Psychological Science
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Sensory-Specific Satiety Is Intact in Amnesics Who Eat Multiple Meals
Suzanne Higgs, Amy C. Williamson, Pia Rotshtein and Glyn W. Humphreys
Psychological Science 2008 19: 623
DOI: 10.1111/j.1467-9280.2008.02132.x
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PS YC HOLOGICA L SC IENCE
Research Report
Sensory-Specific Satiety Is Intact
in Amnesics Who Eat Multiple
Meals
Suzanne Higgs, Amy C. Williamson, Pia Rotshtein, and Glyn W. Humphreys
University of Birmingham
ABSTRACT—What
is the relationship between memory and
appetite? We explored this question by examining preferences for recently consumed food in patients with amnesia.
Although the patients were unable to remember having
eaten, and were inclined to eat multiple meals, we found
that sensory-specific satiety was intact in these patients.
The data suggest that sensory-specific satiety can occur in
the absence of explicit memory for having eaten and that
impaired sensory-specific satiety does not underlie the phenomenon of multiple-meal eating in amnesia. Overeating
in amnesia may be due to disruption of learned control by
physiological aftereffects of a recent meal or to problems
utilizing internal cues relating to nutritional state.
Reports that amnesic patients eat multiple meals suggest that
memory for recent eating may be one factor controlling food
intake (Hebben, Corkin, Eichenbaum, & Shedlack, 1985; Rozin,
Dow, Moscovitch, & Rajaram, 1998). In addition to exhibiting
anterograde amnesia due to bilateral hippocampal damage, the
neuropsychological patient H.M. reported problems in identifying his state of food repletion and depletion (Hebben et al.,
1985). He also ate a second meal within 1 min of finishing the
first. Rozin et al. (1998) found that 2 amnesic patients with hippocampal damage similar to that of H.M. consumed two lunches
in quick succession, and usually began to consume a third meal
if it was offered. Furthermore, reminding neurologically intact
participants of the lunch that they ate earlier on the day of a
study inhibits their subsequent consumption of snacks, relative
to consumption in a condition in which participants are reminded of the lunch they ate the previous day (Higgs, 2002).
Address correspondence to Suzanne Higgs, University of Birmingham, Edgbaston, Birmingham, B15 2TT, England, e-mail: s.higgs.1@
bham.ac.uk.
Volume 19—Number 7
Despite these intriguing findings, little is known about the
mechanisms underlying multiple-meal eating in amnesia.
Because the procedure in previous studies has been to offer the
same meals in succession, one explanation is that the usual
decline in palatability and intake of a food that has been eaten to
satiety is disrupted in amnesia (Rolls, Rolls, Rowe, & Sweeney,
1973). In the first experiment reported here, we tested whether 2
densely amnesic patients with bilateral damage to the medial
temporal lobes reported such sensory-specific satiety. This experiment also provided an opportunity to test whether explicit
memory of having recently eaten a food is required for the expression of sensory-specific satiety (Rozin et al., 1998). In our
second experiment, we checked whether our patients ate multiple meals as they were offered. Finally, to control for the
possibility that the amnesic patients had deficits in taste perception or were biased in their use of our rating scales, in our
third experiment we assessed their hedonic ratings of yogurt
samples differing in sweetness.
METHOD
Test of Sensory-Specific Satiety in Amnesia
Participants
Two amnesic patients (S.P. and G.A.) and 8 control subjects
(4 men and 4 women; age range 5 53–58) participated in this
experiment. Both patients had lesions that included medial
temporal and frontal lobe structures (see Fig. 1). G.A. was formerly a professional musician, and S.P. had been a bank manager. Both had a category-specific recognition deficit for living
things following infection from herpes simplex encephalitis
(Humphreys & Riddoch, 2003), and both were anosmic. Each
patient completed neuropsychological testing, which confirmed
a selective impairment in long-term memory for new material
disproportionate to deficits in general cognitive or intellectual
functioning (see Table 1). All procedures were approved by the
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623
Sensory-Specific Satiety in Amnesics
Fig. 1. Common areas of brain damage for the 2 patients. The right hemisphere is on the right. Common areas of damage include anterior and
middle cingulate (bilateral), superior medial frontal cortex (left), middle orbitofrontal cortex (right), rolandic operculum (bilateral), putamen
(right), amygdala (bilateral), insula (bilateral), parahippocampal region and hippocampus (bilateral), superior temporal cortex (bilateral), temporal pole (right), and fusiform gyrus (right). From left to right, the slices run from lowest to highest; the position of the slices is shown on the right.
