Chocolate Craving and Hunger State: Implications for the Acquisition and Expression of Appetite and Food Choice

Appetite, 1999, 32, 219–240 Article No. appe.1998.0207, available online at http://www.idealibrary.com on

Chocolate Craving and Hunger State: Implications for the Acquisition and Expression of Appetite and Food Choice

E. L. GIBSON and E. DESMOND ICRF Health Behaviour Unit, Department of Epidemiology and Public Health, University College London

The importance of hunger state for the acquisition and expression of chocolate craving was investigated. Seventeen chocolate cravers and 12 non-cravers were supplied with chocolate and instructed to eat some twice a day for 14 days. Within each group, subjects were allocated to one of two conditions, hungry- or full-trained. Hungry-trained subjects were asked to eat the chocolate exclusively at least 2 h after last eating; full-trained subjects were asked only to eat the chocolate 15–30 min after eating a meal. A diary was kept to encourage and allow assessment of compliance. At the start and end of the 2 weeks, subjects rated their craving for and anticipated intake of chocolate prior to eating it; then, on initial tasting, pleasantness of the taste was rated. All subjects made these ratings on one day when hungry and on another when full, as defined above. For cravers and non-cravers who ate chocolate exclusively when hungry, chocolate craving increased post-training, but, at least for cravers, only when ratings were made while hungry. For full-trained subjects, chocolate craving decreased posttraining, but this decrease did not depend on whether subjects were currently hungry or full. A similar pattern of results was found for anticipated intake and pleasantness of taste, except that pleasantness did not increase in hungry-trained subjects. The results are interpreted with reference to learned control of appetite and in particular to recent findings on incentive learning processes. Craving for chocolate or other foods may be an expression of a strong appetite elicited by hunger that has been acquired by repeated experience of eating the craved food when hungry.  1999 Academic Press

I The concept of craving for foods, of which chocolate is the dominant example, has received considerable attention in recent years, both in the lay media (Howarth, 1997) and in the scientific literature (Hill & Heaton-Brown, 1994; Macdiarmid & Hetherington, 1995; Rogers, 1995; Rozin et al., 1991; Weingarten & Elston, 1991). Explanations for chocolate and other food cravings remain diverse and controversial Leigh Gibson is supported by the Imperial Cancer Research Fund. The authors are very grateful for the advice provided by Professor Jane Wardle (Director, ICRF Health Behaviour Unit) and Dr Charles Legg at the City University, London, where this work formed part of Eska Desmond’s B.Sc. project. The authors are also grateful to Cadbury Ltd (Bourneville, U.K.) for the generous donation of Cadbury’s Dairy Milk chocolate. Address correspondence to: Dr E. L. Gibson, ICRF Health Behaviour Unit, Department of Epidemiology and Public Health, University College London, 2-16 Torrington Place, London WC1E 6BT, U.K. 0195–6663/99/020219+22 $30.00/0

