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C International Psychogeriatric Association 2014

International Psychogeriatrics: page 1 of 12 


doi:10.1017/S1041610214000532

Disorders of taste cognition are associated with insular


involvement in patients with Alzheimers disease and vascular
dementia: Memory of food is impaired in dementia and
responsible for poor diet
...........................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................

Teiko Suto,1 Kenichi Meguro,1 Masahiro Nakatsuka,1 Yuriko Kato,1 Kimihiro Tezuka,1
Satoshi Yamaguchi1 and Manabu Tashiro2
1
2

Division of Geriatric Behavioral Neurology, CYRIC, Tohoku University, Sendai, Japan


Division of Nuclear Medicine, CYRIC, Tohoku University, Sendai, Japan

ABSTRACT

Background: In dementia patients, dietary intake problems may occur despite the absence of swallowing
problems. We investigated cognitive functions on food and taste in Alzheimers disease (AD) and vascular
dementia (VaD) patients.
Methods: Participants included 15 healthy controls (HC), 30 AD and 20 VaD patients. Food Cognition Test:
Replicas of three popular foods in Japan with no odors were presented visually to each participant, with the
instruction to respond with the name of each food. Replicas of food materials were subsequently presented
to ask whether they were included in these foods. Taste Cognition Test: Replicas of 12 kinds of foods were
presented to describe their expected tastes.
Results: The AD/VaD groups exhibited significantly lower scores on Food/Taste Cognition Tests compared
with the HC group. These scores correlated inversely with Mini-Mental State Examination (MMSE) scores in
the AD group. Decreased dietary intake was observed in 12 of the 50 patients; 8 of the 12 exhibited decreased
Taste Cognition Test scores, higher than that of the normal-intake patients. There was no difference in the
filter paper taste disc test between HC/AD/VaD groups. To test the hypothesis that the insula is associated
with taste cognition, two MMSE-matched AD subgroups (n = 10 vs. 10) underwent positron emission
tomography. Glucose metabolism in the right insula was lower in the low taste cognition subgroup. The VaD
patients with insular lesions exhibited impaired Taste Cognition Test findings.
Conclusions: It is important to consider the cognitive aspect of dietary intake when we care for dementia
patients.
Key words: Alzheimers disease, vascular dementia, taste, semantic memory, insula

Introduction
Eating can be a great pleasure but its failure can
lead to undernutrition. Further, eating disorder can
also decrease quality of life (QOL), particularly
among older adults (Leow et al., 2010). Appetite
depends on the taste of food, its visual impression
is also important. Appetite is affected by past
empirical memory of food and depends greatly
on sensation through the eyes, nose, and ears.
Therefore, the color and shape of food that is
Correspondence should be addressed to: Professor Kenichi Meguro, Division
of Geriatric Behavioral Neurology, CYRIC, Tohoku University, 2-1 Seiryomachi, Aoba-ku, Sendai 980-8575, Japan. Phone: +81-22-7177359; Fax:
+81-22-7177339. Email: k-meg@umin.ac.jp. Received 17 Dec 2013; revision
requested 18 Feb 2014; revised version received 22 Feb 2014; accepted 3 Mar
2014.

cooked in consideration of its visual impression


can have great effects on appetite. Dietary intake
decreases gradually with age and progression of
dementia is considered to be a factor contributing
to decreased dietary intake. We often experience
problems with eating behavior when caring for
dementia patients. However, taste in food can often
change and dietary intake decreases, even in the
absence of dysphagia.
Taste signals are first received at the taste buds
in the tongue, soft palate, and surrounding areas
controlled by the cranial nerves (VII, IX, X, XI) via
the thalamus (Nakamura et al., 2013). Thus, it is
not surprising that the sight of food is sufficient to
activate the insula (Simons et al., 2005). In addition
to food appearance activating gustatory processing
areas including the insula, insular responses to the

