The value of studying laboratory meals

The value of studying laboratory meals

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France Bellisle Nutritional Epidemiology Research Team (EREN), Paris 13 University, INSERM (U1153), INRA (U1125), CNAM, Bobigny, France

10.1

Introduction

A meal is a physiological, psychological, sensory, and ethological event. In animal species living in societies it is also a social event. While many other adjectives could be added to the list, the recognition that food intake behavior in animals (including humans) is associated with many diverse aspects of an individual’s experience creates very complex demands for any scientific attempt to describe, understand, and possibly explain and control this very basic, life-sustaining event. One critical aspect of food intake behavior is its periodic nature. Even under conditions of constant access to nutrient sources, intake is organized in a series of eating episodes, interspersed by other moments when the animal does not eat. These episodes, mostly occurring during the species-specific circadian activity phase, vary in number, in size, and in duration. In human societies, they also vary in composition, social context, and many other dimensions. Humans like to call their eating episodes “meals” or “snacks.” These terms are highly imprecise (Bellisle, 2014) and their definitions vary in different cultures, let alone different scientific contexts. “Laboratory meals” are specimens of such behavior. They allow the consumption responses of an individual to be examined in a particular context in which significant aspects of the environment are held constant, while others (sensory, social, psychological, etc.) vary under the strict control of the experimenters. Another critical aspect of food intake behavior is that it is essential to life, covering the bodily needs for energy and nutrients, with long-term repercussions on health and body weight control. The frequency of obesity and associated metabolic diseases has reached the proportions of a globalized epidemic. While experts debate the relative contributions of decreasing physical effort in developed societies and changes in the diet, it appears important to test a variety of hypotheses, particularly those involving critical mechanisms, under the strict conditions of the laboratory. A large number of determinants of meal consumption can be manipulated under laboratory settings: time of day, time of week, sensory stimulation, physiological status, ambience, temperature, social facilitation, and so forth. The laboratory is a privileged environment in which to conduct a scientific investigation of behavior under strict, reproducible conditions; to observe behavior repeatedly in the same individuals and study temporal changes or stability; to establish dose/ effect or exposure/effect relationship between causal factors and effect; and to draw Context. https://doi.org/10.1016/B978-0-12-814495-4.00010-6 Copyright © 2019 Elsevier Inc. All rights reserved.

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parallels between animal observations and human responses to well-defined influences. Tightly controlled laboratory tests offer a high degree of sensitivity and control over the intervention and the outcome measures (Blundell et al., 2010). In the following pages, we will look at the historical roots of the laboratory study of food intake behavior in humans. We will then examine a few characteristics of the laboratory context itself as it developed from early pioneer days to the present. Illustrative examples of the methods and results typical of the laboratory studies will be presented in the examination of the “Satiety Cascade” and the “preload paradigm.” A section will cover the specific demands of the laboratory study of the human appetite. Finally, the important question of the generalization of laboratory observations and other difficulties of the laboratory approach will be discussed.

10.2

A brief historical perspective

The laboratory investigation of appetite was born in the 19th century physiology laboratory. In the mid-19th century, Claude Bernard posed the foundations of the study of experimental medicine (Bernard, 1865) and realized important physiological studies (particularly in the physiology of nutrition) that led to the concept of the “milieu interieur,” the internal environment. In animal species, the constancy of the milieu interieur is an essential condition for survival. Many parameters of this internal status need to be regulated within the narrow limits of what Cannon (1932) later called “homeostasis”: the body temperature and glycemia for example. It soon became evident that while powerful physiological processes come into play to insure regulation, they need to be complemented by the animal’s active behavior in order to complement internal processes. While the pancreas releases hormones to maintain glycemia within regulated limits, food intake has to take place periodically in order to supply the organism with adequate energy and nutrients. Following the scientific investigation of the various internal mechanisms involved in energy and nutrient regulation under strict laboratory conditions, it became evident that research had to extend its domain to behavioral responses that complement internal ones. In this perspective, behavior appears to be a natural extension of regulatory mechanisms. For many heirs of the physiological tradition, the laboratory appeared a logical place to study its role, under the strict rules of the experimental method. The search of physiological factors that affect and even define motivational constructs such as hunger and satiety (Blundell, 1979; Le Magnen, 1992) was at the origin of laboratory research. The nature of the “hunger signal’ that triggers food intake has generated much research. In turn, identifying the laws governing behavior, not only eating but also other regulatory or non-regulatory behaviors, owes a lot to the laboratory investigation of physiological responses associated with eating. The discovery and mechanistic analysis of the conditioned reflex by Pavlov (1927) is the example par excellence. A dog salivates when meat is ingested (an unconditioned response) and also in anticipation of eating, when various characteristics of the environment have become associated with the imminent access to meat (a conditioned response). Conditioned responses such as salivation and other aspects of the “cephalic phase of

