.3% and area G at 80 ± 19% from the anterior end of the lateral sulcus.
Estimation of cortical areas subsequently activated after area G
To examine the cortical areas activated sequentially after the first activation in area G in
either hemisphere, we located ECDs by finding the TOBFs at various peak latencies up to 1500
ms after the onset of stimulation. We found 176 activated regions in a total of 46 hemispheres
and analyzed them. In some sessions, ECDs were repeatedly located in the same cortical regions
of one hemisphere. Among the activated regions, the hippocampus was indicated in 22 time
points, the superior temporal sulcus in 23, the parahippocampal gyrus in 19, the frontal
operculum in 13 (including the anterior part of the insula in three), the central sulcus in nine, the
intraparietal sulcus in eight, the caudate nucleus in four, the inferior part of the insular cortex in
four and the cingulate gyrus in four (Figure 5). Activation of all the
regions examined was found in both hemispheres. Locations of activations in the central sulcus
were just above those in area G, and clearly lower than those produced by radial nerve
stimulation (Yang et al., 1993).
|
We investigated the latencies of activations in various regions. The average latency of TOBF in area G was 155 ms in response to NaCl and 267 ms in response to saccharin. To utilize all values obtained by NaCl and saccharin and to plot them on the same histogram, the differential latency of the two tastants in activating area G (267 – 155 = 112 ms) was subtracted from the latency for saccharin in each session. The latency distributions of activations of various regions are shown in Figure 6, where the fastest activations (blank bars) are differentiated from the later ones (hatched bars). As indicated in Figure 6 b–e, the activities were produced in various regions of the cortex with different latencies after area G. In particular, it was found that the fastest activations of the frontal operculum anterior to area G (in Figure 6b; mean 447 ± 320 ms) started at 286 ms behind those of area G (in Figure 6a; mean 161 ± 77.4 ms). It is also apparent that the activities of the parahippocampal gyrus, the hippocampus and the superior temporal sulcus were delayed, though clear modes were noticeable in the histogram for hippocampus (mode 350 ms, mean 393 ms) and superior temporal sulcus (mode 350 ms, mean 584 ms). The superior temporal sulcus was the last to be activated among the areas observed.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Relation between the bottom of the central sulcus (SI) and area G
In response to NaCl, a region in the central sulcus was first activated in seven of the 22
hemispheres, which was less frequent than in area G (n = 12). The region was located at
the bottom of the sulcus but not at the postcentral bank. On the other hand, the central sulcus was
rarely activated by saccharin. Thus, this region may not be related to both taste stimulations, but
only to some aspect of NaCl stimulation. The lower end of the central sulcus was once presumed
to be the primary gustatory cortex (Bornstein, 1940a, b), and it has been established that thalamic afferents from the parvicellular part of the
posterior ventromedial nucleus terminate at both areas G and 3 in squirrel monkeys (Benjamin and Burton, 1968) and macaque monkeys (Ogawa et al.,
1985; Pritchard et al., 1986). It is possible that
some sort of taste information is sent to area 3 at the bottom of the central sulcus, and that the
latter is activated with taste stimulation as fast as area G. In macaque monkeys, area 3 can be
activated by electrical stimulation of taste nerves with a latency as short as the activation of area
G (Ogawa et al., 1985).
Though we removed the limit of the latency of the first peak of the GEMs, say 200 or 400 ms depending upon taste stimulations, we found area G was the first activated in most cases. In a few cases, however, short latency activation was not noticeable in area G. This might be attributable to several factors, e.g. a high level of spontaneous activity in the brain which leads to a low signal/noise ratio, a lower level of consciousness such as drowsiness of subjects which blurts activation in area, or changes in the angles between the axes of the SQUID sensors and ECDs. Activation of area 3 after a short latency might interfere with that of area G, resulting in difficulty in separation of ECDs in the two neighboring structures. The same argument may be applied to detection of activation in area 3.
Source of difference in the initial peak latency between gustatory evoked magnetic changes to two tastants
The first peak latency of the GEMs for NaCl (155 ms) was much faster than that for
saccharin
(267 ms), giving a difference of 112 ms. Since the onset latency of potentials evoked by electrical
stimulation of chorda tympani is ~9-11 ms (Ogawa et al., 1985),
most of the latency of GEMs and probably the latency difference between the two tastants may
be
caused by the receptor mechanism of the receptor cells in the mouth.
