The authors have declared that no competing interests exist.
Conceived and designed the experiments: JMB DF. Performed the experiments: NRS JMC LLW OMM. Analyzed the data: JMB ECH. Wrote the paper: JMB PJR DF ECH. Designed and constructed soup-bowl apparatus: JFB.
Psychological and neurobiological evidence implicates hippocampal-dependent memory processes in the control of hunger and food intake. In humans, these have been revealed in the hyperphagia that is associated with amnesia. However, it remains unclear whether ‘memory for recent eating’ plays a significant role in neurologically intact humans. In this study we isolated the extent to which memory for a recently consumed meal influences hunger and fullness over a three-hour period. Before lunch, half of our volunteers were shown 300 ml of soup and half were shown 500 ml. Orthogonal to this, half consumed 300 ml and half consumed 500 ml. This process yielded four separate groups (25 volunteers in each). Independent manipulation of the ‘actual’ and ‘perceived’ soup portion was achieved using a computer-controlled peristaltic pump. This was designed to either refill or draw soup from a soup bowl in a covert manner. Immediately after lunch, self-reported hunger was influenced by the actual and not the perceived amount of soup consumed. However, two and three hours after meal termination this pattern was reversed - hunger was predicted by the perceived amount and not the actual amount. Participants who thought they had consumed the larger 500-ml portion reported significantly less hunger. This was also associated with an increase in the ‘expected satiation’ of the soup 24-hours later. For the first time, this manipulation exposes the independent and important contribution of memory processes to satiety. Opportunities exist to capitalise on this finding to reduce energy intake in humans.
Obesity remains a major health concern
The prospect that memory plays an important role in the regulation of food intake is consistent with an emerging literature on ‘memory for recent eating’ in humans
With this paradigm, a potential concern is that the effect on food intake is revealed only after an instruction to recall a recent meal. Whether humans routinely retrieve explicit memories of recent meals remains unclear. An alternative strategy is to disrupt memory encoding during a meal and then measure appetite and intake at a subsequent meal. This can be achieved by asking volunteers to engage in a distracting task (
Perhaps the most striking evidence for impaired encoding is found in patients with retrograde amnesia. Again, consistent with Higgs’s interpretation, bilateral hippocampal damage is associated with hyperphagia - after eating one meal to fullness, an amnesic may go on to consume further meals and to report no memory for recent eating and little change in hunger
Together, these findings highlight a potentially important role for episodic memory in the control of meal size and appetite in humans. This merits attention, not least because it challenges our understanding of short-term energy regulation and, in particular, the long-standing assumption that cognition plays a role primarily around a meal and during the early stages of the ‘satiety cascade’
Previously, Wansink
A second objective was to establish the extent to which our memory manipulation impacts beliefs about the soup at a subsequent test session. Recently, we and others have explored a range of phenomena relating to ‘expected satiation’ – the extent to which a food is expected to deliver fullness when compared with other foods on a calorie-for-calorie basis
Expected satiation can be viewed as an example of ‘semantic memory’ or ‘general knowledge’ about the world. By contrast, ‘episodic memory’ refers to the encoding of autobiographical information relating to a specific event that is located in time. Episodic and semantic memories appear to function in distinct yet interdependent ways. For example, expisodic memory is often ‘reconstructed’ or biased by semantic memory
Participants were tested in a between-subjects design. On arrival, they were shown either 300 ml or 500 ml of soup. Participants then consumed either 300 ml or 500 ml. An orthogonal combination of seeing either 300 or 500 ml and then eating either 300 ml or 500 ml rendered four separate conditions. ‘Incongruous eating’ was achieved by covertly manipulating soup entering or leaving the bowl during the meal. Appetite was assessed for three hours after the meal and the expected satiation of the soup was assessed approximately 24-hours later.
One hundred volunteers (69 female and 31 male) completed the study and produced responses to an awareness questionnaire indicating that they were unaware that the soup bowl had been modified. Six other participants reported a degree of awareness and were rejected and replaced on this basis. All were staff or students at the University of Bristol. Volunteers had a mean BMI of 23.4 (
Participants were recruited by email. Vegetarians and vegans were excluded, together with anyone who declared a food allergy and/or intolerance. All received ten pounds Sterling for their assistance. The study was approved by University of Bristol Faculty of Science Human Research Ethics Committee. All provided written informed consent before assisting with the study.
Soup was added or removed from a transparent soup bowl using a peristaltic pump (see
The bottom of the soup bowl was connected to a length of temperature-insulated food-grade tubing. This connection was hidden from the participants using a tablecloth. The tubing fed through a hole in the table (immediately under the bowl) and connected to the pump and then to a reservoir of soup via a hole in the screen. The experimenter was able to manipulate the direction and rate of flow using an adjustable motor controller that was attached to the pump. The pre-heated soup was ‘creamed tomato soup’ (supplied by Sainsbury’s Supermarkets Ltd., London; 38 kcal/100 g).