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digestion” (Powley & Berthoud, 1985; Teff, 2011) in turn affect digestive processes, and food motivation in future ingestive episodes. The sensory characteristics of familiar foods themselves become conditioned cues that predict the postingestive effects of consumption. Their predictive value is constantly updated via successive exposures so that they determine a person’s food preferences and motivation at various moments of the lifetime, what recent science calls “liking” and “wanting” (Berridge, 2004; Finlayson, King, & Blundell, 2007). The study of gastric secretions at the time of meals in dogs led to the demonstration of a far reaching mechanism of adaptation to the environment, the conditioned reflex, that applies in numerous areas of life. Subsequent developments in behavioral science used laboratory tests of food consumption in animals or humans to demonstrate and elucidate the mechanisms of instrumental conditioning. From Watson (1926) to Skinner (1938), the demonstration of the laws of instrumental learning, which clearly reach well beyond food consumption responses, were studied in laboratory settings, where independent factors (type, number, duration, frequency, intensity of food rewards) could be demonstrated to elicit measurable and predictable changes in strictly measured, dependent consumption responses (number, frequency, intensity, persistence, etc.). Examining animals in their natural environment confirmed the validity of laws of learning identified from laboratory observations, and showed how species-specific fixed action patterns and environment-specific influences modulated the performance of learned responses (Domjan & Burkhard, 1986). In the history of behavioral science, food intake was viewed as the behavioral mechanism insuring regulation of critical parameters of the internal milieu. Classic theories of food intake control focused on specific regulated parameters. Jean Mayer’s glucostatic theory of eating behavior held that, while the blood glucose level is regulated within narrow limits by hormonal mechanisms, food consumption is triggered periodically by decreases in the rate of use of glucose (Mayer, 1953). The most direct test of the glucostatic hypothesis, the observation of a hungry animal’s or person’s eating behavior following an injection of glucose, can only be performed under strict laboratory conditions. Mayer’s early works have led to the search for glucose sensors in the brain, and of the brain structures that command eating behavior as a response to changes in glucose utilization. Early research identified a “hunger center” and a “satiety center” in the hypothalamus, whose activation/inhibition stimulated or inhibited eating (Anand & Brobeck, 1952; Hetherington & Ranson, 1940; Hoebel & Teitelbaum, 1962; Stellar, 1954). Other physiology-oriented theories of food intake control followed. The lipostatic theory, originally proposed by Kennedy (1953), held that the amount of fat in the body was the regulated parameter that stimulated or inhibited eating in order to maintain the body fat mass constant. The discovery of leptin, the “hormone of satiety” secreted by the adipose tissue and capable of inhibiting food intake, has since brought support to the lipostatic theory (Zhang et al., 1994). From the early days of the regulatory theories up to the present, the notion that eating is triggered and controlled by the fluctuations of physiological parameters in the brain or in the periphery of the body has led to the development of laboratory methods to test the influence of nutrients, hormones, peptides, and so forth on characteristics of eating behavior in the context of a laboratory in which both independent and dependent variables can be measured with precision.