T. Suto et al.

sight and thought of food may be modulated by


the internal state of the body (Malik et al., 2008).
Dementia patients exhibit taste disorder. Steinbach
et al. (2010) used taste slip and an odor test using
Sniffin Sticks, and observed decreased olfaction
and taste in Alzheimers disease (AD) patients
compared with healthy volunteers.
Common approaches for patients with eating
disorders use easy-to-swallow food, which is
a gel containing water, protein, and fat, similar
to the normal biological constituents of food,
and has been produced to prevent aspiration
and eliminate pharyngeal residues by providing a
homogeneous and appropriate viscosity. Although
easy-to-swallow food has been established to
provide food in patients with swallowing disorders,
soft food has been invented with a focus on
maintaining food form while improving dietary
intake. It was developed as a new food type with
improved shape and appearance (Kuroda, 2001).
Food shape provides pleasure and satisfaction to
patients by bringing color and shape to the meal.
For example, most soft fish food are prepared
in the shape of a fish in conditions that are close
to the original state of the food ingredients. Soft
food is effective to not only improve QOL but
also to increase dietary intake for dementia patients
(Kuroda, 2001). Soft food has been developed
by focusing on form perception and vision-related
semantic memory. We hypothesized that cognitive
function related to eating may be damaged and
exhibit effects on eating behavior in dementia.
Regarding taste memory, there have been no
reports whether dementia patients have difficulty
in remembering taste of food, although transgenic
mice model showed impaired implicit taste memory
as well as explicit spatial memory (Janus et al.,
2004). AD patients have semantic memory
disorders. According to the hub-and-spoke
theory of conceptual knowledge (Rogers et al.,
2004), we considered the tests assessing the name
(hub) and the attributes or property (taste
spoke) of foods. The hub-and-spoke model
posits the existence of a pan-modal integrative
hub region, the anterior temporal lobe (Pobric
et al., 2010), as well as the modality-specific
knowledge region (spoke; Hoffman et al., 2012).
Patients can name something they can see but
cannot recognize the attributes. Regarding food,
these patients may name the food when eating a
meal but may not accurately recognize what kind
of food it is. Food attributes or properties include
the ingredients that were used as well as their
taste. Errors of food perception may cause the
experience of the food to be different from what
is expected, which may cause discomfort in patients
and affect eating behavior. Therefore, we focused

on the cognitive function of eating a meal and


hypothesized that dementia patients have a disorder
of taste-related semantic memory. The modalityspecific knowledge region associated with taste or
gustatory function has been investigated (Binder
and Desai, 2011). However, there have been no
studies of taste-related semantic memory, i.e. taste
cognition for AD and vascular dementia (VaD)
patients; although several previous studies have
conducted taste perception tests (Steinbach et al.,
2010).
In this study, we examined whether AD or
VaD patients accurately recognized both the
name of food and its taste property. Specifically,
patients who could accurately name the food might
not necessarily recognize its taste property. For
example, if a patient is able to name the curry
and rice but cannot imagine the appropriate
food ingredients, he/she would find it difficult to
accurately recognize curry and rice. Furthermore,
if a patient is suspected to have a disorder of taste
perception, he/she may not recognize a lemon to
be acid. To examine this state, we developed
questions concerning matching of food ingredients
of the meal with taste perception. Using the
question concerning matching with food ingredients
of the meal, we further confirmed whether patients
accurately responded with respect to common
foods, such as curry and rice. In the questions
related to taste cognition, a test of basic taste,
i.e. sweetness, saltiness, vinegar, and bitterness
was conducted. A taste perception test was also
administered to evaluate perception. To confirm
the hypothesis that the insula is associated with
taste cognition, vascular lesions were evaluated
extensively in VaD patients using magnetic
resonance imaging (MRI), and positron emission
tomography (PET) was used to assess AD patients.

Materials and methods 1


Institutional facility
The study was performed in a long-term care facility
in Tome, Miyagi prefecture, northern Japan. It is
a 150-bed institution including a 40-bed special
care unit for dementia. A dietician and a speech
therapist work there. All of the patients in the study
were institutionalized. Data from healthy adults
were obtained at a memory clinic in Osaki, Miyagi
prefecture, northern Japan. Tome and Osaki are
typical agricultural areas neighboring each other,
and people have similar eating habits.
Participants 1
Thirty AD patients (4 men and 26 women)
and 20 VaD patients (8 men and 12 women)

Food cognition in dementia

were studied. The inclusion criteria were: (1)