Ethics Committee of the School of Psychology, University of
Birmingham, and the participants gave informed written consent.
Procedure
Sensory-specific satiety was measured by comparing the change
in liking and desired intake of a food that was eaten to satiety
with the change in liking and desired intake of foods that were
only sampled. Participants rated four samples before and after
consuming one of the foods (sandwiches) as lunch. As in previous studies, ratings of the sampled foods were averaged for
comparison with the food eaten to satiety.
Testing took place individually between 12:00 and 2:00 p.m.
On arrival, participants rated their feelings of ‘‘hunger,’’ ‘‘fullness,’’ and ‘‘thirst’’ using 100-mm line scales (anchors were not
at all, on the left, and very, on the right). They then tasted the four
samples and rated their liking for and desired intake of each,
using similar scales. The questions were ‘‘How much do you like
the taste of this food?’’ ‘‘How much do you like the texture of this
food?’’ and ‘‘How much of this food could you eat?’’ For the first
two questions, the anchors on the rating scales were not at all, on
the left, and extremely, on the right; for the third question, the
anchors were nothing at all, on the left, and a large amount, on
the right. The foods, which were selected for their different
sensory properties, were (a) a quarter of a chocolate-chip cookie
(Cookie Coach Co., Manchester, England), (b) 2 tablespoons of
rice pudding (Muller rice; Muller Dairy, Shrewsbury, England),
(c) two potato chips (Walkers Crisps, Leicester, England), and
(d) one eighth of a sandwich made from two standard slices of
bread (ham or chicken; Ginsters, Cornwall, England). The
samples were served individually as small portions, in a random
order. A glass of tap water was provided for participants to sip in
between making their ratings. A separate piece of paper was
used for rating each food, and participants were instructed to eat
all of each sample.
After removal of the sample foods, participants consumed
sandwiches to satiety. Two sandwiches (four slices of bread) were
cut into quarters to provide eight portions (approximately 40 g
and 96 Kcal per portion). Once the participants had helped
themselves to as many portions as they wanted, the sandwiches
were removed. Five minutes later, a second set of sample foods
was presented, and participants once again rated their liking for
and desire to eat each sample, as well as their hunger and
fullness and thirst. The sample foods were then removed. Five
624
minutes later, the patients were asked if they had just eaten. They
were informed that they had in fact just eaten and were asked to
select the food (from a list of the four foods sampled) that they had
eaten in a larger quantity than the others. The patients were
tested in three (S.P.) or seven (G.A.) sessions separated by at least
a week. Each session was identical. S.P. attended fewer sessions
because he had to travel some distance to be tested. The control
subjects were tested on one occasion each.
A follow-up session with G.A. tested the generalizability of
the results to different foods. The procedure was the same as that
just described, but the foods were sandwiches, apple slices, biscuits, and cheese pastries. The cheese pastries were consumed
to satiety as lunch.
Multiple-Meal Study
In a separate study, participants were served two lunches, separated by 15 min. Each lunch consisted of eight portions of tuna
or ham sandwiches (Ginsters, Cornwall, England; approximately
40 g and 96 Kcal per portion) and four portions of cake (Lemon
Cake, The Handmade Flapjack Co., Coventry, England; approximately 35 g and 148 Kcal per portion). Participants helped
themselves to as much food as they wanted. When they had
finished eating, evidence that a meal had been consumed was
removed. Fifteen minutes later, an identical meal was presented,
and the participants were asked to help themselves to as much as
they wanted. Before and after lunch, participants completed line
rating scales assessing their hunger and fullness. G.A. and S.P.
were tested twice each, and 4 age-matched, male control subjects were tested once.
Hedonic-Ratings Study
Using the 100-mm line scales described previously, participants
in the third experiment (G.A., S.P., and 2 age-matched, male
control subjects) rated their liking for the taste of five samples of
yogurt differing in sweetness. Sucrose (Tate and Lyle, United
Kingdom) was added to plain full-fat yogurt (Coberco, Arhem,
The Netherlands) at the following concentrations: 1, 5.9, 10, 17.6,
and 30% sucrose/yogurt by weight. The 10% concentration was
equivalent to the sugar concentration of commercially available flavored yogurts. Fifty-milliliter portions of yogurt were
served in opaque plastic cups and presented in a random order.
