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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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Downloaded from pss.sagepub.com at University of Aberdeen on August 24, 2010 PSYCHOLOGICAL SCIENCE

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 Despite these intriguing findings, little is known about the appetite? We explored this question by examining prefer- mechanisms underlying multiple-meal eating in amnesia. ences for recently consumed food in patients with amnesia. Because the procedure in previous studies has been to offer the Although the patients were unable to remember having same meals in succession, one explanation is that the usual eaten, and were inclined to eat multiple meals, we found decline in palatability and intake of a food that has been eaten to that sensory-specific satiety was intact in these patients. satiety is disrupted in amnesia (Rolls, Rolls, Rowe, & Sweeney, The data suggest that sensory-specific satiety can occur in 1973). In the first experiment reported here, we tested whether 2 the absence of explicit memory for having eaten and that densely amnesic patients with bilateral damage to the medial impaired sensory-specific satiety does not underlie the phe- temporal lobes reported such sensory-specific satiety. This ex- nomenon of multiple-meal eating in amnesia. Overeating periment also provided an opportunity to test whether explicit in amnesia may be due to disruption of learned control by memory of having recently eaten a food is required for the ex- physiological aftereffects of a recent meal or to problems pression of sensory-specific satiety (Rozin et al., 1998). In our utilizing internal cues relating to nutritional state. second experiment, we checked whether our patients ate mul- tiple meals as they were offered. Finally, to control for the possibility that the amnesic patients had deficits in taste per- Reports that amnesic patients eat multiple meals suggest that ception or were biased in their use of our rating scales, in our memory for recent eating may be one factor controlling food third experiment we assessed their hedonic ratings of yogurt intake (Hebben, Corkin, Eichenbaum, & Shedlack, 1985; Rozin, samples differing in sweetness. Dow, Moscovitch, & Rajaram, 1998). In addition to exhibiting anterograde amnesia due to bilateral hippocampal damage, the neuropsychological patient H.M. reported problems in identi- METHOD fying his state of food repletion and depletion (Hebben et al., 1985). He also ate a second meal within 1 min of finishing the Test of Sensory-Specific Satiety in Amnesia first. Rozin et al. (1998) found that 2 amnesic patients with hip- Participants pocampal damage similar to that of H.M. consumed two lunches Two amnesic patients (S.P. and G.A.) and 8 control subjects in quick succession, and usually began to consume a third meal (4 men and 4 women; age range 5 53–58) participated in this if it was offered. Furthermore, reminding neurologically intact experiment. Both patients had lesions that included medial participants of the lunch that they ate earlier on the day of a temporal and frontal lobe structures (see Fig. 1). G.A. was for- study inhibits their subsequent consumption of snacks, relative merly a professional musician, and S.P. had been a bank man- to consumption in a condition in which participants are re- ager. Both had a category-specific recognition deficit for living minded of the lunch they ate the previous day (Higgs, 2002). 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 Address correspondence to Suzanne Higgs, University of Birming- ham, Edgbaston, Birmingham, B15 2TT, England, e-mail: s.higgs.1@ disproportionate to deficits in general cognitive or intellectual bham.ac.uk. functioning (see Table 1). All procedures were approved by the