staying at the institute for more than three
months with no changes in drug treatments, (2)
AD was diagnosed according to the NINCDSADRDA (National Institute of Neurological and
Communicative Disorders and StrokeAlzheimers
Disease and Related Disorders Association) criteria
(McKhann et al., 1984) and VaD according
to the NINDS-AIREN (National Institute of
Neurological Disorders and StrokeAssociation
Internationale pour la Recherch et lEnseignement
en Neurosciences) criteria (Roman et al., 1993), and
(3) AD patients did not exhibit any cerebrovascular
diseases (CVDs), as shown by MRI (see below),
and VaD patients revealed CVDs in the responsible
areas causing cognitive decline.
The exclusion criteria were: (1) poor visual acuity
even when corrected to less than 10/20 for each eye,
or color blindness, as assessed by a ophthalmologist
independent of this study, (2) other diseases,
such as malignant tumor or infection, or systemic
diseases causing cognitive impairment, i.e. vitamin
B6/12 deficiency or hypothyroidism, (3) history
of schizophrenia or visual hallucination, (4)
dysphagia, as assessed by a speech pathologist, (5)
treatment with drugs that could affect appetite,
(6) aphasia or communication disorders, (7) MiniMental State Examination (MMSE; Folstein et al.,
1975) scores of 5 or less that could affect
understanding the test instruction, (8) disliking
the consumption of any of the test-meals (see
below) to exclude the possibility of a favor effect,
and (9) showing behavioral abnormalities, such
as delusion. Using the Behavioral Pathology in
Alzheimers Disease Frequency-Weighted Severity
scale (BEHAVE-AD-FW; Monteiro et al., 2001),
we extensively assessed delusional ideas to exclude
those manifesting delusion of poisoning, which
could affect the results (Nakatsuka et al., 2013).
Since we investigate the semantic memory on
taste in AD, patients with semantic dementia should
be excluded. The patients did not meet the criteria
of semantic dementia based on family interview,
neuropsychological assessment nor evidence of
temporal lobe atrophy in MRI, as confirmed by
the current diagnostic criteria (Gorno-Timpi et al.,
2011).
As for controls, 15 healthy controls (HC; 5
men and 10 women) were also studied. They were
cognitively healthy, based on the MMSE scores over
26 and observations by their families. They all had
no CVDs on MRI images and met the exclusion
criteria.
The mean (SD) ages in the HC, AD, and VaD
groups were 83.8 (7.7), 84.5 (6.6), and 84.9 (5.6)
years, respectively, showing no group differences.
The mean (SD) MMSE scores were 26.6 (2.5),

14.5 (6.0), and 14.2 (3.6) in the HC, AD, and


VaD groups, respectively, showing a significant
group difference (F = 25.478, p < 0.01). Post
hoc tests showed significant (p < 0.01) differences
between the HC and AD groups, and between
the HC and VaD groups. No ADVaD differences
were observed. According to the questionnaire
answered by the family, the participants exhibited
no remarkable differences in their daily lifestyle
related to cooking; i.e. they were all able to prepare
test-meals.
Written informed consent was obtained from
each of the participants and from the family of
those with dementia according to the Declaration
of Helsinki (BMJ 1991;302:1194). The study was
approved by the ethical committee of Tohoku
University Graduate School of Medicine, as well
as those of the respective institutes.
Magnetic resonance imaging
All participants underwent MRI (Achieva 1.5T,
Philips Electronics, Japan) at the hospital.
Combined axial T1 -weighted, T2 -weighted, and
FLAIR (fluid attenuated inversion recovery) images
were used to evaluate atrophy and CVD. Lesions
were considered to be CVD when they exhibited
low intensity on the T1 -weighted or FLAIR images
and high intensity on the T2 -weighted image at the
same location, with diameters 4 mm (Ishii et al.,
2007). The thalamus and insula, included in the
taste pathway, together with the frontal, temporal,
parietal, occipital lobes, basal ganglia were visually
assessed for the presence of CVDs. A boardcertified neurologist (M.N.) and a geriatrician
(S.Y.) assessed the findings independently and were
in agreement. In the event of a disagreement, a
board-certified senior neurologist (K.M.) made the
final decision.
Food Cognition Test
N A M I N G ( F O O D NAMING ) A N D M A T C H I N G
W I T H F O O D I N G R E D I E N T S ( F O O D MATCHING )

We developed an original Food Cognition Test, to


confirm whether three relatively common kinds of
food models, nigiri sushi, onigiri, and curry
and rice were understood (Figure 1). To exclude
the effect of odor, replicas were used. They were
realistic replicas prepared by a Japanese company
that provides the replicas for restaurants, and were
all matched with real foods by the participants.
The frequency and familiarity were high class
according to the Guidelines for nutrition care and
management in geriatric healthcare facilities (Kato
et al., 2005).
First, the naming (FOODNaming ) was tested
showing a replica model of curry and rice. A

T. Suto et al.

Figure 1. The upper line shows the three food models, curry and rice, onigiri, and nigiri sushi, whereas lower line represents the
food item models of potato, lemon, tomato, pork, onion, shishamo (sh), cabbage, and carrot. Upper models were used
for FOODNaming , and lower models were used for FOODMatching .