 1999 Academic Press

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(Max, 1989; Michener & Rozin, 1994; Schuman et al., 1987). Yet the cravings for food appear to be experienced by between 60 and 97% of respondents, depending on the sample studied (Rodin et al., 1991; Rozin et al., 1991; Weingarten & Elston, 1991), and so call for further scientific investigation. An enduring theme has been that chocolate craving is the subjective manifestation of an addication to psychoactive chemicals contained in cocoa (di Tomaso et al., 1996; Max, 1989). There are, however, a number of difficulties for the acceptance of this drug addiction model. The cocoa in chocolate contains several potentially psychoactive chemicals, for instance the sympathomimetic biogenic amines, tyramine and phenylethylamine, and the methylxanthines, theobromine and caffeine (Hurst & Toomey, 1981; Max, 1989). Nevertheless, for this to be a likely mechanism for chocolate “addiction” or craving, certain conditions should be met: first, the active ingredient(s) should be measurably stimulant, euphoric or at least reinforcing when taken orally in appropriate dosage; second, such cravings should occur for all foods containing sufficient of these substances (assuming adequate exposure), but not for foods that do not; third, the craving should be at least partly reduced by ingestion of the active ingredients even in the absence of ingestion of the craved food. Few data are available on reinforcing effects following ingestion of chocolate (or other craved foods). Biogenic amines in food are metabolized by enzymes such as monoamine oxidase (MAO) in the gut and liver, so that they would not be expected to reach the brain (Karoum et al., 1979; Marley & Blackwell, 1970). Nevertheless, MAO activity can vary naturally across individuals and is known to be low in migraine sufferers (Sandler et al., 1974), which might explain their susceptibility to provocation by certain foods, including chocolate. Even so, in patients who believed that cocoa-containing products precipitated their migraines, ingestion of either chocolate or a relatively high dose of 2-phenylethylamine (3 mg) did not consistently affect electro-encephalographic activity, let alone produce a reinforcing effect (Scott et al., 1977). In contrast to the biogenic amines, methylxanthines ingested in foods or drinks can reach the brain in psychoactive amounts (Tarka, 1982). Furthermore, chronic caffeine users appear to suffer withdrawal which may contribute to maintenance of caffeine use habits (Rogers et al., 1995). Yet, liking for or “addiction” to caffeinecontaining beverages does not appear to be associated with chocolate craving or liking (Rozin et al., 1991). Also, caffeine levels in chocolate are typically rather low, whereas theobromine is normally present in more substantial amounts (Max, 1989). Although such levels of theobromine may be discriminable by some individuals (Mumford et al., 1994), it is not clear whether this is a central or peripheral effect, the latter being more likely given that theobromine does not readily enter the brain (Tarka, 1982), and there is as yet no evidence to suggest that the amount of theobromine obtained from chocolate would provide stimulant or reinforcing effects. Recently, di Tomaso et al. (1996) isolated a putative neuromodulatory ligand of brain cannabinoid receptors, anandamide and two related lipid compounds, Noleoylethanolamine and N-linoleoylethanolamine, from cocoa powder (but not from white chocolate). Di Tomaso et al. (1996) suggested that these latter two cannabinoids might contribute to chocolate craving by prolonging the availability of anandamide, but against this it should be noted that, amongst self-reported “chocolate addicts”, eating chocolate resulted in increased feelings of guilt, without changing feelings of depression or relaxation (Macdiarmid & Hetherington, 1995).

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The second problem for an explanation of chocolate craving based on an “addiction” to effects of biogenic amines is that many of these substances are present in a wide variety of foodstuffs. For instance, cheese, yeast extract and pickled herrings can contain remarkably high amounts (1–3 mg/g) of the sympathomimetic tyramine (named from “tyros”, Greek for cheese) (Marley & Blackwell, 1970). Smaller amounts are present in fruits such as bananas and tomatoes, as well as in a variety of meat and dairy products (Hurst et al., 1982), while concentrations of amines including phenylethylamine in different chocolate brands can vary by at least a factor of 10 (Hurst & Toomey, 1981). Even if it were argued that some people may crave some of these foods some of the time, on this basis the presence of amines in food does not seem to provide a convincing explanation for the dominance of chocolate amongst craved foodstuffs. The third issue as to alleviation of craving by ingredients was addressed by Michener and Rozin (1994). Their results were that cocoa powder alone did not reduce craving any more than placebo capsules or nothing, while white chocolate, with or without cocoa powder capsules, reduced craving to some extent, but not as effectively as milk chocolate (though that may be influenced by expectation). Thus, ingestion of the cocoa ingredients had no impact on chocolate craving, while the sensory similarities of white chocolate to milk chocolate (sweetness and cocoa butter) allowed a significant if partial alleviation of craving. Another proposal is that chocolate craving represents a need to achieve stimulation of endogenous opioid receptors, akin to opiate drug addiction (Drewnowski et al., 1992; Mercer & Holder, 1997). However, evidence for opioid mediation of responses to preferred food stimuli implicates many sweet and fatty foods for which there is little evidence of craving (Blass et al., 1989; Cooper et al., 1988; Yeomans & Wright, 1991; Yeomans et al., 1990). Furthermore, an endogenous neurochemical response elicited by sensory stimuli seems more appropriate as a mechanism underlying reinforcement generally, rather than a specific food craving (Wise, 1997). The results of Michener and Rozin (1994) suggest not only that a pharmacological model of chocolate addiction or craving is inappropriate, but also that the orosensory components of chocolate are essential to satisfying the craving. Those authors also point out that the consumption of calories might be important; however, in their study these factors could not be separated, since the sensory stimuli of chocolate are always followed by absorption of calories, and so those stimuli will also be strong cues for caloric effects. This raises the question of the contribution of repletion of energy deficit to the development of food craving: chocolate is a notably energydense food, as indeed are other popularly craved foods such as pizza, cakes and ice cream (Rodin et al., 1991; Weingarten & Elston, 1991). This issue has been considered previously in relation to restrained eating (Hill et al., 1991; Rodin et al., 1991; Weingarten & Elston, 1991), the argument being that persons attempting to restrict their intake may be more at risk of developing food cravings due to greater hunger and/or avoidance of favourite foods. However, those studies did not find a strong relationship between restrained eating and food craving. This might appear to oppose a role for hunger in eliciting food cravings but questionnaire measures of restrained eating tend to correlate positively with adiposity (Hill et al., 1991; Wardle et al., 1992), suggesting a chronic and unsuccessful struggle to control intake, rather than acute or chronic energy deficit (Booth, 1994). The importance of deprivation state in influencing the reinforcing value of food has been well-documented, even if the details of the learning mechanisms and sites

