| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD; and 2Oxford Centre for Functional Magnetic Resonance Imaging (FMRIB), John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom
Submitted 13 August 2002; accepted in final form 1 February 2003
 |
ABSTRACT |
|---|
|
|
|
INTRODUCTION |
|---|
|
;
Kawamura and Kare 1987) (after
sweet, salt, bitter, and sour; umami captures what is sometimes described as
the taste of protein). In fact, multidimensional scaling methods in humans
(Yamaguchi and Kimizuka 1979;
Yoshida and Saito 1969) have
shown that the taste of glutamate [as its sodium salt monosodium glutamate
(MSG)] cannot be reduced to any of the other four basic tastes. Specific
receptors for glutamate in lingual tissue with taste buds have been also
recently found (Chaudhari et al.
2000). Umami taste is found in a diversity of foods like fish,
meats, milk, tomatoes, and some vegetables, and is produced by the glutamate
ion and also by some ribonucleotides (including inosine and guanosine
nucleotides), which are present in these foods.
Besides their effects as unique tastants, umami substances have also been
reported to show synergism, i.e., when two umami substances are mixed, the
mixture effect is stronger than the sum of the effects given by the two
substances (Rifkin and Bartoshuk
1980; Yamaguchi
1967). The synergism characteristic of umami occurs when MSG is
combined with the ribonucleotide inosine 5'-monophosphate, IMP (or with
its guanosine equivalent). The result of combining these two taste stimuli is
a synergistic (i.e., supra-additive) effect in the subjective experience of
taste intensity (Rifkin and Bartoshuk
1980; Yamaguchi
1967). The synergism can be demonstrated psychophysically even
when appropriate ratio scales and correction for any nonlinearity in the
psychophysical function are used (Rifkin
and Bartoshuk 1980). Glutamate is high in concentration in foods
such as tomatoes, green vegetables, and fish, and is relatively high in human
breast milk; nucleotides are present in, for example, meat and in some fish
such as tuna (Yamaguchi and Ninomiya
2000). The mixture of these components underlies the rich taste
characteristic of many cuisines.
Some fibers in the taste nerves of rodents have been shown to have
selective responses to umami tastants such as MSG
(Ninomiya and Funakoshi 1987),
and in macaques, it has been shown that single neurons in both the primary
taste cortex in the insular/frontal opercular region and in the secondary
taste cortex in the orbitofrontal cortex are selectively activated by MSG
(Baylis and Rolls 1991;
Rolls 2000), glutamic acid, or
IMP (Rolls et al. 1996).
Nothing is known, however, about the cortical responses to umami substances
and their interactions in the human brain. We designed an event-related
functional MRI (fMRI) experiment to investigate these questions.
|
|
METHODS |
|---|
|
Ten healthy right-handed subjects (of which 6 were males) participated in the study. Written informed consent from all subjects and ethical approval were obtained before the experiment.
Stimuli and experimental design
Solutions consisted of 0.05 M MSG (the monosodium salt of
L-glutamic acid), 0.005 M IMP (which in this experiment was used in
a form without sodium ions), a combination of the two (MSGIMP made to contain
a concentration of 0.05 M MSG and 0.005 M IMP), or glucose (1.0 M). These
concentrations of MSG and IMP were chosen based on psychophysical
investigations we performed on human subjects that indicated that enhancement
was exhibited at these concentrations (see RESULTS). Furthermore,
these concentrations are close to a midpoint of the sensitivity curves of
single neurons to these stimuli in macaques
(Baylis and Rolls 1991;
Rolls et al. 1996). The
glucose was used to reveal the brain areas activated by an exemplar of a
prototypical type of taste, sweet, so that we could determine whether the
umami stimuli activated similar areas. Glucose was used as the exemplar
(rather than sucrose) because it has been used as the taste stimulus in many
previous neurophysiological and some neuroimaging studies
(O'Doherty et al. 2001b; Rolls
et al. 1989,
1990;
Yaxley et al. 1990), in which
the effects of feeding to satiety were often of interest to investigate the
brain mechanisms underlying appetite. Glucose was used in those studies
because it is rapidly absorbed and can act as a satiety signal without further
metabolism (Rolls 1999).
The experimental protocol consisted of an event-related interleaved design using these four taste stimuli as well as a tasteless control solution, which was delivered to the subject's mouth through five polythene tubes that were held between the lips. Each tube of approximately 1 m in length was connected to a separate reservoir via a syringe and a one-way syringe valve (supplied by Fisher Scientific).