tester asked What is this? to a participant after


showing a food model. The participant was then
asked to confirm whether the food item shown
matched with the meal, i.e. was included in or
arranged as part of the meal (FOODMatching ).
The food item models of potato, lemon,
tomato, pork, onion, shishamo (fish),
cabbage, and carrot were presented separately
to the participant, the name was enquired and
the participant was asked whether the item was
included in the curry and rice. Similarly, the
tester presented the second meal model onigiri
(rice ball) and enquired about the name onigiri,
followed by the separate presentation of food item
models of tomato, salmon, lemon, pickled
Japanese plum, carrot, and takuan, enquiry
about the name and whether the item was included
in the onigiri. Finally, the tester presented the
third meal model nigiri sushi and enquired about
the name nigiri sushi, followed by the separate
presentation of food item models of tuna,
roast pork, salmon, tomato, squid, sweet
potato, bonito, orange, shrimp, octopus,
lotus, scallop, and sea bream, enquiry about
the name and whether the item was included in
the nigiri sushi. The number of correct answers
was scored. In FOODNaming , correct responses for

the total three kinds of meals and food earned 30


points, and in FOODMatching , correct answers for all
earned 27 points.
MATCHING WITH TASTE PERCEPTION
( T A S T E MATCHING )

Three respective items of food models showing


sweet, salty, sour, and bitter were
presented and participants responded with the
name and taste of 12 items in total (Figure 2).
The food models for sweet were rice
dumpling, cake, and soft cream, those for
salty were salted salmon roe, salted cod roe,
and salted squid, those for sour were lemon,
pickled Japanese plum, and orange, and those
for bitter were nigauri, butterbur sprout, and
green pepper, respectively. After it was confirmed
that the participant could identify the food, the
participant selected one of the tastes: sweet,
salty, sour, and bitter, described on a piece of
paper (TASTEMatching ). The order of presentation
of food was random in each test. The maximum
score was 12, as the total number of correct answers
for 12 items.
Perfect testretest reliability was observed for
the Food Cognition Tests for the HC groups and
the dementia patients who agreed to retest (n =

Food cognition in dementia

Figure 2. The food models for sweet were rice dumpling, cake, and soft cream, those for salty were salted salmon roe, salted
cod roe, and salted squid, those for sour were lemon, pickled Japanese plum, and orange, and those for bitter were nigauri,
butterbur sprout, and green pepper, respectively.

38). The remaining 12 dementia patients did not


agree to perform the retest. The Cronbachs
values were 0.84, thus, confirming the validity of
the evaluations.

Taste Perception Test


A clinical taste test was conducted using the
filter disc method established by otolaryngologists
(Tomita, 1986). The filter disc method is
quantitative, easily available, requires only a short
time and requires no specific training. The
measurement site is an area that is accurately
controlled by the cranial nerves VII, IX, X, and
XI (Tomita, 1986). We administered this Taste
Perception Test to eight healthy young adults to
examine four test sites on the tongue and confirmed
that there were no differences from the tongue
tip to the chorda tympani nerve field (data not
shown). Therefore, for the participants, the tests
were conducted at one site on the tip of the tongue,
in consideration of the burden and safety of these
tests.
Since it was preferable to choose substances
with four kinds of taste from the ones used
previously, to compare the test results with the
previous report by von Skramlik et al. (1956),
sugar was used for sweetness, salt for saltiness,

tartrate for vinegar, and quinine hydrochloride for


bitterness, respectively. Test procedures involved
placing a reagent of sweet, salty, sour,
and bitter on the tongue tip in sequence. The
participant identified the tastes by presenting a card
describing the taste as sweet, salty, sour, or
bitter. Before the next taste, the participant rinsed
his/her mouth with water to eliminate any residual
taste. The instructions for the test order were that
sweetness, saltiness, or vinegar could be selected as
the first taste, but that bitterness must be tested last.
The intensity of the taste was increased from Nos. 1
to 5 in order and the number of correct answers
was examined. The average taste of participants
with normal taste was Nos. 2 to 3. The results are
presented as the mean number of correct answers.

Dietary intake
Dietary intake was determined in accordance with
the Guidelines for nutrition care and management
in geriatric healthcare facilities (Kato et al., 2005).
The percentage of dietary intake was estimated by
calculating the mean for three days before the test;
summing the total energies of the main and side
dishes and between meal food intake. The scores
were null (0%) to complete intake as 10 (100%).
According to the guideline, scores less than 7 (70%)

T. Suto et al.

were defined as decreased dietary intake. For


example, when a patient took a complete intake
(100%) of a rice bowl, 40% intake of a side dish,
and a full intake (100%) of a snack, the total intake
was 70%, scored as 7.