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of reinforcers involved remain uncertain (Balleine et al., 1995; Booth, 1985, 1987; Sclafani, 1997). Such learning has been demonstrated in numerous studies to be a fundamental part of processes controlling appetite and satiety (Birch et al., 1990; Booth, 1972, 1977, 1985) as well as food choice (Gibson et al., 1995). Thus, the acceptance or rejection of a food can depend on the presence of particular internal states, which, in configuration with the orosensory cues from the food, predict specific postingestive consequences (Booth, 1985; Gibson & Booth, 1989) or at least such internal states become conditioned modulatory stimuli influencing the strength of cue-consequence associations (Davidson, 1993; Davidson & Benoit, 1996). In addition, Weingarten (1983) showed that non-food environmental cues such as a light and tone, when paired repeatedly with meal delivery to hungry rats, can come to initiate meals in rats with free access to food; such contextual cues may act as occasion setters which elicit memories of the action-outcome and cue-consequence learning that occurs when food is eaten while hungry. Furthermore, the motivation to procure a particular food depends on having experienced eating that food in a particular hunger state: that is, the “incentive value” of the food, as expressed by a change in the action to procure it, is enhanced by hunger, or reduced by satiety, only if the eating outcome has already been experienced while hungry, or satiated (Balleine, 1992; Balleine et al., 1995; Dickinson & Balleine, 1994). Despite uncertainty over the mechanisms behind such evidence for the learned control of appetite, it can be inferred that strong appetitive urges could be expressed for particular foods in particular situations and states, given appropriate experience of eating those foods. It is proposed that craving for chocolate is in fact just such an appetite, acquired through repeated experience of eating this energy-dense food when hungry. This agrees with the suggestion that craving for chocolate is a strong desire, or appetite, labelled as craving for attitudinal and cultural reasons (Rogers, 1994, 1995; Wardle, 1987a), and indeed craving is typically defined essentially as a paraphrasing of a strong and specific appetite. Therefore, an experiment was designed to test the hypotheses that chocolate craving would be increased by repeated experience of eating chocolate when hungry and decreased by repeatedly eating chocolate when full: this was expected to be the case in both established chocolate cravers and non-cravers. In addition, we predicted that the change in craving for chocolate would be most clearly expressed when tested in the same appetitive state in which repeated chocolate intake had just been experienced. In addition, support for our predictions would further argue against craving being based on pharmacological reinforcement, because although severe hunger can enhance drug self-administration (Carroll et al., 1979), repeated association of a drug reinforcer with a food satiated state should not specifically reduce responding for such a reinforcer (Carroll, 1982).

M Participants Subjects were recruited from amongst 170 undergraduates at The City University, London, U.K., who had completed a questionnaire on chocolate eating habits and attitudes. Respondents were categorized as either cravers or non-cravers if their