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10.3

The laboratory context

Studying meals in the laboratory context is a potent method when a precise mechanism of action of a particular factor of interest on food consumption has to be elucidated, allowing a high degree of control. For example, when a dose/response function is to be quantified between the levels of a particular factor (fasting duration, portion size, intensity or diversity of sensory stimulation, etc.) and some aspect of responding (meal size, rate of eating, experience of palatability, etc.) the laboratory context offers the possibility of experimentally manipulating the levels of the factor of interest and quantifying precise changes in the response. It makes it possible also to examine how the consumption response itself affects other aspects of appetite, for example, satiety. In all these situations, clear operational definitions of independent and dependent variables must be used in an experimental protocol designed to test a causal hypothesis. Physiological or sensory effects on consumption can be quantified in this fashion, and also social or affective influences (presence/absence of other persons at the time of eating (Cruwys, Bevelander, & Hermans, 2015); influence of parents, friends, or unfamiliar persons (Hermans, Herman, Larsen, & Engels, 2010; Mennella, Griffin, & Beauchamp, 2004), and environmental conditions (Bellisle & Dalix, 2001). Many important contributions of laboratory work to the understanding of human appetite have been published over the years. Examples of such situations are found in -

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studies addressing how specific tastes and flavors influence liking and consumption of foods (Yeomans, 1998) and how these effects are mediated by certain brain peptides (Yeomans & Gray, 2002). the inventory of the numerous factors (physiological, sensory, psychological, social) present at the time of ingestion that affect various aspects of consumption (meal size, ingestion rate, experienced palatability and satiation, etc.) (Blundell, 2017). the observation and assessment of a purely sensory mechanism affecting satiation and satiety, independently of postingestive metabolic effects. “Sensory-specific satiety” was first identified in human laboratory works by Rolls, Rolls, Rowe, and Sweeney (1981), and then studied in many other laboratories (Hetherington, 2013). the measurement of various aspects of the “cephalic phase of digestion” that occurs at the beginning of ingestion, and can exert a variety of effects on later appetite and metabolism (Bellisle, Louis-Sylvestre, Demozay, Blazy, & Le Magnen, 1983; Teff, 2011). the scientific discussion of the satiating value of energy ingested in liquid form versus solid foods (Allison, 2014; Allison & Mattes, 2009). the parallel investigation of the action of certain influences in different species, for example when methods derived from animal work are used in a human study for measuring the reward value of foods and the motivation to consume (Hogenkamp, Shechter, St-Onge, Sclafani, & Kissifeff, 2017). the recent development of the study of brain responses at the time of food stimulation. A recent report showed how neuromodulation directed at the prefrontal cortex of obese individuals decreased their snack food intake and hunger (Heinitz et al., 2017). In this study, transcranial direct current stimulation, a noninvasive technique used to modulate brain activity, modified subjects’ responses in a vending machine paradigm and during snack food taste tests. the investigation of changes in ingestive responses over time in the same individual, by repeated testing in a controlled eating situation. Learning effects, habituation effects, or

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changes occurring in the participant’s mental or physical status can then be quantified. Changes in acceptance of novel flavors in bottle-fed infants, for example, have been followed over several months in laboratory tests (Mennella et al., 2004). Learning, based on previous experience with foods, has been shown to modulate “expected satiety” at the beginning of a meal and affect the amount of food an individual ingests (Yeomans, McCrickerd, Brunstrom, & Chambers, 2014). the optimization of the sensory characteristics of foods and beverages investigated in numerous academic and industry laboratories (for example, in the field of salt effects on palatability, Bolhuis, Lakemond, de Wijk, Luning, & de Graaf, 2010, 2012).

10.3.1 The “Satiety Cascade” Food consumption is a periodic behavior. It is triggered at various moments of the day by a number of converging factors (time of day, need state, sensory stimulation, social context, etc.). As eating progresses, inhibitory influences of many origins (sensory, gastric, hormonal, neural, as well as cognitive) develop and finally bring the meal to an end. Satiation is the complex inhibitory process that integrates these influences and terminates a meal. Satiation determines meal size. After the end of one eating episode, many factors contribute to inhibiting further eating until the next meal. These stimulatory and inhibitory influences were conceptualized as the elements of the “Satiety Cascade” first described over 30 years ago (Blundell, Rogers, & Hill, 1987) and regularly updated since then (Blundell et al., 2010; see Fig. 10.1). The Satiety Cascade integrates sensory, cognitive, postingestive, and postabsorptive factors that inhibit the motivation to eat again for a certain time. Because satiation and satiety have to do with the inhibition of appetite, they are considered potent mechanisms determining total daily energy intake and, on the long-term, body weight control. Studying the causal factors involved in satiation and satiety is therefore central to the understanding of appetite and ingestive responses. Laboratory studies have largely contributed to quantifying the action of many factors at various moments of the satiety cascade (Blundell, 2017).