Our measure of expected satiation was based on a ‘method of adjustment,’ and is described in detail elsewhere
Testing took place individually between 11∶00 and 14∶30 hours. Volunteers attended two sessions approximately 24 hours apart. They were asked to abstain from eating for three hours before the initial session, and to confirm that they had complied with this request on arrival. Hunger and fullness were then assessed using 100-mm visual-analogue scales labelled ‘How [hungry/full] are you right now?’ and anchored ‘not at all [hungry/full]’ to ‘extremely [hungry/full].’ Participants were also asked to report how long it had been since their last meal. Using this assessment of hunger, the participants were then pseudo-randomly assigned to one of the four conditions using a minimisation method
Participants were then taken to a testing booth where a bowl of soup was waiting. They were instructed to avoid touching the bowl and to eat until the volume of soup remaining matched a line on the side of the bowl. The line ensured that eating terminated with 100 ml of soup remaining, thereby obscuring the bottom of the bowl. To accommodate for this amount, across conditions, the initial starting portion was 100 ml larger than the amount consumed. All participants were informed that eating their prescribed portion was a mandatory part of the procedure.
After the meal, hunger and fullness ratings were then taken once again. Participants were then given a pack containing an information sheet with written instructions, a food diary for the rest of the day, and three hunger and fullness rating scales, labelled one-hour, two-hours and three-hours. They were also issued a buzzer that sounded every hour for three hours. On each occasion, they were instructed to complete the appropriate hunger and fullness rating. This procedure has been used in previous studies in our laboratory and compliance with these instructions has been found to be high
Approximately 24 hours later the participants were shown a bowl containing 400 ml of tomato soup and evaluated its expected satiation. They then completed the Dutch Eating Behaviour Questionnaire (DEBQ)
Finally, a measure of their height and weight was taken. Debriefing took place by email, after all of the data had been collected.
One-way ANOVA was used to explore evidence for differences in baseline characteristics across conditions. Specifically, we assessed BMI, age, initial hunger, and scores on the three subsections of the DEBQ.
To explore hunger ratings in the inter-meal interval, we used a mixed-model ANOVA with time (0, 60, 120, and 180 minutes) as a within-subjects factor and amount seen (300 ml or 500 ml) and amount eaten (300 ml or 500 ml) as between-subjects factors. The same approach was also used to analyse ratings of fullness. Where we found a significant main effect or interaction term we used ANOVA to scrutinise the effects of perceived and actual amounts, at each time point, separately. In all cases, to reduce error variance, we included baseline ratings as a covariate where a significant correlation existed between a dependent measure and its baseline counterpart. Finally, for each participant, we calculated an expected-satiation score (kcal) by taking an average (mean) of the selected comparison foods. Higher values indicate that the soup was expected to deliver greater satiation in the second test session. To explore the effects of amount seen and amount eaten we submitted these expected satiation scores to a 2 x 2 ANOVA.
Twenty-five participants were recruited into each condition. Across conditions, we found no significant differences in BMI, initial hunger, initial fullness, age, and scores on the separate subsections of the DEBQ (all
Condition | ||||
see 500 ml/eat 300 ml | see 300 ml/eat 500 ml | see 500 ml/eat 500 ml | See 300 ml/eat 300 ml | |
Age (y) | 24.2 (8.5) | 25.7 (8.3) | 26.9 (8.8) | 27.6 (10.4) |
BMI | 22.4 (2.5) | 23.9 (4.4) | 23.8 (3.7) | 23.4 (2.9) |
DEBQ | ||||
Restrained eating | 2.6 (0.86) | 2.6 (0.78) | 2.4 (0.62) | 2.6 (0.91) |
External eating | 3.5 (0.55) | 3.2 (0.44) | 3.4 (0.72) | 3.5 (0.66) |
Emotional eating | 2.5 (0.67) | 2.1 (0.62) | 2.3 (0.75) | 2.4 (0.75) |
Initial hunger (mm) | 62.7 (23.3) | 58.6 (25.1) | 68.4 (16.6) | 67.6 (13.3) |
Initial fullness (mm) | 23.9 (20.4) | 27.7 (19.3) | 17.4 (18.9) | 21.0 (13.8) |
Gender (n) | F = 17/M = 8 | F = 17/M = 8 | F = 16/M = 9 | F = 19/M = 6 |
Means (+/−
Hunger increased significantly during the inter-meal interval (
Separate values are provided for participants in each condition.
Separate values are provided for participants in each condition.
In response to the open-ended question about the purpose of the study, 53% thought that the study was assessing the extent to which soup is filling in comparison to other types of foods, 18% thought that the study was investigating the validity of ratings of hunger and fullness, and 13% suggested that the study was investigating the relationship between expectations of fullness and actual fullness. Other participants offered alternative suggestions, none of which related to the objectives of the study. Six participants failed to complete the question.
In response to the question ‘was the soup manipulated in any way?’ six participants confirmed that it had been artificially refilled or drained. As noted above, these were excluded and replaced. A further 19% responded ‘yes’ to this question. However, none of these participants commented on a change in volume (most referred to the viscosity of the soup).
Two additional studies were conducted to demonstrate that; i) participants were able to discriminate between 300 ml and 500 ml bowls of soup and, ii) during the inter-meal interval participants had different memories of the amount of soup that they consumed. In each case we used the same equipment and materials as in the main study.