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score on a 13-item “chocolate craver” scale was within the top or bottom tertiles, respectively. This scale consisted of items with a loading exceeding 0·50 on the primary factor produced by factor analysis of 20 5-point items (i.e. responses between “Strongly agree” and “Strongly disagree” to chocolate-related statements) from the original questionnaire (Cronbach’s alpha=0·89, suggesting good internal consistency). The three items with the highest loading on the primary factor were: “When I am hungry, I often think about eating chocolate”, “I regard myself as someone who craves chocolate” (craving defined as “strong desire that you find distracting”); “When passing newsagents, vending machines etc., I cannot resist buying chocolate”. Further details about the questionnaire may be obtained from the authors. Subjects had also earlier completed the anglicized version of the Dutch Eating Behaviour Questionnaire (DEBQ) (Wardle, 1987b), which measures restrained, external and emotional eating tendencies. Eighteen “cravers” and 18 “non-cravers”, as defined above, who had indicated their willingness to take part in further studies of chocolate eating habits, were invited, and agreed, to take part in this experiment. Data are presented for 17 cravers (14 women, 3 men) and 12 non-cravers (9 women, 3 men) who fully complied with the instructions. It is not surprising that most of the non-compliers were non-cravers, since they would clearly be less motivated than the cravers to persevere with chronic chocolate consumption and the demands of the protocol. Subjects were not paid for participation. The study received ethical approval from The City University, and every subject gave signed consent. Design This study was designed to assess the impact of eating chocolate twice a day for 2 weeks, in one of two appetitive states, on appetite for chocolate, as measured by momentary rated craving and anticipated intake. Thus, subjects were asked to eat the chocolate exclusively either at least 2 h after last eating (labelled “hungry”) or 15–30 min after eating a meal (labelled “full”). Two hours post-meal is the minimum time by which sensations of fulness have disappeared and plasma glucose approaches, or falls below, fasting levels, while hunger levels have started to rise (Sepple & Read, 1989): conversely, at 15–30 min post-meal, feelings of fulness are still strong, while nutrient delivery to the duodenum and subsequent absorption underlie strong satiation at this time. To allocate cravers and non-cravers evenly to the hungry and full experimental conditions for chocolate consumption, subjects were sorted into pairs of approximately equal craving scores within the craver and non-craver groups. Then one of each pair was randomly allocated either to the hungry or full condition, and vice versa. The effect of the chocolate eating and appetitive state manipulation on appetite for chocolate was assessed by employing a within-subjects design. Firstly, subjects rated craving and desire for chocolate both before and after the 2-week consumption period. Secondly, at both the pre- and post-consumption stage, subjects made these rated assessments of appetite when hungry on one day and when full on another (these states are referred to as the test states). That is, subjects who were to eat chocolate for a fortnight when full (this state is referred to as the training state) initially rated their chocolate appetite on Day 0 when hungry, then on Day 1 when full. At the end of the fortnight, these subjects rated their appetite when full on Day

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14, and then when hungry on Day 15. Day and state were reversed for those eating chocolate for the 2 weeks when hungry (hungry trained). Although this design is not fully counterbalanced, since test state sequence is confounded with training state, a counterbalanced design was not used for two reasons: first, the number of cravers available for recruitment from the original questionnaire sample was considered too small to provide sufficient subjects for the doubling of groups that would be necessary; second, it was considered quite probable that a group first tested post-training in the untrained state would merely provide evidence for extinction/relearning of the hypothesized effect of training. To summarize, the design consisted of two between-subject factors, i.e. craving status and appetitive training state for consumption, as well as two within-subjects factors, i.e. pre/post-consumption period and appetitive test state (appetite assessed when hungry and full). Procedure Each subject received a “chocolate diary” containing full instructions for completion, as well as rating scales for craving and pleasantness of taste, and questions on the anticipated intake. Questions were organized in “Before Eating” and “After Eating” sections, and composed as follows: 1. If any amount of chocolate was available, how much would you want to eat right now? (Answers were open, but were converted to estimated gram weights for analysis). 2. Look at the chocolate but do not eat any. Now rate how much you crave the chocolate by placing a mark against the point on the line which best applies to you. Craving is defined as a strong desire that you find distracting. (The 100-mm line was anchored by 0=“not at all craved” and 100=“extremely craved”.) In the “After Eating” section, the following question was asked: 3. How pleasant do you find the taste of this chocolate? (100-mm line anchored by 0=“extremely unpleasant” and 100=“extremely pleasant”.) All these questions were repeated for each of 4 days (i.e. 2 days at the start and 2 at the end of the consumption fortnight). At the beginning of each page, instructions emphasized the appropriate appetitive state in which to complete the questions. A further four pages of the diary were dedicated to the first and second weeks, and first and second chocolate eating episodes of the day. Each page contained instructions, a list of six questions, and a day×question table for responses. Four questions asked whether the subject ate or drank anything along with the chocolate, and if so, what. The final two questions asked how long before and after eating the chocolate did the subject last/next eat, thus allowing actual reported time since/to eating to be calculated. Each subject was supplied with 15 100-g bars (525 kcal; 2·2 MJ) of Cadbury’s Dairy Milk chocolate, which were a gift of Cadbury Ltd (Bourneville, U.K.). One bar was to be used for hedonic ratings on Day 0 and 15, the remainder to be consumed over the intervening 2 weeks. Thus, subjects were asked to divide each bar in half at the start of the day, and consume them on two separate occasions on each day, in whichever appetitive state was appropriate to that subject’s grouping. The maximum amount of chocolate to be consumed per day was 100 g; however, because the study included non-cravers who were not normally used to consuming