10.3.2 The preload paradigm In order to investigate satiety influences, laboratory studies of meal intake use highly standardized paradigms that facilitate the quantification of causal relationships. The preload paradigm is one typical methodological approach that has been applied in a large number of human and animal works. In the “preload paradigm,” a load of food is ingested at a fixed interval before a subject (animal or human) has ad libitum access to food (Fig. 10.2). It is therefore possible to measure how the parameters of the load (nutrient composition, energy content, sensory aspects, etc.) will affect ingestive responses. For example, it is possible to see whether any energy or nutrient compensation occurs at the ad libitum meal to adjust for the contents of the preload. When testing human subjects, changes in subjective appetite sensations can be followed in the interval between preload and ad libitum intake. Using a slightly modified version of the paradigm, it is also possible to study the duration of the inhibition of intake induced by a preload: in these

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Energy balance

Meal quality Expectations Reward/Pleasure Recognition Associations

Stretch Osmotic load CCK GLP-1 PYY Ghrelin

Sensation + prior beliefs and associations

Sensory

FOOD Satiation

Insulin Leptin Adiponectin(?)

Meal quantity

Stomach + intestines

Cognitive

Nutrient status Insulin Oxidation Glucose Amino acids

Fat-free mass Fat mass RMR

Liver + metabolites

Postingestive

Postabsorptive

early

late

Satiety Original Satiety Cascade modified by Mela and Blundell

Fig. 10.1 The satiety cascade. The satiety cascade was originally presented in Blundell et al. (1987). It is periodically up-dated to integrate new scientific findings. Source: Blundell, J. E., de Graaf, K., Hulshoff, T., Jebb, S., Livingstone, B., Lluch, A., et al. (2010). Appetite control: Methodological aspects of the evaluation of food. Obesity Reviews, 11, 251–270.

Appetite ratings Preload

Hunger, fullness, desire to eat, thirst

Ad libitum meal

Variable interval: 15 min to 6 h

Time

Expectation: Subjects ingesting a preload will eat less at next meal

Fig. 10.2 The preload paradigm. Typically, under repeated-measure designs, participants are tested at the same time of day, under identical deprivation conditions. Standardized preloads are ingested. After a variable time delay, the effects on spontaneous food intake are measured. Subjective measures of appetite are often obtained at predetermined time intervals after the preload and/or the test meal. The preload can be overtly or covertly manipulated in order to test the satiating potency of many factors: energy content, energy density, sensory characteristics, nutrient composition, presence of potential satiety-enhancing factors, etc.

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circumstances, the postmeal interval is not determined by the experimenter, but is allowed to vary until the subject will spontaneously initiate the following meal. Over the years, the preload paradigm has given rise to a substantial inventory of factors that influence the amount of food eaten, and other aspects of satiety (Blundell, 2017), among which -

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The energy density of the preload has a major effect on satiety, for a given energy content (Rolls, Bell, & Waugh, 2000). For an equivalent energy load, a hierarchy of satiating potency exists between the macronutrients: protein induces stronger satiety than carbohydrates, which in turn induce more satiety than fats (Veldhorst et al., 2008). The presence of fiber in a food enhances its satiety effects (Drapeau & Tremblay, 2000; Lluch et al., 2010). Physical phase affects satiety: energy ingested in liquid form elicits less satiety than the same energy load ingested in solid form. This robust observation, confirmed in numerous controlled laboratory studies, suggests a “passive overconsumption” of energy ingested in beverages facilitating weight gain (Almiron-Roig et al., 2013; Mattes, 2006). Various non-nutrients and bioactive food constituents, such as caffeine, enhance satiety (Tremblay & Bellisle, 2015). The importance of texture: viscosity of a beverage contributes to increasing its satiating power (Mattes & Rothacker, 2001).