At the beginning of each taste delivery, one of the four stimuli, chosen by
random permutation, was delivered in 0.75-ml aliquots to the subject's mouth.
Swallowing was cued by a visual stimulus after 10 s (following initial
instruction and training). After a random delay of 2–10 s, a tasteless
control solution (using the main ionic components of saliva: 25 mM KCl + 2.5
mM NaHCO3) (O'Doherty et al.
2001b) was administered in exactly the same way, and the subject
was cued to swallow again after 10 s. There was then a 2- to 10-s random delay
period until the next taste was delivered. The tasteless solution was used as
the comparison condition for the taste solution and allowed nontaste effects
such as somatosensory effects produced by liquid in the mouth and the single
tongue movement made to distribute the liquid throughout the mouth to be
controlled for. This taste trial was repeated for each of the four tastes, and
the whole cycle was repeated 12 times. It was a feature of the experimental
design that a tasteless solution was used to control for nontaste (including
somatosensory) effects of placing solutions in the mouth and that all
activations analyzed took this into account by subtraction. The tasteless
solution also provided a rinse for the preceding tastant.
During the experiment, subjects were asked to rate each of the taste stimuli for intensity using a visual analog scale anchored at –2 for very weak and +2 for very intense.
fMRI data acquisition
Images were acquired with a 3.0-T VARIAN/SIEMENS whole-body scanner at the
Centre for Functional Magnetic Resonance Imaging at Oxford (FMRIB), where 14
T2* weighted echo-Planar imaging (EPI) slices were acquired every 2 s (TR =
2). We used the techniques that we have developed over a number of years to
carefully select the imaging parameters to minimize susceptibility and
distortion artifact in the orbitofrontal cortex as described in detail by
Wilson et al. (2002). The
relevant factors include imaging in the coronal plane, minimizing voxel size
in the plane of the imaging, as high a gradient switching frequency as
possible (960 Hz), a short echo time of 25 ms, and local shimming for the
inferior frontal area.
The matrix size was 64 x 64 and the field of view was 192 x 192 mm. Continuous coverage was obtained from +60 (A/P) to –38 (A/P). Acquisition was carried out during the task performance, which lasted a total of 25 min and 28 s, yielding 764 volumes in total. A whole brain T2* weighted EPI volume of the above dimensions and an anatomical T1 volume with slice thickness of 6 mm and in-plane resolution of 0.75 x 0.75 mm was also acquired. The acquisition protocol used in this study is similar to that used in previous studies from our laboratory in which we used fMRI to image the orbitofrontal cortex.
fMRI data analysis
The imaging data were analyzed using SPM99 (Wellcome Department of
Cognitive Neurology, London). Preprocessing of the data used SPM99
realignment, reslicing with sinc interpolation, normalization, and spatial
smoothing with a 10-mm full width at half-maximum isotropic Gaussian kernel
and global scaling. The time series at each voxel was high-pass and low-pass
filtered with a hemodynamic response kernel. A general linear model was then
applied to the time course of activation of each voxel and linear contrasts
were defined to test the specific effects of each condition. Voxel values for
each contrast resulted in a statistical parametric map of the t
statistic, which was then transformed into the unit normal distribution (SPM
z). Group effects were assessed by conjunction analyses of
subject-specific contrasts. Reported P values based on this group
analysis for a priori regions of interest (i.e., the insula and the
orbitofrontal cortex) were corrected for the number of comparisons made within
each region (Worsley et al.
1996). Checks were performed using the estimated motion as a
covariate of no interest to rule out the possibility of the observed results
being due to motion-related artifact. Conjunction analysis
(Friston et al. 1999) was then
performed to reveal significant common activations for each effect of
interest.
|
|
RESULTS |
|---|
|
The taste intensity ratings (using a visual analog scale anchored at
–2 for very weak and +2 for very intense) taken in the experiment were
–0.75 ± 0.38 for IMP (mean ± SE), 0.46 ± 0.36 for
MSG, 0.92 ± 0.35 for MSG+IMP (MSGIMP), and 1.5 ± 0.50 for
glucose. Statistically it was shown that the intensity of the taste of umami
produced by the mixture of MSG and IMP was greater than that produced by the
MSG alone (even if the rating scales are taken as implying that the threshold
is at –2 on the rating scale used, paired t = 1.95, df = 9,
P < 0.04; 1-tailed). We refer to this as taste enhancement within
the domain of umami taste. Although the effect is not supralinear (or
"synergistic"; if the rating scales are taken as implying that the
threshold is at –2 on the rating scale used) on average across subjects
with the relatively small number of subjects used, supralinearity has been
found when larger psychophysical studies are performed
(Rifkin and Bartoshuk
1980).