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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), tem- poral 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 minutes later, the patients were asked if they had just eaten. They Birmingham, and the participants gave informed written consent. 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 Procedure eaten in a larger quantity than the others. The patients were Sensory-specific satiety was measured by comparing the change tested in three (S.P.)or seven (G.A.) sessions separated by at least in liking and desired intake of a food that was eaten to satiety a week. Each session was identical. S.P. attended fewer sessions with the change in liking and desired intake of foods that were because he had to travel some distance to be tested. The control only sampled. Participants rated four samples before and after subjects were tested on one occasion each. consuming one of the foods (sandwiches) as lunch. As in pre- A follow-up session with G.A. tested the generalizability of vious studies, ratings of the sampled foods were averaged for the results to different foods. The procedure was the same as that comparison with the food eaten to satiety. just described, but the foods were sandwiches, apple slices, bis- Testing took place individually between 12:00 and 2:00 p.m. cuits, and cheese pastries. The cheese pastries were consumed On arrival, participants rated their feelings of ‘‘hunger,’’ ‘‘full- to satiety as lunch. ness,’’ 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, Multiple-Meal Study In a separate study, participants were served two lunches, sep- using similar scales. The questions were ‘‘How much do you like arated by 15 min. Each lunch consisted of eight portions of tuna the taste of this food?’’ ‘‘How much do you like the texture of this or ham sandwiches (Ginsters, Cornwall, England; approximately food?’’ and ‘‘How much of this food could you eat?’’ For the first 40 g and 96 Kcal per portion) and four portions of cake (Lemon two questions, the anchors on the rating scales were not at all,on Cake, The Handmade Flapjack Co., Coventry, England; ap- the left, and extremely, on the right; for the third question, the proximately 35 g and 148 Kcal per portion). Participants helped anchors were nothing at all, on the left, and a large amount,on themselves to as much food as they wanted. When they had the right. The foods, which were selected for their different finished eating, evidence that a meal had been consumed was sensory properties, were (a) a quarter of a chocolate-chip cookie removed. Fifteen minutes later, an identical meal was presented, (Cookie Coach Co., Manchester, England), (b) 2 tablespoons of and the participants were asked to help themselves to as much as rice pudding (Muller rice; Muller Dairy, Shrewsbury, England), they wanted. Before and after lunch, participants completed line (c) two potato chips (Walkers Crisps, Leicester, England), and rating scales assessing their hunger and fullness. G.A. and S.P. (d) one eighth of a sandwich made from two standard slices of were tested twice each, and 4 age-matched, male control sub- bread (ham or chicken; Ginsters, Cornwall, England). The jects were tested once. 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 Hedonic-Ratings Study used for rating each food, and participants were instructed to eat Using the 100-mm line scales described previously, participants all of each sample. in the third experiment (G.A., S.P., and 2 age-matched, male After removal of the sample foods, participants consumed control subjects) rated their liking for the taste of five samples of sandwiches to satiety. Two sandwiches (four slices of bread) were yogurt differing in sweetness. Sucrose (Tate and Lyle, United cut into quarters to provide eight portions (approximately 40 g Kingdom) was added to plain full-fat yogurt (Coberco, Arhem, and 96 Kcal per portion). Once the participants had helped The Netherlands) at the following concentrations: 1, 5.9, 10, 17.6, themselves to as many portions as they wanted, the sandwiches and 30% sucrose/yogurt by weight. The 10% concentration was were removed. Five minutes later, a second set of sample foods equivalent to the sugar concentration of commercially avail- was presented, and participants once again rated their liking for able flavored yogurts. Fifty-milliliter portions of yogurt were and desire to eat each sample, as well as their hunger and served in opaque plastic cups and presented in a random order. fullness and thirst. The sample foods were then removed. Five Participants consumed enough to be able to make the ratings

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TABLE 1 these averages and the control subjects’ ratings were analyzed Results of Neuropsychological Testing of the Patients by a two-way analysis of variance with rating type (pleasantness of taste, pleasantness of texture, desire to eat) and food type Control Measure G.A. S.P. data (food eaten to satiety, sampled food) as within-subjects factors and group (patient, control) as a between-subjects factor. Intake Visual short-term memory of the sandwiches as lunch and change in rated appetite and Corsi block test 5 7 5 (2) Verbal short-term memory thirst were averaged for the patients across sessions and com- Digits forwards 7 7 7 (2) pared with the control data using a two-tailed t test. Intake in the Digits backwards 4 6 5 (2) multiple-meal study was analyzed by t test. Sentence Repetition (PALPA Test 55; N 5 60) 57 60 60 (0) RESULTS Word Repetition (varying number of syllables, PALPA Test 30; N 5 24) 24 24 24 (0) Test of Sensory-Specific Satiety in Amnesia Long-term memory The patients could not remember having eaten when questioned WRM Words (N 5 50) 24 31 45.3 (3.4) after the second set of ratings, and on average correctly identi- WRM Faces (N 5 50) 31 33 44.3 (3.5) fied the food eaten in a larger quantity 38% of the time. Nev- WMS Logical Memory 2522.5 (6.3) ertheless, the main effect of food type was significant, F(1, 16) 5 WMS Visual Reproduction 6529.0 (5.2) 6.6, p < .05; both the patients and the control subjects showed a Executive function decline in rated liking for and desire to eat the food eaten to Brixton test (N 5 54) 41 42 50a Stroop test (N 5 112) 11 92 112 (0) satiety relative to the sampled foods. There was no effect of WCST 48 (3) 98 (6) 67.5 (5.5) group, F(1, 16) 5 0.038, p 5 .5, or of rating type, F(2, 32) 5 0.7, NART IQ equivalent 103 110 100a p 5 .5, nor were there any significant interactions (all ps > .3). Comprehension (Synonym Figure 2 shows that the rated liking for and desire to eat the Matching, PALPA Test 50) sandwiches decreased after they had been consumed as lunch, 5 High imageability (N 60) 60 60 60 (0) but that the rated liking for and desire to eat the other foods Low imageability (N 5 60) 58 57 60 (0) (cookies, potato chips, and rice pudding) did not change. Smell UPSIT 10.0 14.0 30.8 Changes in rated hunger and fullness (difference between ratings before and after lunch) differed between patients and Note. N 5 number of items. G.A. is a 49-year-old male whose amnesia results control subjects, t(8) 5 À3.0, p < .05, and t(8) 5 2.3, p < .05, from herpes simplex encephalitis, contracted 14 years prior to this study; his clinical symptoms are amnesia, category-specific recognition deficit, and respectively. The control subjects showed the expected changes dysexecutive symptoms. S.P. is a 51-year-old male whose amnesia results from (mean change 5 À29.9 mm for hunger and 37.1 mm for full- herpes simplex encephalitis, contracted 6 years prior to this study; his clinical symptoms are amnesia, category-specific recognition deficit, and mild dysex- ness), but the patients’ rated hunger and fullness did not change ecutive symptoms. Scores in boldface indicate significant impairment relative (mean change 5 1.1 mm for hunger and À4.5 mm for fullness). to normal. Control data are provided in the norms for the Corsi block test There were no significant differences for rated thirst. The pa- (Kessels, van Zandvoort, Postma, Kappelle, & de Haan, 2000), the War- rington recognition memory (WRM; Warrington, 1984) test for words and faces, tients also tended to eat more of the lunch than did the control the Wechsler Memory Scale (WMS; Wechsler, 1999), the Brixton test (a test of subjects (patients: M 5 362 Kcal, SD 5 39; control subjects: visual problem solving and executive function; Burgess & Shallice, 1997), the 5 5 5 À 5 clinical Stroop test (Trenerry, Crosson, DeBoe, & Leber, 1989), the Psycho- M 224 Kcal, SD 106), t(8) 1.70, p .1. linguistic Assessment of Language Processing in Aphasia (PALPA; Kay, Lesser, In the follow-up session with G.A., his rated liking of the & Coltheart, 1992), and the Wisconsin Card Sort Test (WCST; Heaton, Che- cheese pastry decreased after he had eaten it to satiety (change lune, Talley, Kay, & Curtiss, 1993). Control data for the University of Penn- 5 À À sylvania Smell Identification Test (UPSIT; Doty, Shaman, & Dann, 1984) come in rated liking 5 mm for taste and 46 mm for texture), but from 4 male control subjects age-matched to the patients. In all other cases, his liking for the taste of foods that he had only sampled 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 (sandwiches, apple slices, and biscuits) increased (change in Adult Reading Test (IQ equivalent; Nelson & Willison, 1991). rated liking 5 15 mm for taste. (Liking for the texture of foods he aThe control data for the Brixton test and NART IQ equivalent are average had only sampled did not change; change in rated liking 5 À3 normal scores. mm for texture). When rating the pastry for the second time, G.A. said it tasted ‘‘sour.’’ Furthermore, he chose one of the uneaten (one or two spoonfuls) and rinsed their mouths with water in foods (sandwiches) when asked what he would most like to eat, between samples. and could not remember eating the pastry.