In the preload paradigm, the temporal succession of events has to be strictly controlled. The preload paradigm requires laboratory conditions in order to yield valid results. It is important, to test how well the results obtained under laboratory settings generalize to the free-living conditions. One very active area of research is the exploration of how satiety effects generalize to long-term, free-living, food consumption, and possibly confirm that satiety enhancement is indeed a means to decrease long-term food intake and beneficially affect body weight control (Tremblay & Bellisle, 2015). Many publications have brought support to this idea. For example, Rolls, Roe, Beach, and Kris-Etherton (2005) provided foods with low energy density to dieters for one year, and observed that weight loss was improved by 50% compared with control.

10.3.3 The laboratory as a microcosm of the eating environment In a laboratory study, the experimental environment reproduces one eating situation where behavior is measured. In animal studies, the laboratory situation cannot possibly reproduce all the characteristics of the wild eating environment. It is highly important, however, to make the laboratory eating environment compatible with the animal’s species-specific action patterns. Among several crucial dimensions, respecting the circadian activity/rest phase is important. Nocturnal animals should be tested during the dark phase of their circadian cycle. Many other ethological factors, such as preferred food texture (a strong acceptance factor in rodents, for example), should be taken into consideration. In human studies, a small fraction of the numerous influences that affect eating in free-living conditions can be imported into the lab. This requirement will always raise

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legitimate questions about the generalization of the observed responses from the lab to naturalistic conditions. But it will also allow specific influences to be manipulated in controlled ways in order to quantify their impact on specific aspects of the response. This cannot be done with the same degree of control in the free-living environment, where so many influences vary at the same time in unpredictable and unreproducible ways. The human food intake laboratory can take many forms. In its simplest form, it can look like a sensory evaluation booth. Very elementary food stimuli, at times liquid foods of known sensory and nutrient value, can be presented to a human subject, and his/her consumption behavior can be quantified (amount, duration, rate of eating, etc.) Even such basic forms of laboratory environment have yielded interesting information about human appetite. Under such circumstances, it has been shown, for example, that the preferred intensity of sweetness will differ depending on whether the experimental food, let us say a yogurt, is swallowed or not (Lucas & Bellisle, 1987). Other food consumption laboratories can be much more complex. Many laboratories are disguised as small dining rooms or even small restaurants or cafeterias. In preload studies, the participant’s self-selected food choices at the ad libitum test meal are often studied, as well as the energy or nutrient composition. In such situations, a cafeteria-like buffet is served for the subjects to select their preferred food options in a realistic context. The buffet style allows assessment of the potential effect of a preload manipulation on food choices (in terms of preference and/or avoidance, selection of foods based on sensory characteristics and/or energy density, etc.), even if the energy intake at the meal remains constant (Blundell et al., 2010). In recent years, many food consumption laboratories have developed into highly complex environments, replicating plausible eating places for human consumers at certain moments of the day. One example of such sophisticated environments is the Living Lab of the Institut Paul Bocuse, in Lyon, where study participants have their meals in a pleasant restaurant-like environment, while their behaviors are measured using video recordings, and food options are designed to test specific hypotheses about human appetite. Validation studies have shown that the parameters of intake recorded under identical test conditions in this environment are reproducible and sensitive to variations of hunger states (Allirot, Saulais, Disse, Roth, & Cazal, 2012). In most academic laboratories, however, meal menus are not as elaborate as the Bocuse dishes, and merely represent a selection of popular food options (pizza, macaroni and cheese, cookies, candy, and water) (Carnell et al., 2018). These options are not different in the context of a lab or in naturalistic settings. In naturalistic conditions, consumers select foods that have at least middling palatability levels (de Castro, Bellisle, & Dalix, 2000; de Castro, Bellisle, Dalix, & Pearcey, 2000). In the laboratory, most food is usually selected to have at least acceptable palatability, or it is ascertained that the participating subjects will have at least minimal acceptance of the test foods. In some cases, low palatability food stimuli can be used, particularly in tests of the influence of sensory factors on some aspects of the ingestive responses. The circumstances of eating in free-living conditions are highly diverse, and humans in their history have found themselves eating in all sorts of social and material conditions where the eater has limited control over his/her environment. The laboratory is one more such situation. The experimenter selects a sub-set of factors to

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examine their influence on meal eating. Although the laboratory can be a very simplified environment, it can also integrate a large number of variables of interest: not only types and characteristics of foods, but also time of day (or week or season), social environment (eating alone or in company), ambiance factors, and characteristics of the consumers (age, sex, ethnicity, motivational attitudes such as dietary restraint or emotional eating, etc.). Whatever the level of sophistication, care must be taken to keep important influences under strict control: -

the social context is important, so the laboratory should make sure that no unwanted social influences impinge on the consumer’s responses during the meal; attention to the meal is important, so potential distractors should be strictly controlled; temperature and other ambiance factors should be constant, particularly in repeated testing situations.