Materials and methods 2


Participants 2
To test the hypothesis that the insula is associated
with taste cognition, 20 AD patients were selected
from among Participants 1 to undergo PET.
They were classified into two MMSE-matched
subgroups, i.e. the normal TASTEMatching AD
subgroup (10 women, mean MMSE = 11.5),
and the impaired TASTEMatching AD subgroup
(10 women, mean MMSE = 11.4), with the
groups showing normal and impaired scores
on TASTEMatching , respectively. There were no
significant group differences for MMSE scores.
Other semantic memory rather than taste cognition
was assessed with the naming of daily objects
included in the Western Aphasia Battery; two
subgroups did not show any differences (data
not shown). Using 18 F-fluorodeoxyglucose (FDG)PET, cerebral metabolic rate for glucose (CMRglc)
was calculated.
Positron emission tomography
The PET study was performed using a model SET
2400W scanner (Shimadzu, Japan) at the Cyclotron
Radioisotope Center, Tohoku University, at rest
with the eyes open. The PET room was kept
well-lighted and quiet. A short cannula was
placed in the median cubital vein for blood
sampling. A transmission scan (six minutes) was
performed with a 68 Ge/68 Ga external rotating line
source approximately 30 minutes after a bolus
intravenous injection of 185 mBq of FDG. Forty
minutes after the injection, a two-dimensional
(2D) emission scan (ten minutes) was performed
for quantitative analysis, followed by a threedimensional (3D) emission scan (five minutes).
Blood samples were collected 40 minutes after the
injection and 18 F radioactivity was measured using a
well-type scintillation counter. The plasma glucose
concentration was also measured 40 minutes after
the injection. A time activity curve was estimated
from the plasma radioactivity using a simplified
method (Wakita et al., 2000).
CMRglc parametric images were obtained from
each 2D image using an autoradiographic method
(Phelps et al., 1979). Basic image processing and
voxel-based data analysis were performed using
SPM2 (Statistical Parametric Mapping, 2002).
PET data were subjected to an affine and non-linear

spatial normalization to the standard Montral


Neurological Institute PET template of SPM2 and
to reslicing of 2 2 2 mm, followed by smoothing
using an isotropic Gaussian filter of 12 mm in
diameter. The anatomically standardized images
were then normalized by analysis of covariance
(ANCOVA) to a mean voxel count of 50. Subgroup
image differences were compared by paired t-test,
with significance accepted if the voxels survived
a corrected threshold of p < 0.001 for multiple
comparisons.

Results
Food Cognition Test
All healthy participants responded correctly for
FOODNaming , FOODMatching , and TASTEMatching .
Figure 3 presents the findings of the Food
Cognition Test. No significant group differences
were noted for FOODNaming ; however, significant
group differences were observed for FOODMatching
and TASTEMatching . The AD and VaD groups
showed lower scores than the HC groups; no AD
VaD difference was observed.
In the AD group, the correlation coefficient
between MMSE and FOODNaming was 0.630
(Pearson, p < 0.01), and that between MMSE
and FOODMatching was 0.666 (Pearson, p < 0.01).
The partial correlation coefficient between MMSE
and FOODMatching , using FOODNaming as a control
variable, was 0.379 (p = 0.056). In the VaD
group, the correlation coefficient between MMSE
and FOODNaming was 0.112 (p = 0.775) and
that between MMSE and FOODMatching was 0.078
(p = 0.842).
In the AD group, the correlation coefficient
between MMSE and TASTEMatching was 0.731
(Pearson, p < 0.01). The partial correlation
coefficient between MMSE and TASTEMatching ,
using FOODNaming , and Taste Perception Test
as control variables, was 0.455 (Pearson, p < 0.05),
which suggested that taste cognition correlated with
the MMSE independent of these variables. No such
correlations were observed in the VaD group.
Taste Perception Test
The Taste Perception Test results are shown in
Figure 4 (left part). There were no significant
group differences. In the AD group, a significant
correlation was observed between MMSE and
Taste Perception Test scores (Pearson, r =
0.581, p < 0.01); showing a decreasing tendency
of taste with disease severity, consistent with
the previous study (Steinbach et al., 2010). No
remarkable taste differences (sweet, salty, sour, and

Food cognition in dementia

Figure 3. (Colour online) Shown are the means with SDs. No signicant group differences were noted for FOODNaming . Signicant group
differences were observed for FOODMatching (ANOVA, F = 9.648, p < 0.01) and TASTEMatching (ANOVA, F = 8.746, p < 0.01). For both tests,
signicant differences were observed between the HC and AD groups (post hoc test, p < 0.01), and the HC and VaD groups (post hoc test,
p < 0.01); no ADVaD difference was observed. HC = healthy control; AD = Alzheimers disease; VaD = vascular dementia. : different
from HC.