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a great deal of chocolate, subjects were informed that they need not consume the entire bar on each day, so long as some chocolate was eaten twice a day. Subjects were not required to record the actual amount of chocolate eaten during training. Subjects were asked to avoid eating any other chocolate on any occasion in the 2 weeks, and to avoid making substantial changes to their dietary habits. Since cravers reported typically eating an average of 68 g of chocolate per day (Table 1), they should not have been unduly deprived of chocolate. Data Analysis In principle, the design allows analyses of four-way interactions for each of the dependent variables (craving, anticipated intake, pleasantness of taste), i.e. craving status×training state×test state×pre/post training. However, such interactions are difficult to interpret, while the main effects and several of the lower order interactions are of little relevance to the hypotheses. Therefore, only main effects and interactions involving craving status are reported from the four-way analyses of variance (ANOVA). Then, separate three-way ANOVA were also conducted, i.e. within each training condition, effects of craving status, test state and pre/post training were analysed. Since some significant interactions from the 4-way ANOVA on rated craving included craving status, these effects were investigated further by 3-way ANOVA separately for cravers and non-cravers. However, there was no evidence for any interactions with craving status for anticipated intake or pleasantness of taste, and so for those variables 3-way ANOVA were conducted on effects of training condition, test state and pre/post training on data combined for cravers and noncravers. Consequently, results are presented both for cravers and non-cravers separately (Figs 1–3) and, for anticipated intake and pleasantness, combined for all subjects (Tables 2 and 3). A priori within-subject comparisons between pre- and post-training data were made by paired t-tests. Analyses were also run on arcsine (craving and pleasantness ratings) and natural logarithmic (anticipated intake) transformed data, but no qualitatively different results were found, and so analyses on the original untransformed data are given. All analyses were conducted using SPSS version 6.1 (SPSS U.K. Ltd, Woking).

R Subject Characteristics Participants were predominantly female, in their early twenties and of normal weight for height (Table 1). Cravers were more emotional eaters than non-cravers, but the two groups did not differ significantly on restrained or external eating behaviour. As would be expected, cravers reported (in the pre-study questionnaire on chocolate eating habits) eating more chocolate (bars) per week than non-cravers (Table 1). Procedural Compliance Subjects were included in these analyses only if they reported accurate compliance with the procedure. Nevertheless, considerable variation could be achieved for

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T 1 Subject Characteristics Non-cravers (N=12)

Cravers (N=17)

Female (%) Smokers (%)

75 33

82 41

Age (years) BMI (kg/m2)

22·4 (0·7 21·4 (0·7)

21·2 (0·6) 21·1 (0·7)

Chocolate bars (55 g)/week DEBQ scores Restraint Emotional External

1·5 (0·3)

8·6 (1·0)∗∗∗

2·2 (0·2) 2·4 (0·2) 2·8 (0·3)

2·9 (0·3) 3·3 (0·2)∗∗ 3·4 (0·2)

Data are expressed as mean (SE), unless stated otherwise. DBEQ=Dutch Eating Behaviour Questionnaire. ∗∗∗p<0·001, cravers vs. non-cravers, t(27)=5·55, twotailed. ∗∗p<0·01, t(27)=3·68, two-tailed.