10.3.4 The human meal as an independent or a dependent variable The laboratory offers a controlled environment in which the numerous influences that affect meal intake can be studied; it also allows an investigation of how meal intake itself can affect other aspects of appetite or behavior. In other words, in a laboratory context, meal intake can be studied as an independent or as a dependent variable. For example, meal size and eating rate can be affected by factors such as palatability or texture (Bellisle & Le Magnen, 1980). Conversely, eating rate at meal time can affect postprandial satiety effects (Ferriday et al., 2015). Some ambitious protocols use food intake under laboratory conditions as both an independent and a dependent variables. For example, a recent study looked at morning and afternoon appetite in obese individuals with or without binge eating disorder (Carnell et al., 2018). After an 8 h fast, the participants first received a standardized liquid meal of fixed composition, then a stress test. Access to an ad libitum buffet was allowed 2 h 40 min after the liquid load. Appetite and stress were monitored using rating scales, and blood was drawn for hormone measures. This study illustrated why and how the afternoon/evening represented a high-risk period for overeating, particularly in individuals with binge eating disorder exposed to stress.

10.4

The demands of laboratory testing of human food consumption

The study of human meal intake under laboratory conditions is not a novel area of research. Over the years, researchers have developed specific tools and gained expertise from repeated testing in laboratory conditions. The emerging picture is that the laboratory is a highly controlled environment to gain access to some of the determining influences of human appetite, but also a very demanding one. A number of review papers have been published about the methodological demands associated with the

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study of human appetite under laboratory settings (for example Blundell et al., 2009, 2010; Chapelot, 2013).

10.4.1 The design of the laboratory test meal The value of data obtained under laboratory conditions will critically depend on the hypothesis tested, and the adequacy of the protocol. Operational definitions of the critical variables should be established at the outset of the project. It is important to insure adequate statistical power with a sufficient number of participants, and an adequate statistical analysis plan that will permit significant effects to be identified. The validity (internal and external) and reliability of the critical variables should guide the elaboration of the testing situation. The food stimuli and the conditions of their presentation should be thoroughly considered, as well as the time sequence of all relevant events taking place in the experimental situation. A special attention should be paid to potential confounders, which are numerous when considering human behavior in general, and human eating behavior in particular (time of testing, appropriateness of the food stimuli, individual characteristics such as body weight status or psychological attitudes, including dietary restraint, etc.).

10.4.2 The demands of preload studies The preload paradigm has benefited from the cumulative experience of research teams working on satiety or other aspects of postingestive appetite. Detailed advice for efficient standardization has been published (Blundell et al., 2010; Chapelot, 2013; Kissileff, 1985). Standardization of preloads in terms of energy content, macronutrient composition, energy density, physical state (solid vs. liquid), weight or volume, and sensory and cognitive characteristics is important, as well as the full characterization of the test situation: conditions of the ad libitum meal (single food versus buffet, social surroundings, etc.), time sequence of preload and test meal administration, and the nature and duration of the appetite measurements between preload and test meal, or even following the test meal (Blundell et al., 2010).

10.4.3 Assessing subjective motivation associated with meals The use of self-report tools for the assessment of subjective appetite prior to, during, or following a laboratory meal is also a frequent procedure used in laboratory settings. These tools have developed from paper-and-pencil instruments to hand-held electronic devices. They typically address such aspects of motivation as experienced hunger or fullness at specific times relative to ingestive events. Many formats have been standardized and validated over the years. The most frequently used is the horizontal visual analogue scale marked at both ends with anchors expressing the extremes of a given sensation (hunger or fullness, for example). These validated tools provide data with good sensitivity, reliability, and validity (Flint, Raben, Blundell, & Astrup,

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2000), especially when appetite ratings are expressed over several hours as area under the curve (AUC), rather than absolute value of discrete points.