Responses to umami taste
The effects of umami taste as produced by the prototypical stimulus 0.05 M MSG on cortical activation in the group analysis are shown in Fig. 1, row 3, the activations produced by IMP (0.005 M) are shown in Fig. 1, row 2, and the activations produced by the sweet tastant 1 M glucose are shown in Fig. 1, row 1. For all stimuli, activation of the insular-opercular taste cortex, which is the putative human primary taste cortex, and the orbitofrontal cortex were found. The activation produced by IMP shows that umami, even when the solution administered contains no sodium ions, activates these areas of the cerebral cortex.
|
Activation was also found by all these taste stimuli in the group analysis in a part of the rostral anterior cingulate cortex, as shown in Fig. 1, right, ACC, and discussed in the DISCUSSION.
To analyze whether there are areas of overlap of the activations produced
by the umami stimuli and the glucose used as a prototypical taste stimulus, we
show in Fig. 1, row 5, the
conjunction across stimulus conditions and subjects
(Friston et al. 1999) of the
effects produced by MSG, IMP, MSGIMP, and glucose. Activations (significant at
the P < 0.05 level, corrected for multiple comparisons) were found
at the rostral border of the insula, which by comparison with the macaque, is
likely to be the primary taste cortex, and in a part of the orbitofrontal
cortex, which is likely to be a secondary taste cortical area
(Baylis et al. 1994;
Rolls 2000). The analysis thus
shows that rather similar cortical areas were activated by the glucose and
umami taste stimuli, providing evidence that umami is specifically activating
regions that are demonstrably activated by classical taste stimuli.
To reveal the main effects produced by the three umami stimuli (umami
taste), we show in Fig. 2 the
conjunction across stimulus conditions and subjects
(Friston et al. 1999) of the
effects produced by MSG, IMP, and MSGIMP. Significant activations (at the
P < 0.05 corrected for multiple comparisons) were found in the
primary taste cortex (insula/operculum), putative secondary taste cortex
(caudolateral orbitofrontal cortex), and in a region of the rostral anterior
cingulate cortex.
|
The only significant difference in activation between glucose and umami
stimuli (as revealed by masking the statistical maps at P < 0.05)
was found in a ventral part of the rostral anterior cingulate cortex, which
was activated reliably by glucose but not by any of the umami stimuli. This
activation is shown in Fig. 1.
Given the role of this region of the ACC in motivation and emotion-related
behavior (Bush et al. 2000), it
is notable that the glucose stimulus was clearly rated as being the most
pleasant tastant to all subjects (glucose = 1.54 ± 0.17, MSGIMP = 0.5
± 0.31, MSG = 0.22 ± 0.32, IMP = –0.4 ± 0.32, with
+2 = very pleasant, –2 = very unpleasant). Comparisons performed
subsequent to an ANOVA showed that the glucose was significantly more pleasant
than any of the umami stimuli (P < 0.0001 in each case using a
post hoc pairwise t-test comparison).
Combination of MSG and IMP
Given the evidence that IMP (or its guanosine equivalent) and MSG can show
synergism psychophysically (Rifkin and
Bartoshuk 1980), we performed a contrast to investigate whether
any brain areas are significantly more strongly activated by the MSGIMP
combination than by the sum of the effects of MSG alone and IMP alone.
Figure 3 shows the results of a
stringent group analysis (based on the conjunction of activations in
individual subjects) (Friston et al.
1999) thresholded for the group conjunction test at P
< 0.001, which reveals a significant cluster with 30 voxels in the left
lateral orbitofrontal cortex (x,y,z = –44,34,–18;
z = 3.49). Furthermore, it was found that this activation is
significant using corrected statistics (P < 0.05 with a small
volume correction). Thus supra-linear additivity in the blood
oxygenation-level dependent (BOLD) signal was found in this anterior part of
the orbitofrontal cortex (Fig.