Recently it was reported that different receptor mechanisms are involved depending on the
tastants
at the taste cell membranes (Roper, 1992): sodium activates receptors
directly
coupled with ionic channels, while sweet substances require intracellular second messengers
such as
G-protein to open ionic channels. Such differences yield a difference in latency in the generation
of
receptor potentials at the receptor cells, and ultimately in the onset latency of activation in area
G. Our
finding that the peak latency for salty taste was shorter than that for the sweet tastant was
consistent
with the report of Kobal (1985).
Possible differences in the activation of area G between NaCl and saccharin are yet to be studied.
Precise location of the primary gustatory area: whether it is in the frontal or parietal operculum
PET or fMRI studies (Hirsch et al., 1994; Kinomura et al., 1994 ; Small et al., 1997)
revealed
activation in the frontal operculum and the anterior insula. In addition, some of the investigators
presumed the frontal operculum and the anterior insula to be the primary gustatory cortex merely
in accordance with the position of area G in subhuman primates (Ogawa et al.,
1985; Pritchard et al., 1986). However, the
poor
temporal resolution of PET or fMRI makes it difficult to verify this assumption. On the other
hand,
MEG supplies data with high temporal resolution, allowing identification of the human primary
gustatory
area activated with the shortest latency. The frontal operculum and anterior insula were activated
at a
latency of 470 ms on average, longer than that of area G in the present MEG study. Thus it is
indicated
that the frontal operculum and anterior insula are not the primary gustatory area.
Our conclusion is that the primary gustatory area in human beings is located at the transition
between the parietal operculum and the insula, in contrast to that in subhuman primates. In the
human
being the gustatory cortex has shifted to the parietal cortex along the anteroposterior axis together
with
the oral representation zone of the somatosensory area in comparison with the location
in subhuman
primates. This is probably because of the enlargement of the frontal association area in the
process
of evolution: area G is located near the anterior end of the lateral sulcus in squirrel monkeys (Benjamin
and Burton, 1968), moves posteriorly towards the central sulcus but still remains
anterior
to it in
macaques (Ogawa et al., 1985; Pritchard et al.,
1986), and moves further backwards traversing the central sulcus to the parietal
cortex in
human beings. Such movement of sensory areas on the cerebral cortex along with phylogenetic
evolution is also known in other areas: the visual cortex is present at the lateral surface of
occipital
cortex in subhuman primates, but it turns the occipital pole to reside at the mesial surface of
occipital
cortex in the human brain because of the development of the parietal and temporal association
areas.
Gustatory related cortical areas other than area G
Table 1 summarizes cortical regions activated by gustatory
stimulation in
the present study, compared with those observed by PET (Kinomura et al.,
1994). Both findings were similar except for the lingual gyrus and thalamus, which
were only
found with PET. Activation of thalamus probably does not yield magnetic field changes large
enough to
be detectable by MEG due to its structure.
|
Since the frontal operculum and the anterior insula were activated at a latency longer than that of area G, they may serve as higher gustatory areas like the precentral opercular area (PrCO) and the orbitofrontal opercular area (OFO) in macaque monkeys (Ogawa, 1994
).
Small et al. (1997) observed activation in the orbitofrontal
cortex by
fMRI or PET and suggested it to be a higher gustatory area, as in macaques (Rolls,
1989). In our MEG
experiments, however, no ECD was detected in the orbitofrontal cortex. Probably the ECDs
generated
from the orbitofrontal cortex lie mainly in the radial direction to the SQUID sensors and escape
from
detection by MEG. Activity in the hippocampus and parahippocampus was observed in both PET and MEG studies. However, the spatial accuracy of hippocampal ECD locations is assumed to be poor in MEG because their location in the cranial cavity is as deep as the brainstem, which is not accurately located by MEG. Activity within these structures may be ascribed to the nature of the tasks imposed on the subjects. Subjects in the PET study were asked to discriminate NaCl from water and those in the MEG study had to report on the quality and intensity of taste they perceived.
Kettenmann et al. (1996) found magnetic field changes
in and
around the superior temporal sulcus for olfactory stimulation. Taking into consideration the fact
that this
is an area associated with various sensory modalities, it is highly possible that the STS is one of
the
areas associated with both gustatory and olfactory information.
The frequency with which activation in a given area was detected by MEG was dependent upon both the area concerned and the subject examined: area G was activated as the fastest activation site in almost all sessions, with a few exceptions in which activation in area G was missing or replaced by that in the central sulcus, whereas activation in the intraparietal sulcus and the frontal operculum was seen in only two subjects. When the activated areas were scrutinized for every subject, it was noticed that activation in the hippocampus was missing when the superior temporalsulcus or caudate nucleus were activated. It is not clear whether such individual variations in activation sites are due to individual variations in taste coding in the brain or failure of the algorithm to estimate ECDs in the two regions.
