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Psychological Science http://pss.sagepub.com/ 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 The online version of this article can be found at: http://pss.sagepub.com/content/19/7/623 Published by: http://www.sagepublications.com On behalf of: Association for Psychological Science Additional services and information for Psychological Science can be found at: Email Alerts: http://pss.sagepub.com/cgi/alerts Subscriptions: http://pss.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav 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 r Volume 19—Number 7 DownloadedCopyright from pss.sagepub.com2008 Association at University for Psychological of Aberdeen on Science August 24, 2010 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), 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.