Twenty participants were tested. Half were presented with a bowl containing 300 ml of soup. The other half were given 500 ml. They were then instructed to imagine that they would be consuming the entire bowl of soup. The bowl was then removed and participants were presented with a pre-weighed empty bowl and a jug containing 1 litre of soup. They were asked to recall the amount of soup they had seen previously and to serve that amount into the empty bowl (participants were not pre-warned that their memory would be tested in this way). In a second task, participants were presented with a soup bowl containing either 300 ml or 500 ml, a jug of soup, and an empty bowl. They were instructed to pour soup into the empty bowl until they were equal in volume.
Independent samples
See 300 | See 500 | |||
Mean | S.D. | Mean | S.D. | |
Portion-size memory (immediate) | 433.8 | 99.7 | 572.6 | 109.4 |
Matching task | 491.9 | 54.9 | 648.2 | 20.6 |
To demonstrate that this discrimination persists in the memories of participants during the inter-meal interval, we recruited a further 20 participants and assigned them alternately to one of the two ‘incongruous eating’ conditions (either see 300 ml/eat 500 ml or see 500 ml/eat 300 ml). The protocol was identical to the first session in the main experiment except that participants were asked to return to the laboratory two hours after consuming the soup. They were then presented with a pre-weighed bowl containing 100 ml of soup (the amount remaining at the end of their meal) and a jug containing 1 litre of soup. They were then asked to recall and then serve the volume of soup they had consumed earlier. Across the two conditions, independent-samples
For the first time, we attempted to quantify the independent role of cognition (episodic memory) as a determinant of satiety in humans. This was achieved by covertly manipulating the amount of soup entering or leaving a soup bowl during a meal. Immediately after consuming the soup, hunger ratings were suppressed. Participants who consumed 500 ml reported a greater reduction in hunger than those who consumed 300 ml. We attribute this to the immediate proximal effect of the food promoting neural and endocrine signalling
Further into the inter-meal interval, a different pattern of results was observed. Two and three hours after the meal, hunger was no longer predicted by the actual amount consumed. This was the case despite the fact that participants ate either 300 ml or 500 ml of soup. Instead, where differences in hunger were observed, these related to the perceived amount at the beginning of the meal. Specifically, participants who were shown 500 ml of soup experienced greater satiety than those who were shown 300 ml. This result accords with Higgs’ original proposition that satiety is influenced by memory for a recently consumed meal
The prospect that satiety is influenced by memory for recent eating is consistent with studies exploring the role of expectations around mealtime. Several studies show that beliefs about the content or energy density of a meal can have a marked effect on subsequent hunger and fullness
One possibility is that memory for recent eating serves a purpose. Specifically, it may help to interpret post-ingestive signals by attributing them to a recently consumed meal
These ideas are important and well grounded. Nevertheless, they remain largely untested in humans. In particular, an opportunity exists to explore obese/lean differences in memory function and appetite control. One hypothesis is that diets that are high in saturated fat impair hippocampal function and that this leads to a deficit in memory performance
A potential concern is that the manipulation of perceived intake amounts to a form of deception that tells us little about normal appetite regulation. In response, we note that our volunteers were unaware that the volume of soup had been manipulated. This makes it very difficult to attribute our findings to a simple demand characteristic. An important issue relates to whether the memory for recent eating can be modified. Many everyday behaviours are supported by implicit memory
Our manipulation check indicates that participants are able to discriminate between a 300 ml and a 500 ml portion of soup and that this ability is also expressed in memory for these portions, both immediately after exposure and after a two-hour interval. This is critical, because it shows that memory is differentially influenced by our manipulation, even though participants are never instructed to encode the amount that they have consumed. In of itself, this does not demonstrate a causal relationship between hunger and memory for recent eating. However, this would seem a parsimonious explanation for our findings. Nevertheless, two alternatives merit consideration. First, the effect of perceived volume reflects subtle differences in the capacity of the (perceived) large and small portion to elicit a conditioned cephalic phase response at the time of ingestion
In addition to the immediate effects of memory on post-meal hunger and fullness, we also assessed effects on the expected satiation of a fixed portion of soup (400 ml) at a subsequent test session. Regardless of amount eaten, those participants who initially saw a smaller portion of soup (day 1) then went on to expect the 400 ml portion to be relatively less satiating (day 2). A likely explanation is that participants were biased by their recent post-ingestive experience. Those who initially saw a large portion then went on to experience a greater reduction in hunger. This memory for hunger then biased estimates of expected satiation 24-hours later. Although this interpretation remains to be tested formally, it is consistent with models that characterise the retrieval of abstract knowledge (expected satiation included) in terms of multiple activation of episodic memory traces
Previously, we have shown that expected satiation is dynamic and it ‘drifts’ over time
Finally, memory for recent eating is helpful because it enables us to draw on beliefs about a food, and in particular, beliefs relating to post-ingestive consequences. These expectations are likely to be governed by flavour-nutrient associations that are refined over time as we interact with individual foods
The authors acknowledge the assistance of Rebecca L Griggs in collecting data associated with our manipulation check.