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Identification of seminal works that built the foundation for functional magnetic resonance imaging studies of taste and food


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The evaluation of human brain processing of food and taste has been conducted for decades. The large number of articles published has advanced our understanding towards the neurobiology behind gustatory perception. By the approach of reference publication year spectroscopy, the present study identifies the publication years and the respective seminal works that received much more citations compared to other studies published in the same period. Results reveal that seminal works were written by multiple authors and focused on animal studies, psychophysical studies and development of questionnaire tools.
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CURRENT SCIENCE, VO L. 113 , NO. 7, 10 OCTOBER 2017 1 225
Identification of seminal works that built the foundation for functional
magnetic resonance imaging studies of taste and food
Andy Wai Kan Yeung
The evaluation of human brain processing of food and taste has been conducted for decades. The large
number of articles published has advanced our understanding towards the neurobiology behind gustatory
perception. By the approach of reference publication year spectroscopy, the present study identifies the pub-
lication years and the respective seminal works that received much more citations compared to other studies
published in the same period. Results reveal that seminal works were written by multiple authors and
focused on animal studies, psychophysical studies and development of questionnaire tools.
It is important to understand how the
brain processes taste and food informa-
tion, as excessive intake of calories may
lead to overweight and eventually obe-
sity. Functional magnetic resonance im-
aging (fMRI) studies have utilized the
latest technology to evaluate the human
brain and have provided vast amount of
data that were converted into insightful
informati on for a better understanding of
the neurobiological mechanism of taste
and food perception, such as taste inte n-
sity1 and quality2.
Bibliometric studies have identified
highly cited neuroscience articles in gen-
eral3– 5. However, the seminal works
that contributed to modern fMRI tast e
studies have yet to be identified and ap-
preciated by the scientific communit y.
Therefore, the aim of t his study was
to identify the publication years and
the respective seminal works that re-
ceived much more citations compared
to other papers published in the same pe-
Source of data
The study was based on data provided by
the Web of Science Core Collection
hosted by Clarivate Analytics. The
search string was: TS = (food OR taste
OR gustatory OR gustation OR sweet
OR sweetness OR salty OR saltiness OR
sour OR sourness OR bitter OR bitter-
ness OT umami OR savory OR savoury)
AND TS = (fMRI OR ‘functional mag-
netic resonance imaging’ OR ‘functi onal
MRI’). Onl y articles published in Eng-
lish were considered. The search yielded
933 articles. Reference lists of these arti-
cles served as the basis of analyses in the
present study.
Reference publication year
Full records and cited references from all
933 articles were imported into CREx-
plorer, a software developed based on the
concept of plotting references in docu-
ments along a timeline, and thus the plot
resembled a spectrogram6,7. The plot
consisted of two parts: a bar chart dis-
playing the raw frequency of cited refer-
ences published in each year, and a
spectrogram showing positive and nega-
tive peaks that indicated years when the
citation count deviated from the 5-yr
median. Positive peaks indicated higher -
than-average citation count received by
articles published in those years. Details
of the ten largest positive peaks were ex-
amined to identify the articles that had
the largest contributions.
Distribution of positive peaks
The ten largest positive peaks in terms of
difference from 5-yr median were loca-
ted between 1971 and 2007 (Figure 1).
There were two peaks in the 1970s, three
in the 1980s, one in the 1990s and four in
the 2000s.
Types of seminal works
The largest peak was in 2003: the fMRI
studies of taste and food have been cited
2753 times on the works published in
that year, which was more than the
median citation count during 2001–2005
by 183. In that year, Killgore et al. pub-
lished an fMRI paper reporting differen-
tial brain activation by photographs of
high- and l ow-calorie foods (Table 1).
Among the ten articles most cited from
their respective publi cation year, four
Figure 1. Results fr om r eference publi
cati on year spectroscopy. The referenc e lists of
933 selected articles were analys ed by CRExplorer. R eferences were sort ed b y public a-
tion year (x-
axis), and citation counts received by each publicat ion in the same year
were sum
mated ( left y-axis). T he spectrogram was gener ated by plot
ting the diff erence
in annual c itation count from its 5-yr median.