Figure 4. (Colour online) Shown are the means with SDs. No group differences were noted for the Taste Perception Test and the dietary
intake scores. HC = healthy control; AD = Alzheimers disease; VaD = vascular dementia.

bitter) were noted for the correlations with MMSE


scores, or between the Taste Perception Test scores
and any scores on the Food Cognition Tests.
In the VaD group, there was no significant
correlation between MMSE and Taste Perception
Test scores (Pearson, r = 0.177, p = 0.648),
which may be influenced by the food properties
independent of the disease severity.
Dietary intake
The mean dietary intake scores are shown in
Figure 4 (right part). There were no significant
group differences. Twelve dementia patients among
the 50 patients exhibited decreased dietary intake,
with scores 7 (70%) or less. Eight of the 12
patients exhibited decreased TASTEMatching scores
(six of them also exhibited decreased FOODMatching
scores). For the remaining 38 dementia patients
with normal dietary intake, eight of them exhibited
decreased TASTEMatching scores (six of them also
exhibited decreased FOODMatching scores). There
was a significant difference (at 0.01 level) for the
impaired TASTEMatching between the decreased
dietary intake group (8/12) and the normal dietary
intake group (8/38; 2 -test, 2 = 6.75 > 1 2
(0.01) = 6.64).

Food with a different taste that was provided as a


normal meal (e.g. sweet salted salmon roe, sour rice
dumpling) was prepared and given to the patients to
test whether they could be convinced of such taste
for the possible improvement of dietary intake. One
AD patient (Case #1) and one VaD patient (Case
#2) exhibited improved dietary intake after such
intervention.
Case #1: a 94-year-old woman, diagnosed as AD
with an MMSE score of 10, showed a 40% decrease
in dietary intake. She provided good responses
to the FOODNaming and FOODMatching , but poor
responses to TASTEMatching . The Taste Perception
Test score was low. She responded that the
salted salmon roe was sweet in TASTEMatching .
She described her experience as delicious, after
actually eating the sweet salted salmon roe prepared
by the dietician. PET image of the bilateral insula
showed decreased CMRglc.
Case #2: an 81-year-old woman, diagnosed
as VaD with an MMSE score of 10, showed a
60% decrease in dietary intake (ID 3 in Table 1,
see below). She showed the same test pattern as
Case #1, but the Taste Perception Test score
was average. MRI revealed CVDs in the bilateral
basal ganglia and the insula, together with the
left thalamus. She responded that rice dumpling

8
T. Suto et al.

Table 1. Vascular lesions and Food Cognition Test in VaD


FRONTAL
LOBE

ID

TEMPORAL
LOBE

PARIETAL
LOBE

OCCIPITAL
LOBE

INSULA
R

THALAMUS

BASAL
GANGLIA

FOOD COGNITION TEST


F O O D Naming

F O O D Matching

T A S T E Matching

........................................................................................................................................................................................................................................................................................................................................................................................................................................................

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20

N
N
N
N
N
N
N
Dec
N
N
N
N
N
N
N
N
N
N
N
N

Dec
Dec
N
Dec
Dec
Dec
Dec
Dec
Dec
Dec
Dec
Dec
Dec
Dec
Dec
Dec
N
Dec
N
N

Dec
Dec
Dec
N
Dec
Dec
Dec
Dec
Dec
Dec
Dec
Dec
Dec
N
N
N
N
N
N
N

Dashed line between ID 10 and ID 11 separates the participants with and without insular lesions. The participants with insular lesions (right or left) showed impaired TASTEMatching (9/10),
compared with those without insular lesions (3/10) (2 -test, 2 = 5.21 > 1 2 (0.025) = 5.02).
VaD = vascular dementia; R = right; L = left; N = normal score; Dec = decreased score.
Basal ganglia include the putamen and the globus pallidus.
Presence of vascular lesion.

Food cognition in dementia

Figure 5. (Colour online) Glucose utilization of the right posterior


insula was signicantly lower (p < 0.001, corrected for multiple
comparisons) in the AD subgroup, which exhibited impaired Food
Cognition Test (matching with taste perception). The illustrated
voxels show the right insula: coordinates (x, y, z) = (46, 12, 18),
cluster size (voxels) = 154, z score = 4.88.

was sour in TASTEMatching . She described her


experience as delicious, after actually eating the
sour rice dumpling prepared by the dietician.
Neural basis: PET and MRI findings
A voxel-based analysis revealed that CMRglc in the
right insula was lower in the lower taste cognition
AD subgroup, compared with the higher test score
AD subgroup, as presented in Figure 5.
Table 1 presents the distribution of the vascular
lesions in the VaD patients. While there was
heterogeneity in the vascular lesions in the VaD
group, the participants with insular lesions (right
or left) showed impaired TASTEMatching , compared
with those without insular lesions. For both the
AD and VaD groups, there were no remarkable
findings for the anterior temporal lobes, which was
associated with the hub of semantic memory.