3). The supra-linear additivity in the BOLD signal is further
demonstrated by the time courses for each of the umami taste stimuli in this
significant cluster of voxels in the orbitofrontal cortex, as shown in
Fig. 4A. (The
timecourses across all 10 subjects are shown in
Fig. 4A with respect
to the tasteless solution.) This shows in these voxels a greater activation by
MSGIMP than by either alone. For comparison,
Fig. 4B shows the time
courses for the largest peak in the main effects comparison for umami taste
for the insular/operculum taste region shown in
Fig. 2, and it is evident that
the MSGIMP response was not especially prominent in the insular/opercular
taste cortex.
|
|
|
|
DISCUSSION |
|---|
|
The new findings described here in humans are supported by single-neuron
recordings in nonhuman primates (macaques), which have shown that umami
tastants activate single neurons in the primary and secondary taste cortices,
and that these neurons can be shown to be tuned to umami tastants in a way
that does not reflect their responsiveness to the sodium ion
(Baylis and Rolls 1991;
Rolls 2000;
Rolls et al. 1996). The
populations of neurons with responses to umami tastants such as MSG and IMP
were shown to be separate from the populations activated by the four other
prototypical tastants, sweet (glucose), salt (NaCl), bitter (quinine), and
sour (HCl) (Rolls et al.
1996).
Second, this study uncovered a part of the human orbitofrontal cortex that showed strong supralinear additivity in the BOLD signal produced by the combination of MSG and IMP (the MSGIMP condition) compared with the sum of the MSG and IMP BOLD signals. This region was just anterior (with a peak at y = 34) to the part of the orbitofrontal cortex showing effects in the main comparison between taste and tasteless solution (with a peak at y = 26).
In the light of the much discussed issue of hemispheric specialization
(Davidson 1992), it is
potentially of interest to note that, in the group analysis, the region of the
orbitofrontal cortex showing supra-linear additivity in the BOLD signal is on
the left side of the human brain. This is consistent with the suggestion
corroborated by clinical findings
(Pritchard et al. 1999) that
gustatory processing involves the left side of the human brain
(Craig 2002). However, it
should be noted that in some of the individual subjects, the supra-linear
additivity effects were also seen in the right orbitofrontal cortex. Further,
we note that, as shown in Figs.
1 and
2, there is very clear evidence
of the representation of taste bilaterally in the human brain.
The relative activations by the different umami tastants (MSG, IMP, and the
mixture) were similar in the insula/operculum and main area of the taste
orbitofrontal cortex (peak at y = 26), but were much larger to the
MSGIMP combination in the more anterior area (peak at y = 34), as
shown by the time course data shown in Fig.
4. This supra-linear change in BOLD signal for the mixture MSGIMP
compared with the MSG and IMP may reflect underlying supra-addivity effects in
the neuronal firing rates. Although there is some evidence that the BOLD
signal reflects the underlying neuronal firing rates
(Hyder et al. 2002;
Smith et al. 2002), there is
also evidence that the BOLD signal reflects in addition the inputs to and
processing within a brain area (Logothetis
et al. 2001).
The actual interaction between MSG and IMP may be expressed in part in the
taste receptors themselves, or there may be somewhat different receptors for
the different umami tastants (Chaudhari et
al. 2000; Lin and Kinnamon
1998), but in any case, the results of this study show that there
is a part of the human orbitofrontal cortex in which supra-linear additivity
shows up very strongly in the statistical analysis. The fact that this part of
the human orbitofrontal cortex statistically reflects supra-additive effects
between umami tastants evident in the BOLD signal makes it likely that
activity in this part of the orbitofrontal cortex is especially relevant to
the perceived sensation of umami taste and to the behavioral preferences for
umami taste. The role of this part of the human cerebral cortex in the taste
of umami could arise because it is able to provide a nonlinear amplification
of the MSG and IMP inputs already combined in the taste receptors, or it could
be that this part of the cortex is able to combine information from partly
separate umami channels to produce the large response to the combination of
MSG and IMP. This will be an interesting issue for future investigations.
The evidence described here that the orbitofrontal cortex represents umami
taste (literally "delicious" in Japanese) is consistent with other
evidence that the orbitofrontal cortex also represents information about the
reward value of other primary and secondary reinforcers including taste
(O'Doherty et al. 2001b;
Small et al. 1999), odor
(Zald and Pardo 1997;
Zatorre et al. 1992), and even
abstract monetary rewards (O'Doherty et
al. 2001a).