CURRENT SCIENCE, VO L. 113 , NO. 7, 10 OCTOBER 2017 1226
Table 1. Details of the ten largest positive peaks from the referenc e publication year spectrogram. The most cited article from
each of these peaks has been lis ted
Diff erence
from 5-yr
Total cita-
tion c ount
Most cited article of the r espec tive year
Article citation
count (AC)
Share (AC/
TC, %)
2003 183 2753 Killgore, W . D., Young, A. D., Femia, L. A., Bogorodzki, P.,
Rogowska, J. and Yurgelun-T odd, D. A ., Cortical and limbic
activation during viewing of high -versus low- calorie foods.
Neuroimage, 2003, 19, 1381–1394.
124 4.5
1971 87 135 Oldf ield, R. C., The assessment and analysis of handedness:
the Edinburgh inventor y. Neuropsyc hologia, 19 71, 9, 97–
60 44.4
2001 83 2346 Small, D. M., Zatorre, R. J., Dagher, A., Evans, A. C. and
Jones -Gotm an, M., Changes in brain activity related to eat-
ing c hocolate. Br ain, 2001, 124, 1720–1733.
154 6.6
2007 78 3032 Rothemund, Y., Pr euschhof, C., Bohn er, G., Bauknecht,
H.-C ., Klingebiel, R., Flor, H. and Klapp, B. F., Differential
activation of the dorsal striatum by hi gh-c alorie visual food
stimuli in obese individuals. Neuroimage, 2007, 37, 410–421.
149 4.9
1988 62 393 Talaraich, J. and Tournoux, P., Co-planar Stereotaxic Atlas
of the Human Brain, G eorge Thieme, St uggart, 1988.
98 24.9
1986 54 310 Scott, T. R., Yaxley, S., Sienkiewicz, Z. J. and Rolls, E. T.,
Gustatory respons es in the f rontal opercular cortex of the
alert cynomolgus monkey. J. Neurophys iol., 1986, 56, 876
32 10.3
2004 41 2611 Pelch at, M. L., Johns on, A., C han, R., V aldez, J. and
Ragland, J . D ., Images of desire: food-craving activation dur-
ing f MRI. Neur oimage, 2004, 23, 1486–1493.
76 2.9
1996 36 1063 Cox, R. W., AFNI: s oftwar e for analysis and visuali zation of
functional magnetic reson ance n euroim ages. Comput. Bio-
med. Res., 1996, 29, 162–173.
77 7.2
1983 31 199 Rolls, E. T., Rolls, B. J. and Row e, E. A., Sens ory-s pecif ic
and moti vation-specific satiety for the sight and taste of f ood
and w ater in man. Phy siol. Behav ., 1983, 30, 185–192.
14 7.0
1977 30 114 Murph y, C., Cain, W . S. and Bart oshuk, L. M., Mutual action
of taste and olf action. Sens . Process., 1977, 1, 204–211.
15 13.2
were related to human brain mapping,
three were development of methods for
data collection or analysis, two were
psychophysical studies and one was an
animal study. In terms of accounting for
the largest share of citati ons received by
works published in the respective year,
Oldfield’s seminal paper in 1971 that d e-
scribed an inventory to assess the hand-
edness of a subject accounted for 44. 4%
of citations.
Citation analyses have traditionally fo-
cused on the citation counts of selected
publications4. However, recent bibli-
ometric works have taken a new perspe c-
tive by evaluating the cited references of
selected publications6, 7. Marx and Born-
mann8 have published a comprehensive
overview on this approach, and explained
that one of the greatest advantages of this
is its ability to identify the historical
roots of the selected body of literature
that might be of decisive importance, but
conceptually heterogeneous. For in-
stance, Oldfield’s9 seminal work on the
Edinburgh inventory could be considered
as one of the most important tools to be
administered to subjects before they un-
derwent taste fMRI experiments, as
handedness was considered to influence
the hemispheric dominance of brain acti-
vations by taste10. However, the inven-
tory was not designed for taste or brain
studies and hence would not be included
into the body of literature to be analysed
by traditional search strategy aimed at
identifying taste and food fMRI studies
by relevant keywords. Another crucial
work related to methods is the book by
Talaraich and Tournoux11 depicting the
classical brain atlas derived from dissect-
ing a single human brain. It was digiti zed
and developed into a gold standard
stereotactic coordinate system for analys-
ing neuroimaging data, which was later
superseded by the more precise Montreal
Neurological Institute system12. The last
method identified was by Cox in 1996
that introduced the renowned neuroimag-
ing data processing software called
Analysis of Functional NeuroImages
(AFNI)1 3.