instance in the time since last eating and until next eating meals. The overall mean (SE) minutes averaged from both eating episodes on each day, for hungry- or fulltrained groups, were: minutes since last meal, hungry-trained=233·4 (29·5), fulltrained=31·7 (7·8); minutes until next meal, hungry-trained=181·2 (27·5), fulltrained=421·4 (24·5). As intended, the number of minutes between the meals and the chocolate eating episode (though not the intermeal intervals) differed greatly between subjects eating the chocolate hungry and those eating it full, but the reported times did not differ between cravers and non-cravers, [Time since last meal, training group difference, F(1,25)=35·1, p<0·001; craving status, F<1: Time until next meal, training group difference, F(1,25)=37·7, p<0·001; craving status, F<1]. Craving status and training condition did not interact on either measure (Fs<1). It was considered unreasonable to expect subjects never to eat or drink other items around the time of eating the chocolate, over the entire fortnight. Rather, subjects were asked to report whether such eating or drinking occasions had occurred concurrently with eating the chocolate, and what had been consumed. All subjects reported at least one concurrent drinking episode [median (range) over 2 weeks= 15 (1–28)]. The majority of subjects reported one or more concurrent eating episodes (hungry-trained group=14/16 subjects; full-trained group=6/13 subjects), but the number of episodes did not differ between cravers and non-cravers, either for eating or drinking [both F(1,25)<1, NS]. While the number of concurrent drinking occasions did not vary by appetitive training state, F(1,25)<1, more concurrent eating occasions occurred for hungry-trained subjects than for full-trained subjects [mean (SE) eating occasions over 2 weeks: hungry-trained=4·9 (1·1); full-trained=1·7 (0·8); F(1,25)= 5·14, p<0·05]. However, inclusion of number of eating occasions as a covariate in subsequent analyses did not have any significant effects (data not shown).

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CHOCOLATE CRAVING AND HUNGER STATE

(a) Cravers 100 Craving for chocolate

a 80 c

b

60 40 20 0

Pre Post Test state: Hungry Training state:

Pre Post Full

Hungry

Pre Post Hungry

Pre Post Full

Full

(b) Non-cravers

Craving for chocolate

100 80 d 60 40 20 0

Pre Post Test state: Hungry Training state:

Pre Post Full

Hungry

Pre Post Hungry

Pre Post Full

Full

F 1. The effect of eating chocolate when exclusively hungry or full (training state) and test state (hungry, open symbols; full, closed symbols) on the change in chocolate craving before (Pre) and after (Post) the 2-week training period. Data are expressed as mean±SE. Significant pre/post comparisons: at(9)=2·20, p<0·01, one-tailed; bt(6)=3·98, p<0·01, twotailed; ct(6)=2·91, p<0·02, one-tailed; dt(5)=2·22, p<0·05, one-tailed.

Effect of Training and Test States on Appetitive Responding Rated craving prior to tasting On average, as expected, cravers craved chocolate more than non-cravers [mean rated craving=67·5 vs. 35·8, respectively, 4-way ANOVA, craving status, F(1,25)= 17·81, p<0·001]. Rated craving, averaged over training and test states, decreased after training for cravers but not for non-cravers [Fig. 1: craving×pre/post interaction, F(1,25)=4·71, p<0·05]. The change in craving pre/post training depended on training and test state, as well as craving status [craving×training×test state×pre/post interaction, F(1,25)=4·68, p<0·05]. No other interactions with craving status were found by 4-way ANOVA on rated craving.

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(a) Cravers

Anticipated intake (g)

180 160 140 120 100 80 60

a

40 20

0 Test state: Hungry Training state:

Full

Hungry

Hungry

Full Full

(b) Non-cravers

Anticipated intake (g)

180 160 140 120 100 80 60 40 20 0 Test state: Hungry Training state:

Hungry

Full

Hungry

Full Full

F 2. The effect of hungry or full training conditions and test state (hungry or full) on the change in anticipated intake of chocolate before (hatched) and after (shaded) the 2week training period. Data are expressed as mean+SE. Significant pre/post paired comparisons: at(6)=3·83, p<0·01, two-tailed.

For cravers, despite initially strong craving scores, craving increased still further after 2 weeks, in those subjects who ate the chocolate when hungry (Fig. 1a); this increase was apparent only when craving was rated while hungry, whereas when rated while full, mean craving decreased (Fig. 1a). Indeed, in cravers, change in craving was influenced by test state only in those subjects who had eaten chocolate for 2 weeks when hungry [pre/post change×training×test states interaction, F(1,15)=5·61, p<0·05]. By contrast, in cravers who ate the chocolate for 2 weeks when full, rated cravings were considerably reduced [Fig. 1a: training×test states interaction, F(1,15)=9·28, p<0·01], and this reduction in craving occurred whether subjects had rated their cravings while hungry or full (Fig. 1a). Main effects (3-way ANOVA, cravers only)

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CHOCOLATE CRAVING AND HUNGER STATE

T 2 Anticipated intake of chocolate when hungry and full (test state) before and after eating chocolate for 2 weeks when either hungry or full (training state): data combined for cravers and non-cravers Training Test state state