The activation of the cingulate cortex found in this study by the taste
stimuli is of interest. For example, we have found that pleasant olfactory
stimuli activate a far anterior part of the anterior cingulate cortex, with
aversive olfactory stimuli a slightly more posterior region
(de Araujo et al. 2002). The
far rostral anterior cingulate area activated by glucose shown in
Fig. 1 is close to the area in
which pleasant olfactory stimuli are represented. The cingulate area activated
by umami taste is in the anterior cingulate cortex, a little behind the region
activated by glucose (see Fig.
1). Further, the anterior cingulate cortex has been shown to be
activated by motivationally relevant affective stimuli including pleasant
touch (Rolls et al. 2003), and
there is evidence from animal studies that it is involved in a range of
motivationally oriented unconditioned behaviors and emotional learning
(Cardinal et al. 2002;
Devinsky et al. 1995). In
addition the anterior, ventral cingulate cortex (Brodmann's areas 24a/b and
25) in humans seems to be involved in the pathology of depression in humans,
as well as in the control of normal mood
(Drevets et al. 1997), and in
responding to emotionally significant stimuli, such as cocaine-associated cues
in drug abusers (Childress et al.
1999).
Other affective stimuli have been shown to activate nearby parts of the
anterior cingulate (Bush et al.
2000). However, it is not clear from these imaging studies whether
the cingulate activation reflects a sensory representation of the stimuli,
some more general affective or even arousal reaction to the stimuli, or some
behavioral response or response selection or response inhibition. We now have
reason to believe that the activation shown in this study of the human
cingulate cortex by taste stimuli reflects sensory inputs produced by the
tastants, because in studies now in progress in macaques, taste neurons with
classical taste cell properties in a corresponding region of the macaque
rostral anterior cingulate cortex are being found, and interestingly, these
cingulate taste cells are hunger dependent, and in particular, reflect
sensory-specific satiety in the same way as orbitofrontal cortex taste neurons
(Rolls et al. 1989).
|
|
ACKNOWLEDGMENTS |
|---|
|
|
|
FOOTNOTES |
|---|
Address for reprint requests: E. T. Rolls, Univ. of Oxford, Dept. of Experimental Psychology, South Parks Rd., Oxford OX1 3UD, UK (E-mail: Edmund.Rolls{at}psy.ox.ac.uk; URL: http://www.cns.ox.ac.uk).
|
|
REFERENCES |
|---|
|
Baylis LL, Rolls ET, and Baylis GC. Afferent connections of the orbitofrontal cortex taste area of the primate. Neuroscience 64: 801–812, 1994.
Bush G, Luu P, and Posner MI. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4: 215–222, 2000.[Web of Science][Medline]
Cardinal RN, Parkinson JA, Hall J, and Everitt BJ. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26: 321–352, 2002.[Web of Science][Medline]
Chaudhari N, Landin AM, and Roper SD. A metabotropic glutamate receptor variant functions as a taste receptor. Nature Neurosci 3: 113–119, 2000.[Web of Science][Medline]
Childress AR,
Mozley PD, McElgin W, Fitzgerald J, Reivich M, and O'Brien CP.
Limbic activation during cue-induced cocaine craving. Am J
Psychiatry 156:
11–18, 1999.
Collins D, Neelin P, Peters T, and Evans AC. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comp Ass Tomogr 18: 192–205, 1994.
Craig AD. Opinion: how do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3: 655–666, 2002.[Web of Science][Medline]
Davidson RJ. Anterior cerebral asymmetry and the nature of emotion. Brain Cogn 6: 245–268, 1992.
de Araujo IET, Kringelbach ML, and Rolls ET. Different areas of the human orbitofrontal and cingulate cortex activated by pleasant and unpleasant odors. Soc Neurosci Abstr 517.1, 2002.
Devinsky O,
Morrell MJ, and Vogt BA. Contributions of anterior cingulate cortex to
behaviour. Brain 118:
279–306, 1995.
Drevets WC, Price JL, Simpson JR, Jr, Todd RD, Reich T, Vannier M, and Raichle ME. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386: 824–827, 1997.[Medline]
Friston KJ, Holmes AP, Price CJ, Buchel C, and Worsley KJ. Multisubject fMRI studies and conjunction analyses. Neuroimage 10: 385–396, 1999.[Web of Science][Medline]
Hyder F,
Rothman DL, and Shulman RG. Total neuroenergetics support localized brain
activity: implications for the interpretation of fMRI. Proc Natl
Acad Sci USA 99:
10771–10776, 2002.