In the present study, we found repeated activations of a similar region, particularly area G and its surroundings, for a long time period, say 1500 ms, after stimulation onset. Such a finding could not be made by PET or fMRI with their poor temporal resolution, though it may indicate that area G and/or some other regions are repeatedly referred to even during a simple gustatory cognitive task as in the present study.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Benjamin, R.M. and Burton, H. (1968) Projection of tongue nerve afferents to anterior opercular–insular cortex in squirrel monkey. Brain Res., 7, 221-231.[Medline]
Bornstein, W.S. (1940a) Cortical representation of taste in man and monkey. I. Functional and anatomical relations of taste, olfaction and somatic sensibility. Yale J. Biol. Med., 12, 719-736.
Bornstein, W.S. (1940b) Cortical representation of taste in man and monkey. II. The localization of the cortical taste area in man and a method of measuring impairment of taste in man.Yale J. Biol. Med. , 13, 133-156.
Funakoshi, M. and Kawamura, Y. (1971) Summated cerebral evoked responses to taste stimuli in man. Electroenceph. Clin. Neurophysiol., 30, 205-209.
Grynszpan, F. and Geselowitz, B.D. (1973) Model studies of the magnetocardiogram. Biophys. J., 13, 911-925.
Hirsch, J., DelaPaz, R., Relkin, N., Victor, J., Bartoshuk, L., Norgren, R. and Pritchard, T.C. (1994) Localization of human gustatory cortex using functional magnetic imaging. Chem. Senses, 19, 486.
Kettenmann, B., Jousmi, V., Portin, K., Salmelin, R., Kobal, G. and Hari, R. (1996) Odorants activate the human superior temporal sulcus. Neurosci. Lett., 203, 143-145.[ISI][Medline]
Kinomura, S., Kawashima, R., Yamada, K., Ono, S., Itoh, M., Yoshioka, S., Yamaguchi, T., Matsui, H., Miyazawa, H., Itoh, H., Goto, R., Fujiwara, T., Satoh, K. and Fukuda, H. (1994) Functional anatomy of taste perception in the human brain studied with positron emission tomography. Brain Res., 659, 263-266.[ISI][Medline]
Kobal, G. (1985) Gustatory evoked potentials in man.Electroenceph. Clin. Neurophysiol. , 62, 449-454.[ISI][Medline]
Kobayakawa, T., Endo, H., Saito, S., Ayabe-Kanamura, S., Kikuchi, Y., Yamaguchi, Y., Ogawa, H. and Takeda, T. (1996a) Trial measurements of gustatory-evoked magnetic fields Electroenceph. Clin. Neurophysiol., suppl. , 47,133 -141.[Medline]
Kobayakawa, T., Endo, H., Ayabe-Kanamura, S., Kumagai, T., Yamaguchi, Y., Kikuchi, Y., Takeda, T., Saito, S. and Ogawa, H. (1996b) The primary gustatory area in human cerebral cortex studied by magnetoencephalography. Neurosci. Lett., 212,155 -158.[ISI][Medline]
Motta, G. (1959) I centri conrticali del gusto. Bull Sci. Med., 131, 480-493.
Ogawa, H. (1994) Gustatory cortex of primates: anatomy and physiology. Neurosci. Res., 20, 1-13.[ISI][Medline]
Ogawa, H., Ito, S. and Nomura, T. (1985) Two distinct projection areas from tongue nerves in the frontal operculum of macaque monkeys as revealed with evoked potential mapping. Neurosci. Res., 2, 447-459.[Medline]
Penfield, W. and Boldrey, E. (1937) Somatic motor and
sensory
representation in the cerebral cortex of man as studied by electrical stimulation. Brain, 60, 389-443.
Plattig, K.-H. (1991) Gustatory evoked brain potentials in humans. In Getchell, T.V., Doty, R.L., Bartoshuk, L.M. and Snow, J.B. (eds), Smell and Taste in Health and Disease. Raven Press, New York, pp. 277-286.
Prescott, J. (1989) Brain event-related potentials to primary tastes. In Kurihara, K., Suzuki, N. and Ogawa, H. (eds), Olfaction and Taste XI. Springer-Verlag, Tokyo, pp. 643-645.
Pritchard, T.C., Hamilton, R.B., Morse, J. and Norgren, R. (1986) Projections from thalamic gustatory and lingual areas in the monkey (Macaca fascicularis ). J. Comp. Neurol., 244, 213-228.[ISI][Medline]
Rolls, E.T. (1989) Information processing in the
taste
system of
primates. J. Exp. Biol., 146, 141-164.