Participants consumed enough to be able to make the ratings
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Volume 19—Number 7
S. Higgs et al.
TABLE 1
Results of Neuropsychological Testing of the Patients
Measure
Visual short-term memory
Corsi block test
Verbal short-term memory
Digits forwards
Digits backwards
Sentence Repetition
(PALPA Test 55; N 5 60)
Word Repetition (varying
number of syllables,
PALPA Test 30; N 5 24)
Long-term memory
WRM Words (N 5 50)
WRM Faces (N 5 50)
WMS Logical Memory
WMS Visual Reproduction
Executive function
Brixton test (N 5 54)
Stroop test (N 5 112)
WCST
NART IQ equivalent
Comprehension (Synonym
Matching, PALPA Test 50)
High imageability (N 5 60)
Low imageability (N 5 60)
Smell
UPSIT
G.A.
S.P.
Control
data
5
7
5 (2)
7
4
7
6
7 (2)
5 (2)
57
60
60 (0)
24
24
24 (0)
24
31
2
6
31
33
5
5
45.3 (3.4)
44.3 (3.5)
22.5 (6.3)
29.0 (5.2)
41
11
48 (3)
103
42
92
98 (6)
110
50a
112 (0)
67.5 (5.5)
100a
60
58
60
57
60 (0)
60 (0)
10.0
14.0
30.8
these averages and the control subjects’ ratings were analyzed
by a two-way analysis of variance with rating type (pleasantness
of taste, pleasantness of texture, desire to eat) and food type
(food eaten to satiety, sampled food) as within-subjects factors
and group (patient, control) as a between-subjects factor. Intake
of the sandwiches as lunch and change in rated appetite and
thirst were averaged for the patients across sessions and compared with the control data using a two-tailed t test. Intake in the
multiple-meal study was analyzed by t test.
RESULTS
(one or two spoonfuls) and rinsed their mouths with water in
between samples.
Test of Sensory-Specific Satiety in Amnesia
The patients could not remember having eaten when questioned
after the second set of ratings, and on average correctly identified the food eaten in a larger quantity 38% of the time. Nevertheless, the main effect of food type was significant, F(1, 16) 5
6.6, p < .05; both the patients and the control subjects showed a
decline in rated liking for and desire to eat the food eaten to
satiety relative to the sampled foods. There was no effect of
group, F(1, 16) 5 0.038, p 5 .5, or of rating type, F(2, 32) 5 0.7,
p 5 .5, nor were there any significant interactions (all ps > .3).
Figure 2 shows that the rated liking for and desire to eat the
sandwiches decreased after they had been consumed as lunch,
but that the rated liking for and desire to eat the other foods
(cookies, potato chips, and rice pudding) did not change.
Changes in rated hunger and fullness (difference between
ratings before and after lunch) differed between patients and
control subjects, t(8) 5 3.0, p < .05, and t(8) 5 2.3, p < .05,
respectively. The control subjects showed the expected changes
(mean change 5 29.9 mm for hunger and 37.1 mm for fullness), but the patients’ rated hunger and fullness did not change
(mean change 5 1.1 mm for hunger and 4.5 mm for fullness).
There were no significant differences for rated thirst. The patients also tended to eat more of the lunch than did the control
subjects (patients: M 5 362 Kcal, SD 5 39; control subjects:
M 5 224 Kcal, SD 5 106), t(8) 5 1.70, p 5 .1.
In the follow-up session with G.A., his rated liking of the
cheese pastry decreased after he had eaten it to satiety (change
in rated liking 5 5 mm for taste and 46 mm for texture), but
his liking for the taste of foods that he had only sampled
(sandwiches, apple slices, and biscuits) increased (change in
rated liking 5 15 mm for taste. (Liking for the texture of foods he
had only sampled did not change; change in rated liking 5 3
mm for texture). When rating the pastry for the second time, G.A.
said it tasted ‘‘sour.’’ Furthermore, he chose one of the uneaten
foods (sandwiches) when asked what he would most like to eat,
and could not remember eating the pastry.