Analysis In the first experiment, the amnesic patients’ sensory-specific- Multiple-Meal Study satiety ratings (change in rated liking and desired intake) were On average, the patients consumed nearly 2,000 Kcal over averaged over three (S.P.) or seven (G.A.) sessions, and then the two lunches, which was significantly more than the con-

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Taste liking 20 Texture liking Desire to eat 15

10

5

0

−5

−10

−15 Change in Rating (mm)

−20

−25

−30 Food eaten to satiety Sampled foods Food eaten to satiety Sampled foods Control Subjects Patients

Fig. 2. Mean changes in patients’ and control subjects’ rated liking for taste and texture and rated desired intake of food in the sensory-specific- satiety 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 À4.1, p < .05 (Fig. 3). Only 1 À35 mm, change in fullness 5 26 mm). In contrast, the patients’ of the 4 control subjects ate something at the second lunch, ratings of their appetite did not change between the first and whereas both patients ate almost as much at the second lunch second lunch (change in hunger 5 7.3, change in rated full- as they did at the first. Among the control subjects, premeal ness 5 7.8). rated hunger decreased between the first and second lunch, and premeal rated fullness increased (change in hunger 5 Hedonic-Ratings Study The patients’ ratings of the pleasantness of the yogurt increased 2,000 monotonically with increasing sucrose concentration and did not decline even for the sweetest yogurt. In contrast, the rating 1,500 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 Yogurt sample G.A. S.P. Control data

Amount Consumed (Kcal) 1% sucrose 4 12 17 0 5.9% sucrose 13 43 67 Control Patients 10% sucrose 59 44 74 Subjects 17.6% sucrose 68 73 44 30% sucrose 65 65 22 Fig. 3. Patients’ and control subjects’ mean intake at two consecutive lunches in the multiple-meal study. Control subjects (n 5 4) were tested Note. Ratings were made on a 100-mm line scale, anchored by not at all once, and G.A. and S.P. were tested twice each. The black portions of the pleasant, on the left, and extremely pleasant, on the right. The control data bars refer to the first lunch, and the white portions refer to the second lunch. are from 2 age-matched control subjects.