There were two psychophysical stud-
ies by Rolls et al.14 and Murphy et al.15
published in 1983 and 1977 respectively.
The former studied how satiety modu-
lated the pleasantness brought by the
sight and taste of food, whereas the latter
assessed the interactions between tast e
and smell during sensory evaluation.
They established the scientific theories
for designing relevant fMRI studies.
Similarl y, the animal study conducted by
Scott et al.16 reported a chemotopic or-
ganization of neurons (i.e. clustering of
neurons according to their sensitivity to
different tastes) in the frontal operculum
of two monkeys. This seminal work re-
vealed the organization of taste-responsive
CURRENT SCIENCE, VO L. 113 , NO. 7, 10 OCTOBER 2017 1 227
neurons in the taste cortex, and event u-
ally inspired a human fMRI study that
attempted to replicate a similar chemo-
topic organization17.
The four neuroimaging studies listed
in Table 1 are related to eating behaviour
and food choice. Killgore et al.18 and
Rothemund et al.19 studied the differen-
tial response of subject to viewing pho-
tographs of high- and low-calorie foods
and differential response to viewing pho-
tographs of high-calorie food between
obese and healthy subjects respectively.
Pelchat et al.20 studied how the brain ac-
tivated during food craving, and Small et
al.21 assessed the differential brain re-
sponse to eating chocolate during hungry
and satiated states. These studies probed
into the mechanisms of how the human
brain dictates eating behaviour. It should
be noted that Small et al.21 used positron
emission tomography (PET) for func-
tional imaging, which was largely super-
seded by fMRI due to the necessity
of radioactive tracers and the inherent
lower spatio-temporal resolution using
The present study highli ghted semi-
nal works from tools development, psy-
chophysical studies, animal studies and
earlier human neuroimaging st udies
that have driven the evolution of the
contemporary fMRI studies on taste and
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8. Marx, W . and Bornmann, L., Scientome t-
rics, 2016, 109, 1397–1415.
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9, 97–1 13.
10. Cerf, B., L ebihan, D., Moortele, P., Mac
Leod, P. and Fau rion, A., Ann. N.Y.
Acad . Sci., 199 8, 855, 575–578.
11. Talara ich, J. and Tournoux, P., Co-
planar Stereota xic Atlas o f the Human
Brain, George T hieme, Stuggart, 1988.
12. Evans, A. C., Collins, D. L., Mills, S.,
Brown, E., Kelly, R. and Peters, T. M.,
In Nuclear Science Sympo sium and
Medica l Imaging Conf erence, 1993 IEEE
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13. Cox, R. W., Comput. Biomed . Res.,
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A., Physiol. Be hav., 1983, 30, 185–19 2.
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L. M., Sen s. Pro cess., 1977, 1, 204–211.
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J. and Rolls, E. T., J . Neurophysio l.,
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imag e, 200 4, 23 , 1486–1493.
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Andy Wai Kan Yeung is at 1B39B, Oral
and Maxillofacial Radiology, Applied
Oral Sciences, Prince Philip Dental Hos-
pital, 34 Hospital Road, Sai Ying Pun,
Hong Kong.
e-mail: ndyeung@hku. hk
... Besides, complete record of the publications were also exported into CRExplorer (14), to identify the early seminal works (references) often cited by these papers. The default parameters were used to generate a "reference publication year spectroscopy" (RPYS), which was a figure that showed multiple waves along the timeline representing years the cited references had much more citations relative to preceding 2 and succeeding 2 years (i.e., deviation from 5-year median) (15)(16)(17)(18)(19)(20). Since the institution of the author only subscribed WoS back to year 1956, by using cited reference analysis here the author might be able to reveal important papers published before 1956. ...