Analysis
In the first experiment, the amnesic patients’ sensory-specificsatiety ratings (change in rated liking and desired intake) were
averaged over three (S.P.) or seven (G.A.) sessions, and then
Multiple-Meal Study
On average, the patients consumed nearly 2,000 Kcal over
the two lunches, which was significantly more than the con-
Note. N 5 number of items. G.A. is a 49-year-old male whose amnesia results
from herpes simplex encephalitis, contracted 14 years prior to this study; his
clinical symptoms are amnesia, category-specific recognition deficit, and
dysexecutive symptoms. S.P. is a 51-year-old male whose amnesia results from
herpes simplex encephalitis, contracted 6 years prior to this study; his clinical
symptoms are amnesia, category-specific recognition deficit, and mild dysexecutive symptoms. Scores in boldface indicate significant impairment relative
to normal. Control data are provided in the norms for the Corsi block test
(Kessels, van Zandvoort, Postma, Kappelle, & de Haan, 2000), the Warrington recognition memory (WRM; Warrington, 1984) test for words and faces,
the Wechsler Memory Scale (WMS; Wechsler, 1999), the Brixton test (a test of
visual problem solving and executive function; Burgess & Shallice, 1997), the
clinical Stroop test (Trenerry, Crosson, DeBoe, & Leber, 1989), the Psycholinguistic Assessment of Language Processing in Aphasia (PALPA; Kay, Lesser,
& Coltheart, 1992), and the Wisconsin Card Sort Test (WCST; Heaton, Chelune, Talley, Kay, & Curtiss, 1993). Control data for the University of Pennsylvania Smell Identification Test (UPSIT; Doty, Shaman, & Dann, 1984) come
from 4 male control subjects age-matched to the patients. In all other cases,
control data come from 30 control subjects age-matched to the patients. For the
control data, standard deviations are given in parentheses. NART 5 National
Adult Reading Test (IQ equivalent; Nelson & Willison, 1991).
a
The control data for the Brixton test and NART IQ equivalent are average
normal scores.
Volume 19—Number 7
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625
Sensory-Specific Satiety in Amnesics
Taste liking
Texture liking
Desire to eat
20
15
Change in Rating (mm)
10
5
0
−5
−10
−15
−20
−25
−30
Food eaten to satiety Sampled foods
Food eaten to satiety Sampled foods
Patients
Control Subjects
Fig. 2. Mean changes in patients’ and control subjects’ rated liking for taste and texture and rated desired intake of food in the sensory-specificsatiety study. Results are shown for the food eaten to satiety (sandwiches) and foods that were only sampled. Mean change in rating was calculated
by subtracting the rating before consumption of the lunch from the rating after consumption of the lunch. Negative ratings indicate a decline in
liking or desire to eat after lunch. Error bars indicate standard errors of the means.
trol subjects consumed, t(4) 5 4.1, p < .05 (Fig. 3). Only 1
of the 4 control subjects ate something at the second lunch,
whereas both patients ate almost as much at the second lunch
as they did at the first. Among the control subjects, premeal
rated hunger decreased between the first and second lunch,
and premeal rated fullness increased (change in hunger 5
Amount Consumed (Kcal)
2,000
1,500
Hedonic-Ratings Study
The patients’ ratings of the pleasantness of the yogurt increased
monotonically with increasing sucrose concentration and did
not decline even for the sweetest yogurt. In contrast, the rating
function for the control subjects had an inverted-U shape; their
liking of the yogurts increased as the amount of sucrose in-
1,000
TABLE 2
Results of the Hedonic-Ratings Study
500
0
Control
Subjects
Patients
Fig. 3. Patients’ and control subjects’ mean intake at two consecutive
lunches in the multiple-meal study. Control subjects (n 5 4) were tested
once, and G.A. and S.P. were tested twice each. The black portions of the
bars refer to the first lunch, and the white portions refer to the second lunch.
626
35 mm, change in fullness 5 26 mm). In contrast, the patients’
ratings of their appetite did not change between the first and
second lunch (change in hunger 5 7.3, change in rated fullness 5 7.8).
Yogurt sample
G.A.
S.P.
Control data
1% sucrose
5.9% sucrose
10% sucrose
17.6% sucrose
30% sucrose
4
13
59
68
65
12
43
44
73
65
17
67
74
44
22
Note. Ratings were made on a 100-mm line scale, anchored by not at all
pleasant, on the left, and extremely pleasant, on the right. The control data
are from 2 age-matched control subjects.
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Volume 19—Number 7
S. Higgs et al.
creased, up to an inflection point of 10%, after which liking
declined (see Table 2).
DISCUSSION
The data show that reported multiple-meal eating by amnesics is
unlikely to be due to a failure of sensory-specific satiety. Both
the patients and the control subjects in our first study showed a
decline in rated liking of a food consumed to satiety, whereas
only the patients showed hyperphagia. We further conclude that
it is not necessary to remember having eaten a food in order to
express sensory-specific satiety to that food, because neither of
the patients was aware of having just eaten when queried after
lunch. This finding suggests that cognitive processes based on
explicit expectations about normal portion size, or on memories
of having eaten, do not underlie sensory-specific satiety. A likely
mechanism may be habituation of responses to the sensory
properties of an eaten food (Swithers & Hall, 1994). Our data
also suggest that the decline in pleasantness of an eaten food is
not sufficient for someone to terminate a meal, because in the
second study, the patients, who had previously shown sensoryspecific satiety, ate a second lunch 15 min after consuming an
identical first lunch.