Roper, D.S. (1992) The microphysiology of peripheral taste organs.J. Neurosci. , 12, 1127-1134.[Abstract]
Small, M.D., Jones-Gotman, M., Zatorre, J.R., Petrides, M. and Evans, C.A. (1997) A role for the right anterior temporal lobe in taste
quality recognition. J.
Neurosci., 17, 5136-5142.
Yang, T.T., Gallen, C.C., Schwartz B.J. and Bloom F.E. (1993)
Noninvasive somatosensory homunculus mapping in humans by using a large-array
biomagnetometer.Proc. Natl Acad. Sci. USA
, 90, 3098-3102.
Accepted December 16, 1998
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  M. G. Veldhuizen, G. Bender, R. T. Constable, and D. M. Small Trying to Detect Taste in a Tasteless Solution: Modulation of Early Gustatory Cortex by Attention to Taste Chem Senses, July 1, 2007; 32(6): 569 - 581. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Fontanini and D. B. Katz State-Dependent Modulation of Time-Varying Gustatory Responses J Neurophysiol, December 1, 2006; 96(6): 3183 - 3193. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Onoda, T. Kobayakawa, M. Ikeda, S. Saito, and A. Kida Laterality of Human Primary Gustatory Cortex Studied by MEG Chem Senses, October 1, 2005; 30(8): 657 - 666. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Ogawa, M. Wakita, K. Hasegawa, T. Kobayakawa, N. Sakai, T. Hirai, Y. Yamashita, and S. Saito Functional MRI Detection of Activation in the Primary Gustatory Cortices in Humans Chem Senses, September 1, 2005; 30(7): 583 - 592. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Kobayakawa, M. Wakita, S. Saito, N. Gotow, N. Sakai, and H. Ogawa Location of the Primary Gustatory Area in Humans and its Properties, Studied by Magnetoencephalography Chem Senses, January 1, 2005; 30(suppl_1): i226 - i227. [Full Text] [PDF]
|
|
|
|
|
|
B. P. Halpern Temporal Characteristics of Human Taste Judgements as Calibrations for Gustatory Event-related Potentials and Gustatory Magnetoencephalographs Chem Senses, January 1, 2005; 30(suppl_1): i228 - i229. [Full Text] [PDF]
|
|
|
|
|
|
A. Faurion, T. Kobayakawa, and B. Cerf-Ducastel Cerebral Imaging in Taste Chem Senses, January 1, 2005; 30(suppl_1): i230 - i231. [Full Text] [PDF]
|
|
|
|
|
|
C. Yamamoto, S. Takehara, K. Morikawa, S. Nakagawa, M. Yamaguchi, S. Iwaki, M. Tonoike, and T. Yamamoto Magnetoencephalographic Study of Cortical Activity Evoked by Electrogustatory Stimuli Chem Senses, March 1, 2003; 28(3): 245 - 251. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Mizoguchi, T. Kobayakawa, S. Saito, and H. Ogawa Gustatory Evoked Cortical Activity in Humans Studied by Simultaneous EEG and MEG Recording Chem Senses, September 1, 2002; 27(7): 629 - 634. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. M. Small, R. J. Zatorre, and M. Jones-Gotman Increased intensity perception of aversive taste following right anteromedial temporal lobe removal in humans Brain, August 1, 2001; 124(8): 1566 - 1575. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Barry, J. C. Gatenby, J. D. Zeiger, and J. C. Gore Hemispheric Dominance of Cortical Activity Evoked by Focal Electrogustatory Stimuli Chem Senses, June 1, 2001; 26(5): 471 - 482. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Cerf-Ducastel, P.-F. Van de Moortele, P. MacLeod, D. Le Bihan, and A. Faurion Interaction of Gustatory and Lingual Somatosensory Perceptions at the Cortical Level in the Human: a Functional Magnetic Resonance Imaging Study Chem Senses, May 1, 2001; 26(4): 371 - 383. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. M. Small, R. J. Zatorre, and M. Jones-Gotman Changes in Taste Intensity Perception Following Anterior Temporal Lobe Removal in Humans Chem Senses, May 1, 2001; 26(4): 425 - 432. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Otsubo and O. C. Snead Topical Review: Magnetoencephalography and Magnetic Source Imaging in Children J Child Neurol, April 1, 2001; 16(4): 227 - 235. [Abstract] [PDF]
|
|
|
|
|
|
D. H. Zald and J. V. Pardo Cortical Activation Induced by Intraoral Stimulation with Water in Humans Chem Senses, June 1, 2000; 25(3): 267 - 275. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||