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... Through analyzing the cited references from a pre-defined literature set, one can plot a "reference publication year spectroscopy" (RPYS). An RPYS shows multiple waves along the timeline and illustrates in which years the cited references received much more citations relative to preceding and succeeding years (and thus suggesting that seminal works were published in those years) [10][11][12][13][14]. The primary aim of this study was to identify the historical root of dental anxiety by RPYS and confirm if it was Coriat (1946). ...
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... The search yielded 3380 publications, between 1996 and 2019, which collectively had 69,570 cited references. The full record and cited references of the 3380 CAS publications were imported into the CRExplorer software, which is capable of identifying publications, within a predefined body of the literature, that are most frequently referenced [10][11][12][13][14] . The RPYS plot is composed of two parts: a bar chart that shows the raw frequency of cited references published in each publication year, and a waveform that shows positive and negative peaks which indicate publication years when the citation count largely deviated from its 5-yr median. ...
... Various handedness inventories have been introduced in the academic literature as tools to determine the handedness of subjects, and it was metaanalyzed that the left-handedness of the overall population was approximately 10% (Papadatou-Pastou et al., 2020). The most renowned handedness inventory is undoubtedly the Edinburgh handedness inventory introduced by Oldfield in 1971 (Oldfield, 1971), which was repeatedly identified as one of the most cited references in the neuroscience literature (Edlin et al., 2015;Fazio, Coenen, & Denney, 2012;Yeung, 2017;Yeung & Ho, 2018). ...
Subject handedness is an important parameter to be evaluated and accounted for in neuroscience studies dealing with laterality. The aim of this study was to survey for the details of how researchers administered the Edinburgh handedness inventory (EHI) to assess subject handedness. Web of Science and PubMed databases was searched on 3 August 2021 to identify functional magnetic resonance imaging (fMRI) articles published since 2013 using the EHI or citing Oldfield, the original paper that introduced the EHI. Articles not actually using the EHI and/or its variants were excluded. Two reviewers performed the screening independently and disagreements were solved by mutual consensus. Most of the 406 studies using the EHI did not report details regarding the number of items (94.1%), identity of items (96.1%), response format (97.0%), and cutoff score for right-handedness (87.2%). Items were found dropped or replaced, with response format and cutoff score changed without citing references that justified the modifications. A clearer reporting of the details of the EHI as an assessment tool for determining subject handedness should be encouraged.
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The fMRI usage in food research has recently witnessed a distinct proliferation. In this article, bibliometric network techniques are applied to examine the conceptual/intellectual structure of this domain based on 363 Scopus documents written by 2079 authors representing 35 nations and spanning almost thirty years (1992–2020). The study aims to reveal impactful authors, influential journals, collaboration networks and emerging trends in the domain. Additionally, keyword co-occurrence techniques are employed to scrutinize the field’s major schools of thought. Results show that the most impactful journals publishing fMRI usage in food research are Neuroimage, Proceedings of the National American Academy of Sciences of the United States of America (PNAS) and Neuroreport. Results also show that the author’s collaboration network in fMRI usage in food research is sparse. Furthermore, results related to collaborative networks between institutions and countries reveal a global “North-South” schism between developed and developing nations. Finally, the multiple correspondence analysis (MCA) applied to obtain the fMRI usage in the food research conceptual map reflects the depth and breadth of the field’s foci. Our analysis has far-reaching implications for aspiring researchers interested in fMRI usage in food research as the study retrospectively traces the evolution in research output over the last three decades, establishes linkages between the authors and articles, and reveals trending topics/hotspots within the broad theme of fMRI usage in food research.