10.4.4 The laboratory as a nonnatural environment The laboratory testing of meal intake in human subjects by no means implies that the circumstances of the test have to be “artificial” relative to free-living food consumption. The foods served do not have to be “artificial” foods. Of course, simplified or elementary food stimuli have to be used under certain circumstances (such as liquid foods ingested from a straw), but they can also be anything from cocktail-size sandwiches to elaborate dishes. Many satiety and functional claims have been tested under laboratory conditions using novel foods, or novel recipes of familiar foods, designed by the industry for the purpose of the test (see, for example, the yogurt studies by Lluch et al., 2010). The measuring instruments can be wearable sensors designed to be as light and non-obtrusive as possible. Considerable progress has been made in this area over the years (Bellisle & Le Magnen, 1980; Fontana et al., 2014). Studies used discrete cameras that scan a dining room, or hidden scales that continuously weigh the amount of food being ingested without any interference with the subject’s behavior. The experimental room where intake behavior takes place does not need to look like a stern sensory evaluation booth or a hospital room. It can be decorated as a restaurant or cafeteria typical of places where people frequently have their “free-living” meals. Recent works have developed the notion of a “simulated context,” a naturalistic consumption situation reproduced under laboratory conditions (Holthuysen, Vrijhof, De Wijk, & Kremer, 2017) as a cost-effective procedure that combines increased experimental control with the realism of the simulated context. Various means can be used in order to evoke a realistic meal situation in the laboratory, among which is the use of recent technological advancements in virtual reality or augmented reality, which can create increasingly realistic and immersive environments (Zandstra & Lion, 2018).

10.5

Limitations of the laboratory approach

10.5.1 External validity issues The study of human behavior under laboratory conditions is often criticized for being “artificial” and non-representative of spontaneous, free-living responses. Questions about external validity are legitimate, but are by no means limited to laboratory testing. Just because a behavior has been observed out of the laboratory does not guarantee that it generalizes to all other free-living circumstances. A lot can be done to increase the “naturalness” of the test laboratory and, as long as this is compatible with the demands of the protocol, quite a few of the characteristics of a naturalistic eating environment can be imported into the laboratory. The external validity of laboratory findings remains an important question that requires adequate testing under the

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relevant free-living conditions. It is highly important, for example, to determine whether the potent satiety effects that have been observed under laboratory conditions will be reproduced in free-living consumers, and whether the enhancement of satiety will be sufficient to affect long-term appetite and body weight control (Bellisle & Tremblay, 2011).

10.5.2 The ‘Hawthorne effect’ One obvious limitation of studying human behavior under laboratory conditions is the potential loss of spontaneity and associated distortions. The “Hawthorne effect,” the propensity to change one’s behavior as a result of being observed, is inherent in all scientific studies of human behavior, whether in the field or laboratory. Naturalistic observation conditions can, at times, make the observation procedures less salient than they are in controlled laboratory environments. In some circumstances, however, the observation tools clearly affect the observed behavior. Under naturalistic conditions, the simple fact of keeping a food diary makes people eat less; in behavioral therapy programs for weight loss, the food diary is used not only for dietary assessment, but also as a tool to decrease intake (Butryn, Webb, & Wadden, 2011). Likewise, an individual whose behavior is observed under laboratory conditions, and who is fully aware that his/her behavior is being observed, can consciously or unconsciously modify his/her behavior to please the experimenter, or to displease the experimenter, or simply to give the best possible image of him/herself. Again, this is not only true of laboratory conditions, but the salience of measurement procedures under laboratory settings could amplify the distortion.

10.5.3 Expectations and demands of the experimental settings Scientific research requires approval by ethical committees and, in human studies, participants must be fully informed from the outset of what is expected from them in a particular experimental test. Although this is true in every human experiment, informing participants of the nature of the test without influencing participants’ behavior is often a major challenge. Laboratory testing can create expectations, perhaps worries, and consequent distortions in the behavior. Experimenters should remain aware of these potential sources of bias, and try to minimize their effect from the elaboration of the protocol to the final interpretation of the results. One strategy that can be used, although it has substantial costs, is to have the participants go through the experimental procedure once, without any testing being done, before the start of the actual experiment.