Discussion
Food Cognition Tests
In the HC group, the responses to FOODNaming ,
FOODMatching , and TASTEMatching were extremely
consistent. This suggested that participants had a
disorder if their responses were different from that
of the HC group.
In the AD group, responses to FOODNaming
and FOODMatching were less accurate than the
HC group, although the former was insignificant.
The correlation between MMSE and FOODNaming
suggested that correct naming could become dis-

turbed as disease severity increased. Furthermore,


the correlation between MMSE and FOODMatching
suggested that the attributes or property of the
meal decreased with the increase in severity. While
the probability of a partial correlation between
MMSE and FOODMatching , using FOODNaming as
a control variable, did not reach significance (p =
0.056), the possibility cannot be ruled out
that MMSE and FOODMatching exhibit a slight
correlation, independent of FOODNaming . However,
for the Taste Cognition Test, a significant partial
correlation was noted between the MMSE and
TASTEMatching , using FOODNaming , and Taste
Perception Test as control variables, showing that
taste cognition may be disturbed in the AD group.
This suggested that attributes or taste spoke
tended to decrease with disease severity, despite the
continued ability to respond using the correct names
(hub).
In the VaD group, responses to FOODNaming ,
FOODMatching , and TASTEMatching were also less
accurate than the HC group, similar to the AD
group. However, none of the correlations with
MMSE were significant. Disorder of cognitive
function varied in the VaD patients because the
lesions and symptoms were dependent on each
patient.
Taste Perception Test
In the AD group, a significant correlation was
observed between the MMSE and Taste Perception
Test scores. Taken together with the results above,
the severity of the AD neurodegenerative processes
could affect the bottom-up sensory process, as
well as the top-down cognitive process. Based on
such global dysfunction, specific dysfunction of
the specific region (e.g. the insula) may add and
modify the disorders of taste cognition in AD.
The lack of remarkable correlations between the
Taste Perception Test scores and any scores on
Food Cognition Tests indicated that the impaired
cognitive process could not be simply attributed to
the decreased bottom-up sensory process.
In the VaD group, however, there were no
correlations between the MMSE and any of the
tests scores, including Taste Perception. The results
suggested that for VaD, the regional role (e.g. the
insula) was important for taste cognition.
Semantic memory
AD patients have semantic memory disorders. As
described above, based on the hub-and-spoke
theory of conceptual knowledge (Rogers et al.,
2004), we developed original tests regarding the
name (hub) (FOODNaming ) and the attributes or
property (taste spoke) of foods (TASTEMatching ).

10

T. Suto et al.

Contrary to the report that semantic dementia


patients showed hub damage first followed
by visual spoke damage (Hoffman et al.,
2012), we revealed that the hub was relatively
spared in AD or VaD, whereas the taste hub
(TASTEMatching ) was impaired. Negative findings of
the anterior temporal lobe associated with the hub
(Pobric et al., 2010) supported this discussion.
FOODMatching might be associated with the action
semantics, since the knowledge of food ingredients
was easily retained for people who usually prepared
such meals. Since the participants disclosed no
remarkable difference on daily lifestyle according to
the questionnaire answered by their families, further
investigation is needed to clarify the point.
Several studies have reported a category-specific
naming disorder (living vs. non-living) in AD
(Martinaud et al., 2009). Although it remains
controversial, non-living things tended to be better
named than living things. Foods are made of
living things. Our patients did not exhibit
any differences in the naming scores between
FOODNaming and the daily objects (non-living
things) by the Western Aphasia Battery (WAB);
this category difference did not explain the results.
Furthermore, all of the test meals were familiar to
the participants and those who disliked eating any
of the test-meals were excluded. Thus, the results
were not attributed to the preference effect.
We first showed that AD or VaD patients
exhibited impaired taste-related semantic memory
(taste cognition), despite the fact that they could
name the meal and their taste perception was intact.

Neural basis
Impaired self-awareness of action or anosognosia for
hemiplegia may be associated with the right insula
lesion (Baier and Karnath, 2008). We previously reported that VaD patients improved their functional
status by a comprehensive physical and psychosocial
approach via right insula activation. Patients
with insular lesions cannot integrate external and
internal (physical) information well. Taste cognition
and taste perception were similar. The insula is
associated with taste, and its dysfunction is linked
with cognitive impairment. In addition, taste
cognition, a property of semantic memory, has
been shown to be damaged independently, which
suggests that taste cognition exists independent
of the entire semantic memory and may be damaged
specifically. We demonstrated that taste cognition
was specifically damaged in patients with both AD
and VaD, and that the strongest candidate culprit
lesion of the disorder of taste cognition was the
insula.