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The responses of 165 single taste neurons in the anterior operculum of the alert cynomolgus monkey were analyzed. Chemicals were deionized water, blackcurrant juice, and the four basic taste stimuli: glucose, NaCl, HCl, and quinine HCl. Taste-evoked responses could be recorded from an opercular region that measured approximately 4.0 mm in its anteroposterior extent, 2.0 mm mediolaterally, and 3.0 mm dorsoventrally. Within this area, taste-responsive neurons were sparsely distributed such that multiunit activity was rarely encountered and neuronal isolation was readily achieved. Intensity-response functions were determined for nine cells. In each case, the lowest concentration of the dynamic response range conformed well to human electrophysiological and psychophysical thresholds for the basic taste stimuli. There was some evidence of chemotopic organization. Cells that responded best to glucose tended to be distributed toward the anterior operculum, whereas most acid-sensitive neurons were located more posteriorly. The proportion of cells responding best to NaCl peaked in the middle of the area, whereas quinine sensitivity was rather evenly distributed throughout. Opercular neurons in the monkey showed moderate breadth of sensitivity compared with taste cells of other species and at other synaptic levels. A breadth-of-tuning coefficient was calculated for each neuron. This is a metric that can range from 0.0 for a cell that responds specifically to only one of the four basic stimuli to 1.0 for one that responds equally to all four stimuli. The mean coefficient for 165 cells in the operculum was 0.67 (range = 0.12-0.99). Efforts were made to determine whether neurons could be divided into a discrete number of types, as defined by their responsiveness to the stimulus array used here. It was concluded that most taste cells may be assigned to a small number of groups, each of which is statistically independent of the others, but within which the constituent neurons are not identical. An analysis of taste quality indicated that the sweet and salty stimuli evoked patterns of activity that were significantly intercorrelated. Similarly, patterns representing HCl, quinine HCl, and water were related.
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We performed successive H(2)(15)O-PET scans on volunteers as they ate chocolate to beyond satiety. Thus, the sensory stimulus and act (eating) were held constant while the reward value of the chocolate and motivation of the subject to eat were manipulated by feeding. Non-specific effects of satiety (such as feelings of fullness and autonomic changes) were also present and probably contributed to the modulation of brain activity. After eating each piece of chocolate, subjects gave ratings of how pleasant/unpleasant the chocolate was and of how much they did or did not want another piece of chocolate. Regional cerebral blood flow was then regressed against subjects' ratings. Different groups of structures were recruited selectively depending on whether subjects were eating chocolate when they were highly motivated to eat and rated the chocolate as very pleasant [subcallosal region, caudomedial orbitofrontal cortex (OFC), insula/operculum, striatum and midbrain] or whether they ate chocolate despite being satiated (parahippocampal gyrus, caudolateral OFC and prefrontal regions). As predicted, modulation was observed in cortical chemosensory areas, including the insula and caudomedial and caudolateral OFC, suggesting that the reward value of food is represented here. Of particular interest, the medial and lateral caudal OFC showed opposite patterns of activity. This pattern of activity indicates that there may be a functional segregation of the neural representation of reward and punishment within this region. The only brain region that was active during both positive and negative compared with neutral conditions was the posterior cingulate cortex. Therefore, these results support the hypothesis that there are two separate motivational systems: one orchestrating approach and another avoidance behaviours.
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The neural systems regulating food intake in obese individuals remain poorly understood. Previous studies applied positron emission tomography and manipulated hunger and satiety to investigate differences in appetitive processing between obese and normal-weight individuals. However, it is not known whether manipulation of stimulus value may yield different neural activity in obese as compared to control subjects when intrinsic physiological states are kept constant. We used functional magnetic resonance imaging to investigate 13 obese and 13 normal-weight subjects and manipulated food motivation by presenting visual food stimuli differing in their caloric content and energy density. In contrast to controls, obese women selectively activated the dorsal striatum while viewing high-caloric foods. Moreover, in the high-calorie condition body mass index (BMI) predicted activation in the dorsal striatum, anterior insula, claustrum, posterior cingulate, postcentral and lateral orbitofrontal cortex. The results indicate that in obese individuals simple visual stimulation with food stimuli activates regions related to reward anticipation and habit learning (dorsal striatum). Additionally, high-calorie food images yielded BMI-dependent activations in regions associated with taste information processing (anterior insula and lateral orbitofrontal cortex), motivation (orbitofrontal cortex), emotion as well as memory functions (posterior cingulate). Collectively, the results suggest that the observed activation is independent of the physiological states of hunger and satiation, and thus may contribute to pathological overeating and obesity. Some of the observed activations (dorsal striatum, orbitofrontal cortex) are likely to be dopamine-mediated.