Brain areas other than those damaged in S.P. and G.A. are
likely to be important for the expression of sensory-specific
satiety. This hypothesis is consistent with reports that the neural
correlates of sensory-specific satiety are found in orbitofrontal
cortex (Critchley & Rolls, 1996), rather than medial temporal
structures. Processing of the pleasantness of taste stimuli is
represented in anterior regions of the orbitofrontal cortex
(Kringelbach, O’Doherty, Rolls, & Andrews, 2003), which is
consistent with the findings that orbitofrontal damage in S.P. and
G.A. is restricted to the right hemisphere and that anterior
sections in both hemispheres are spared.
The possibility that the hyperphagia observed is unrelated to
the memory deficits of the patients should be considered.
Amygdala damage, common to both of these patients, has been
associated with hyperoral behavior (in Klüver-Bucy syndrome).
However, we saw no evidence of behaviors associated with
Klüver-Bucy syndrome in these patients. Both patients also
had some bilateral damage to the insula, and such damage is
known to cause gustatory and olfactory deficits (Pritchard,
Macaluso, & Eslinger, 1999; Small et al., 2003). Our findings are
consistent with the patients having some gustatory and olfactory
deficits: Although G.A. and S.P. could discriminate among
sweetened yogurts, unlike the control subjects they did not show
reduced liking for the very sweet yogurt. They are also both
anosmic. However, it is unlikely that these gustatory and olfactory deficits can explain their hyperphagia, because lesions
of the insula are not associated with overeating (Mathy, Dupuis,
Pigeolet, & Jacquerye, 2003). Furthermore, although increased
preference for sweetness is seen in normal aging (Murphy &
Withee, 1986), aging is generally associated with reduced
Volume 19—Number 7
food intake. Finally, the patients ate more of both foods, not
just the sweet food, in the multiple-meal study. Another possibility is that the patients’ overeating reflects perseveration resulting from damage to the frontal cortex; however, the patients
showed no evidence of persistent responses in using the rating
scales.
Alternatively, the most powerful cue for terminating a meal
may be the social norm that eating should stop after a meal has
been consumed (Rozin et al., 1998), and amnesic patients may
eat beyond the bounds of what is considered ‘‘normal consumption’’ because they cannot remember having just eaten
(because of damage to the hippocampus). However, the patients
differed from the control subjects in that their rated appetite did
not change in line with changes in their nutritional state, and
this suggests that their hyperphagia may be related to processing
of visceral satiety signals. Supporting this possibility, data from
rats with selective lesions to the hippocampus suggest that the
hippocampus is required for internal-state signals to organize
eating behavior (Clifton, Vickers, & Somerville, 1998; Davidson, 1993). Similarly, amnesic patients may be unable to use
bodily sensations arising from the ingestion of food. Mealinduced changes in appetite (which were impaired in the patients) may be cognitively mediated and depend on the conjunction of memories of internal-state cues, food-related sensory
cues, and information about the previous postingestive consequences of consuming a food (Baker, Booth, Duggan, & Gibson,
1987; Booth, 1977). Failed configuration learning, due to hippocampal damage, could thus contribute to overeating (Sutherland & Rudy, 1989). Finally, explicit memory that food has
been eaten may be required to label internal cues associated
with food ingestion. A study supporting this possibility has
shown that the behavioral effects of drug-induced bodily states
depend on cognitive variables that affect the labeling of those
states (Schachter & Singer, 1962).
In conclusion, our data demonstrate that impaired sensoryspecific satiety cannot account for the phenomenon of multiplemeal eating in amnesia. The patients in this study showed
sensory-specific satiety although they had no explicit memory
for having eaten food and ate multiple meals.
Acknowledgments—This work was supported by grants to the
first and last authors from the Biotechnology and Biological
Research Council and the Medical Research Council, United
Kingdom, and by a fellowship to the third author given jointly by
the Economic and Social Research Council and the Medical
Research Council, United Kingdom. We thank G.A. and S.P. for
their kind participation in the studies.
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(RECEIVED 6/4/07; REVISION ACCEPTED 12/21/07)
Downloaded from pss.sagepub.com at University of Aberdeen on August 24, 2010
Volume 19—Number 7