Decreased dietary intake was observed in Cases


#1 and #2, and both of them exhibited poor
responses to TASTEMatching . While this finding
does not immediately allow us to conclude that
taste cognition is involved in dietary intake, further
studies are necessary to investigate this possibility.
The importance of the orbitofrontal-insular-striatal
circuit in high-level regulation of feeding was
reported by the indication of binge eating rather
than a decrease in dietary intake (Woolley et al.,
2007). Voxel-based MRI analyses suggested that
there was damage in the right orbitofrontal-insularstriatal circuit. While our AD or VaD patients
did not exhibit binge eating, the suspected similar
neuronal basis should be investigated further.
A previous acute stroke study reported that
taste perception disorders occur frequently after
stroke, especially with the anterior circulation
subtype (Heckmann et al., 2005). For the right-left
difference, a recent stroke study (Stevenson et al.,
2013) reported similar effects for the tongue, as well
the insula, regarding the taste; the left insula group
responded poorer on tasks relative to the right insula
group. Our VaD participants were all in a chronic
state in the care institute, and no such laterality
was noted. Further investigation is needed to clarify
these points.
Dietary intake care based on cognitive aspects
Patients with good dietary intake were included
among the patients with decreased Taste Perception
Test scores and most of them ate normal food with
shape. Therefore, vision-related semantic memory
was considered important for each meal. Dietary
intake did not correlate significantly with MMSE,
naming, or taste cognition. A small number of
patients exhibited decreased dietary intake, which
prevented us from drawing appropriate conclusions.
Various approaches have been undertaken for
patients with reduced dietary intake in care facilities
in consideration of the meal patterns, swallowing
and food preference. However, dietary intake is
rarely improved. We suggest that in future studies,
disorder of taste cognition should be assessed in
dementia patients in actual care facilities.
The findings on Cases #1 and #2 provide
support to the as if somatic marker hypothesis
based on the deteriorated cognitive framework. As
these were observed in only two patients, further
investigation should be conducted to test this
hypothesis.
In general, the quality of experience is integrated
by bottom-up processes, reflecting characteristics
of the stimulus of the sensory organs, and topdown processes, associated with the individual
beliefs, desires, and expectations. Visual perception

Food cognition in dementia

is affected by prior conceptual structures, as


well as by characteristics of the visual stimulus
itself, and assessments of an individuals ability
are influenced by the expectations of his/her
ability, as well as by objective performance
measures. The taste studies provided sufficient
foundation for investigating the influence of
conceptual information on subjective experience
(Lee et al., 2006). Prior intellectual information
and subjective expectations can bias objective
informational search. Emotional experience is not
only based on the effect of physical internal organs,
like taste perception, but is also derived from explicit
recall of the experience (Damasio et al., 2000), like
the emotional experience of memory of taste (taste
cognition). This is supported by what we call the
as if somatic marker hypothesis (Damasio, 1994),
which could also explain the effect of the insula on
smoking relapse vulnerability in addicted smokers
(Janes et al., 2010). We can discuss the possibility
that the cognitive framework of the dementia patient
was deteriorated as Cases #1 and #2.
Limitations and future issues related to this
study
The Taste Perception Test using the filter disc
method is usually conducted based upon the tongue
site. However, in this study the test was conducted
at only one site on the tip of the tongue. This
method must be evaluated further, to confirm
the uniformity of the taste response. Furthermore,
the taste cognition test should be conducted
concomitant with olfactory tests. However, while
the test required a long time to administer, the
taste perception was focused and no olfactory tests
were conducted in this study, in consideration of
the burden to the patients. In future investigations,
the contents of the tests should be redesigned to
improve these aspects.

Conclusions
We administered an original Food Cognition Test
and Taste Cognition Test using food models. The
latter examined how the participants perceived
the taste after seeing the food. Some of the
dementia patients exhibited disorder of taste
cognition in the absence of any taste perception
disorder. Furthermore, this disorder might occur
independent of disorders of naming. It was
suggested that that taste cognition, the most
important property of food that is seen, was
specifically damaged. PET findings of the AD
group, taken together with the MRI results of
the VaD group, suggested that disorder of taste

11

cognition was highly related to damage of the


insular cortex.

Conict of interest
None.

Description of authors roles


K. Meguro designed the study, supervised the data
collection, and wrote the paper. T. Suto, Y. Kato,
K. Tezuka, S. Yamaguchi collected the data and
assisted with writing the paper. M. Nakatsuka was
responsible for the statistical design of the study and
for carrying out the statistical analysis.

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