The need for a simply applied quantitative assessment of handedness is discussed and some previous forms reviewed. An inventory of 20 items with a set of instructions and response- and computational-conventions is proposed and the results obtained from a young adult population numbering some 1100 individuals are reported. The separate items are examined from the point of view of sex, cultural and socio-economic factors which might appertain to them and also of their inter-relationship to each other and to the measure computed from them all. Criteria derived from these considerations are then applied to eliminate 10 of the original 20 items and the results recomputed to provide frequency-distribution and cumulative frequency functions and a revised item-analysis. The difference of incidence of handedness between the sexes is discussed.
A package of computer programs for analysis and visualization of three-dimensional human brain functional magnetic resonance imaging (FMRI) results is described. The software can color overlay neural activation maps onto higher resolution anatomical scans. Slices in each cardinal plane can be viewed simultaneously. Manual placement of markers on anatomical landmarks allows transformation of anatomical and functional scans into stereotaxic (Talairach-Tournoux) coordinates. The techniques for automatically generating transformed functional data sets from manually labeled anatomical data sets are described. Facilities are provided for several types of statistical analyses of multiple 3D functional data sets. The programs are written in ANSI C and Motif 1.2 to run on Unix workstations.
Ten healthy subjects aged 20-25 including five right-handed and five left-handed according to the Dellatolas test participated in this functional magnetic resonance imaging (fMRI) study. A 3 Tesla whole-body MR scanner allowed echo planar imaging (EPI)-64 x 64 pixels, repetition time (TR) = 6 s, field of view (FOV) = 20 x 20 cm2--associated to acute anatomical localization of activated foci (256 x 256 pixels). Subjects were bilaterally stimulated with NaCl 85 mM, aspartame 2 mM, quinine hydrochloride 1 mM, glycyrrhizic acid 0.5 mM, guanosine monophosphate 1 mM and D-threonine 250 mM alternating with water. Stimuli and rinse were continuously pushed as bolus of 50 microliters every 3 s to the subject's mouth through microsyringes. We detected brain activated areas by correlation of the MR signal to an on-line perception profile recorded for each experiment and each subject with the finger-span method. We found most activations in the insula and the perisylvian region in agreement with previous electrophysiological studies on monkeys and clinical reports in humans. The superior part of the insula was bilaterally activated, in accordance with a whole-mouth stimulation. A striking lateralization related to handedness was found in a lower part of the insula. This projection in the dominant hemisphere, located in the same coronal plane as the upper insular activation, is the first evidence of a functional lateralization of brain processing involved in taste perception.
The present study investigated the functional magnetic resonance tomography correlates of taste perception in the human primary taste cortex. There is conflicting evidence in the literature about chemotopical organization in this brain region. The topography of hemodynamic activity elicited by five taste stimuli (sweet, sour, salty, bitter and umami) was analyzed on the flattened cortical surfaces of six single subjects. A high inter-individual topographical variability had to be noted. The results showed different patterns of hemodynamic activity for the investigated tastes with some considerable overlap. However, the taste specific patterns were stable over time in each subject. Such an individual taste specific pattern was also found for the umami taste within the primary taste cortex of each subject. These results suggest that input from glutamate receptors on the tongue might be processed in an exclusive way in the primary taste cortex rather than as a combination of inputs from the classical taste receptors.
  • A W K Yeung
  • H C Tanabe
  • J L K Suen
  • T K Goto
Yeung, A. W. K., Tanabe, H. C., Suen, J. L. K. and Goto, T. K., Neuroimage, 2016, 135, 214-222.
  • T K Goto
  • A W K Yeung
  • H C Tanabe
  • Y Ito
  • H.-S Jung
  • Y Ninomiya
Goto, T. K., Yeung, A. W. K., Tanabe, H. C., Ito, Y., Jung, H.-S. and Ninomiya, Y., Chem. Senses, 2016, 41, 623-630.
  • A W K Yeung
  • T K Goto
  • W K Leung
Yeung, A. W. K., Goto, T. K. and Leung, W. K., Curr. Sci., 2017, 112, 725-734.