10.5.4 Duration limits The duration of any laboratory test of behavior is obviously limited. Human subjects, adults or children, cannot possibly remain under laboratory conditions for more than a few hours or a few days. Most laboratory tests of human food intake last for a few hours: the time required to record the actual meal consumption, plus a few minutes

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prior to the meal (for example in preload studies) and/or up to a couple of hours after the meal (to study the early parts of the satiety cascade). While the information gathered from such studies has been immense, they cover only a small part of the feeding circumstances in a human life. In order to increase the control over important variables, many researchers extend the observation or experimentation phase to longer durations. Typically, participants arrive at the laboratory early in the morning after a night fast, have breakfast, remain under controlled conditions during the morning, have a preload, then are served a test meal 1–2 h later, and remain in the laboratory for a while after lunch. Each of these events can be manipulated for experimental purposes, and/or can be selected for the measurement of some critical aspect of the response. One example is found in a test of a hand-held electronic data capture method for the continuous monitoring of subjective appetite sensations: participants arrived at the lab prior to breakfast, in the fasted state, and then had a fixed breakfast; an ad libitum lunch was served 4 h after breakfast; and the participants’ appetite sensations were rated every thirty minutes until after lunch termination (Gibbons, Caudwell, Finlayson, King, & Blundell, 2011). Studies of the adaptation of energy intake to changing conditions of the food supply can be continued over several days in subjects housed in wards where their food intake can be observed and measured. Food intake behavior over 24 days was examined in response to the covert 25% decrease in energy density of the diet, showing a slow, progressive adaptation of spontaneous consumption (Porikos, Hesser, & Van Itallie, 1982). In a study of genetic factors affecting body weight, twins were maintained for 100 days in a metabolic ward where they were overfed by 1000 kcal a day (Bouchard et al., 1990; Bouchard, Tchernof, & Tremblay, 2014): in these circumstances, food intake was used as a controlled independent variable whose effects were studied on weight changes and associated metabolic responses.

10.6

Conclusions and consideration for future developments

The laboratory meal is a highly useful context for studying several aspects of appetite control in human consumers. Its high internal validity, the reliability of validated tools, the control over independent variables, and the precision of operational definitions are a few of its merits. It simplifies the array of factors susceptible to act on the behavior of interest, and it is optimally used over short periods of time. It has produced large amounts of precious information about the determinants of food intake. Particularly, biological factors affecting hunger and satiety have been characterized, and causal links have been quantified. The value of the laboratory context for the investigation of human appetite depends on the aims of the hypothesis being tested and the quality of techniques used by the experimenter. Improvements in methodology have occurred over time to address some of the limitations classically associated with laboratory studies of human behavior. The foods served and the circumstances of eating can often be very close to what they would be under every day eating conditions. Important laboratory works have been published

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using representative foods, served in realistic eating places, including social interactions, all under the strict experimental control allowed by the laboratory. Over the years, laboratory meals have become increasingly similar to free living eating events as experimenters became more informed and skillful. In appetite research, compromises have to be made about the requirements for internal and external validity, between precision and naturalness (Blundell et al., 2010). There is no absolute border with laboratory science on one side and free living observation on the other. Many features of the free living environment can be imported into the appetite lab, and measurement instruments initially developed in the lab context can be exported to free living research contexts. While the optimal protocol is likely to vary depending on the hypothesis and the type of factors and mechanism at play, overlapping laboratory and free-living protocols can often be used in a variety of contexts in order to address appetite from complementary perspectives.

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Further reading Blundell, J. E., & Bellisle, F. (Eds.), (2013). Satiation, satiety and the control of food intake. Cambridge: Woodhead Publishing. French, J. R. P. (1953). Experiments in field settings. In L. Festinger & D. Katz (Eds.), Research methods in the behavioral sciences (pp. 98–135). New York: Holt, Rinehart & Winston (Chapter 3). Sclafani, A. (2004). Oral and postoral determinants of food reward. Physiology & Behavior, 81, 773–779.