Kawamura Y and Kare M. Umami: A Basic Taste. New York: Marcel Dekker, 1987.
Lin W and Kinnamon SC. Responses to monosodium glutamate and guanosine 5'-monophosphate in rat fungiform taste cells. Ann N Y Acad Sci 855: 407–411, 1998.[Web of Science][Medline]
Logothetis NK, Pauls J, Augath M, Trinath T, and Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 412: 150–157, 2001.[Medline]
Ninomiya Y and Funakoshi M. Qualitative discrimination among `umami' and the four basic taste substances in mice. In: Umami: A Basic Taste, edited by Kare M. New York: Dekker, 1987, p. 365–385.
O'Doherty J, Kringelbach ML, Rolls ET, Hornak J, and Andrews C. Abstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci 4: 95–102, 2001a.[Web of Science][Medline]
O'Doherty J,
Rolls ET, Francis S, Bowtell R, and McGlone F. Representation of pleasant
and aversive taste in the human brain. J Neurophysiol
85: 1315–1321,
2001b.
Pritchard TC, Macaluso DA, and Eslinger PJ. Taste perception in patients with insular cortex lesions. Behav Neurosci 113: 663–671, 1999.[Web of Science][Medline]
Rifkin B and Bartoshuk LM. Taste synergism between monosodium glutamate and disodium 5'-guanylate. Physiol Behav 24: 1169–1172, 1980.[Medline]
Rolls ET. The Brain and Emotion. Oxford: Oxford, 1999.
Rolls ET. The representation of umami taste in the taste cortex. J Nutr S960–S965, 2000.
Rolls ET, Critchley H, Wakeman EA, and Mason R. Responses of neurons in the primate taste cortex to the glutamate ion and to inosine 5'-monophosphate. Physiol Behav 59: 991–1000, 1996.[Medline]
Rolls ET,
O'Doherty J, Kringelbach ML, Francis S, Bowtell R, and McGlone F.
Pleasant and painful touch are represented in the human orbitofrontal and
cingulate cortices. Cereb Cortex
13: 308–317,
2003.
Rolls ET, Sienkiewicz ZJ, and Yaxley S. Hunger modulates the responses to gustatory stimuli of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. Eur J Neurosci 1: 53–60, 1989.[Web of Science][Medline]
Rolls ET,
Yaxley S, and Sienkiewicz ZJ. Gustatory responses of single neurons in the
caudolateral orbitofrontal cortex of the macaque monkey. J
Neurophysiol 64:
1055–1066, 1990.
Small DM, Zald DH, Jones Gotman M, Zatorre RJ, Pardo JV, Frey S, and Petrides M. Human cortical gustatory areas: a review of functional neuroimaging data. Neuroreport 10: 7–14, 1999.[Web of Science][Medline]
Smith AJ,
Blumenfeld H, Behar KL, Rothman DL, Shulman RG, and Hyder F.
Cerebral energetics and spiking frequency: the neurophysiological basis of
fMRI. Proc Natl Acad Sci USA
99: 10765–10770,
2002.
Wilson J, Jenkinson M, de Araujo IET, Kringelbach ML, Rolls ET, and Jezzard P. Fast, fully automated global and local magnetic field optimization for fMRI of the human brain. Neuroimage 17: 967–976, 2002.[Web of Science][Medline]
Worsley KJ, Marrett P, Neelin AC, Friston KJ, and Evans AC. A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp 4: 58–73, 1996.[Web of Science]
Yamaguchi S. The synergistic taste effect of monosodium glutamate and disodium 5'-inosinate. J Food Sci 32: 473–478, 1967.[Web of Science]
Yamaguchi S and Kimizuka A. Psychometric studies on the taste of monosodium glutamate. In: Glutamic Acid: Advances in Biochemistry and Physiology, edited by Wurtman R. New York: Raven, 1979, p. 35–54.
Yamaguchi S and
Ninomiya K. Umami and food palatability. J Nutr
130: 921S–926S,
2000.
Yaxley S,
Rolls, ET, and Sienkiewicz ZJ. Gustatory responses of single neurons in
the insula of the macaque monkey. J Neurophysiol
63: 689–700,
1990.
Yoshida M and Saito S. Multidimensional scaling of the taste of amino acids. Jap Psychol Res 11: 149–166, 1969.
Zald DH and
Pardo JV. Emotion, olfaction, and the human amygdala: amygdala activation
during aversive olfactory stimulation. Proc Natl Acad Sci
USA 94:
4119–4124, 1997.
