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COMMENTARY
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-
riod.
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
spectroscopy
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.
COMMENTARY
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
Year
Diff erence
from 5-yr
median
Total cita-
tion c ount
(TC)
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–
113.
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–
890.
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.
Discussion
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
COMMENTARY
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
PET22.
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
food.
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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