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creased, up to an inflection point of 10%, after which liking food intake. Finally, the patients ate more of both foods, not declined (see Table 2). just the sweet food, in the multiple-meal study. Another possi- bility is that the patients’ overeating reflects perseveration re- DISCUSSION sulting from damage to the frontal cortex; however, the patients showed no evidence of persistent responses in using the rating The data show that reported multiple-meal eating by amnesics is scales. unlikely to be due to a failure of sensory-specific satiety. Both Alternatively, the most powerful cue for terminating a meal the patients and the control subjects in our first study showed a may be the social norm that eating should stop after a meal has decline in rated liking of a food consumed to satiety, whereas been consumed (Rozin et al., 1998), and amnesic patients may only the patients showed hyperphagia. We further conclude that eat beyond the bounds of what is considered ‘‘normal con- it is not necessary to remember having eaten a food in order to sumption’’ because they cannot remember having just eaten express sensory-specific satiety to that food, because neither of (because of damage to the hippocampus). However, the patients the patients was aware of having just eaten when queried after differed from the control subjects in that their rated appetite did lunch. This finding suggests that cognitive processes based on not change in line with changes in their nutritional state, and explicit expectations about normal portion size, or on memories this suggests that their hyperphagia may be related to processing of having eaten, do not underlie sensory-specific satiety. A likely of visceral satiety signals. Supporting this possibility, data from mechanism may be habituation of responses to the sensory rats with selective lesions to the hippocampus suggest that the properties of an eaten food (Swithers & Hall, 1994). Our data hippocampus is required for internal-state signals to organize also suggest that the decline in pleasantness of an eaten food is eating behavior (Clifton, Vickers, & Somerville, 1998; David- not sufficient for someone to terminate a meal, because in the son, 1993). Similarly, amnesic patients may be unable to use second study, the patients, who had previously shown sensory- bodily sensations arising from the ingestion of food. Meal- specific satiety, ate a second lunch 15 min after consuming an induced changes in appetite (which were impaired in the pa- identical first lunch. tients) may be cognitively mediated and depend on the con- Brain areas other than those damaged in S.P. and G.A. are junction of memories of internal-state cues, food-related sensory likely to be important for the expression of sensory-specific cues, and information about the previous postingestive conse- satiety. This hypothesis is consistent with reports that the neural quences of consuming a food (Baker, Booth, Duggan, & Gibson, correlates of sensory-specific satiety are found in orbitofrontal 1987; Booth, 1977). Failed configuration learning, due to hip- cortex (Critchley & Rolls, 1996), rather than medial temporal pocampal damage, could thus contribute to overeating (Suth- structures. Processing of the pleasantness of taste stimuli is erland & Rudy, 1989). Finally, explicit memory that food has represented in anterior regions of the orbitofrontal cortex been eaten may be required to label internal cues associated (Kringelbach, O’Doherty, Rolls, & Andrews, 2003), which is with food ingestion. A study supporting this possibility has consistent with the findings that orbitofrontal damage in S.P.and shown that the behavioral effects of drug-induced bodily states G.A. is restricted to the right hemisphere and that anterior depend on cognitive variables that affect the labeling of those sections in both hemispheres are spared. states (Schachter & Singer, 1962). The possibility that the hyperphagia observed is unrelated to In conclusion, our data demonstrate that impaired sensory- the memory deficits of the patients should be considered. specific satiety cannot account for the phenomenon of multiple- Amygdala damage, common to both of these patients, has been meal eating in amnesia. The patients in this study showed associated with hyperoral behavior (in Klu¨ver-Bucy syndrome). sensory-specific satiety although they had no explicit memory However, we saw no evidence of behaviors associated with for having eaten food and ate multiple meals. Klu¨ver-Bucy syndrome in these patients. Both patients also had some bilateral damage to the insula, and such damage is Acknowledgments—This work was supported by grants to the known to cause gustatory and olfactory deficits (Pritchard, Macaluso, & Eslinger, 1999; Small et al., 2003). Our findings are first and last authors from the Biotechnology and Biological consistent with the patients having some gustatory and olfactory Research Council and the Medical Research Council, United deficits: Although G.A. and S.P. could discriminate among Kingdom, and by a fellowship to the third author given jointly by sweetened yogurts, unlike the control subjects they did not show the Economic and Social Research Council and the Medical reduced liking for the very sweet yogurt. They are also both Research Council, United Kingdom. We thank G.A. and S.P. for anosmic. However, it is unlikely that these gustatory and ol- their kind participation in the studies. factory deficits can explain their hyperphagia, because lesions of the insula are not associated with overeating (Mathy, Dupuis, REFERENCES Pigeolet, & Jacquerye, 2003). Furthermore, although increased preference for sweetness is seen in normal aging (Murphy & Baker, B.J., Booth, D.A., Duggan, J.P., & Gibson, E.L. (1987). 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