Zatorre RJ, Jones-Gotman M, Evans AC,and Meyer E. Functional localization and lateralization of human olfactory cortex. Nature 360: 339–340, 1992.[Medline]
This article has been cited by other articles:
|
|
 |
|
  E. T Rolls Functional neuroimaging of umami taste: what makes umami pleasant? Am. J. Clinical Nutrition, September 1, 2009; 90(3): 804S - 813S. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Grabenhorst, E. T. Rolls, B. A. Parris, and A. A. d'Souza How the Brain Represents the Reward Value of Fat in the Mouth Cereb Cortex, August 14, 2009; (2009) bhp169v1. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. S. Chambers, M. W. Bridge, and D. A. Jones Carbohydrate sensing in the human mouth: effects on exercise performance and brain activity J. Physiol., April 15, 2009; 587(8): 1779 - 1794. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. T. Rolls, F. Grabenhorst, and L. Franco Prediction of Subjective Affective State From Brain Activations J Neurophysiol, March 1, 2009; 101(3): 1294 - 1308. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Grabenhorst, E. T. Rolls, and A. Bilderbeck How Cognition Modulates Affective Responses to Taste and Flavor: Top-down Influences on the Orbitofrontal and Pregenual Cingulate Cortices Cereb Cortex, July 1, 2008; 18(7): 1549 - 1559. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. McCabe, E. T. Rolls, A. Bilderbeck, and F. McGlone Cognitive influences on the affective representation of touch and the sight of touch in the human brain Soc Cogn Affect Neurosci, June 1, 2008; 3(2): 97 - 108. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. T. Rolls, C. McCabe, and J. Redoute Expected Value, Reward Outcome, and Temporal Difference Error Representations in a Probabilistic Decision Task Cereb Cortex, March 1, 2008; 18(3): 652 - 663. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Grabenhorst, E. T. Rolls, C. Margot, M. A. A. P. da Silva, and M. I. Velazco How Pleasant and Unpleasant Stimuli Combine in Different Brain Regions: Odor Mixtures J. Neurosci., December 5, 2007; 27(49): 13532 - 13540. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 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]
|
|
|
|
|
|
T. Wifall, T. Faes, C. Taylor-Burds, J. Mitzelfelt, and E. Delay An Analysis of 5'-Inosine and 5'-Guanosine Monophosphate Taste in Rats Chem Senses, February 1, 2007; 32(2): 161 - 172. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. T Rolls Brain mechanisms underlying flavour and appetite Phil Trans R Soc B, July 29, 2006; 361(1471): 1123 - 1136. [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]
|
|
|
|
|
|
W. K. Simmons, A. Martin, and L. W. Barsalou Pictures of Appetizing Foods Activate Gustatory Cortices for Taste and Reward Cereb Cortex, October 1, 2005; 15(10): 1602 - 1608. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Kadohisa, E. T. Rolls, and J. V. Verhagen Neuronal Representations of Stimuli in the Mouth: The Primate Insular Taste Cortex, Orbitofrontal Cortex and Amygdala Chem Senses, June 1, 2005; 30(5): 401 - 419. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. T. Rolls Taste and Related Systems in Primates Including Humans Chem Senses, January 1, 2005; 30(suppl_1): i76 - i77. [Full Text] [PDF]
|
|
|
|
|
|
J. V. Verhagen, M. Kadohisa, and E. T. Rolls Primate Insular/Opercular Taste Cortex: Neuronal Representations of the Viscosity, Fat Texture, Grittiness, Temperature, and Taste of Foods J Neurophysiol, September 1, 2004; 92(3): 1685 - 1699. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. E. de Araujo and E. T. Rolls Representation in the Human Brain of Food Texture and Oral Fat J. Neurosci., March 24, 2004; 24(12): 3086 - 3093. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. T. Rolls, J. V. Verhagen, and M. Kadohisa Representations of the Texture of Food in the Primate Orbitofrontal Cortex: Neurons Responding to Viscosity, Grittiness, and Capsaicin J Neurophysiol, December 1, 2003; 90(6): 3711 - 3724. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. E.T. de Araujo, M. L. Kringelbach, E. T. Rolls, and F. McGlone Human Cortical Responses to Water in the Mouth, and the Effects of Thirst J Neurophysiol, September 1, 2003; 90(3): 1865 - 1876. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
TOP
ABSTRACT
INTRODUCTION