Anticipated intake (g) Before

After

Difference (After-Before) Mean SE

Differencea p

Mean

SE

Mean

SE

61·2 48·7

12·9 14·1

83·6 47·9

14·2 13·8

22·4 −0·8

10·3 14·5

<0·05 NS

Full Hungry 114·3 (N=13) Full 62·0

23·3 16·8

41·9 38·6

12·6 11·1

−72·4 −23·3

24·3 12·4

<0·025 <0·10

Hungry Hungry (N=16) Full

a Differences by paired t-test: hungry/hungry, t(15)=2·17; hungry/full, t(15)=0·05; full/hungry, t(12)=2·98; full/full, t(12)=1·88.

were significant for pre/post change, F(1,15)=11·80, p<0·01, and test state, F(1,15)= 4·64, p<0·05, but not for training condition, F<1. Not surprisingly, non-cravers prior to training had somewhat low craving scores. However, as for cravers, rated craving increased significantly over the two weeks, but only in those subjects eating the chocolate while hungry (Fig. 1b). In hungrytrained subjects, there was no evidence that cravers and non-cravers differed in any respect other than average craving scores [Fig. 1: 3-way ANOVA, hungry-trained only: craving status, F(1,14)=11·23, p<0·01; craving×pre/post, F(1,14)=3·20, NS; test state×pre/post, F(1,14)=2·25, NS; craving×test state×pre/post, F<1, NS]. In full-trained subjects, again cravers craved chocolate more than non-cravers; 3-way ANOVA: F(1,11)=6·99, p<0·05. Craving, averaged over both test states, decreased significantly after eating chocolate for two weeks when full, F(1,11)= 12·64, p<0·01, and this decrease was similar whether tested hungry or full (test state×pre/post interaction, F<1, NS). Curiously, in these full-trained subjects, the reduction in craving tended to be greatest for cravers but least for non-cravers when subjects were tested hungry, although the significance of this interaction was marginal [craving status×test state×pre/post interaction, F(1,11)=4·67, p=0·05]. Among non-cravers, whether trained hungry or full, test state did not significantly influence the change in craving, F<1, although the increase only reached significance when hungry-trained subjects rated the craving while hungry (Fig. 1b). Conversely, in non-cravers who ate the chocolate when full for 2 weeks, craving tended to decrease [pre/post change×training state interaction, F(1,10)=5·51, p<0·05], although withintest state changes were not significant (Fig. 1b). Overall in non-cravers, test state did not significantly interact with training condition nor pre/post change, F<1. Anticipated intake Overall, mean anticipated intake was greater for cravers than non-cravers [78·8 g vs. 38·3 g, 4-way ANOVA, craving status, F(1,25)=6·78, p<0·02]; otherwise, craving status did not significantly interact with any factor (Fig. 2). As with rated craving, the amount of chocolate that subjects reported wanting to eat depended both on

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(a) Cravers

Pleasantness of taste

100 80

a

b

60 40 20 0

Pre Post Test state: Hungry Training state:

Pre Post Full

Hungry

Pre Post Hungry

Pre Post Full

Full

(b) Non-cravers

Pleasantness of taste

100 80 60 40 c 20 0

Pre Post Test state: Hungry Training state:

Pre Post Full

Hungry

Pre Post Hungry

Pre Post Full

Full

F 3 The effect of eating chocolate when exclusively hungry or full (training state) and test state (hungry, open symbols; full, closed symbols) on the pleasantness of the taste of chocolate before (Pre) and after (Post) the 2-week training period. Data are expressed as mean±SE. Significant pre/post paired comparisons: at(6)=2·45, p=0·05, two-tailed; bt(6)= 2·26, p<0·05, one-tailed; ct(5)=2·70, p<0·025, one-tailed.

whether they ate the chocolate for 2 weeks while hungry or full and on their appetitive state when responding: the change in anticipated intake over the two weeks interacted with both those conditions [Fig. 2: 4-way ANOVA, training state×test state×pre/ post rating, F(1,25)=7·55, p<0·02]. Also, subjects desired to eat more chocolate on average when tested hungry than full [4-way ANOVA, test state effect, F(1,25)= 12·27, p<0·01]—an effect that was not significant for rated craving. Subjects who ate chocolate for 2 weeks when hungry reported wanting to eat more chocolate after the 2 weeks than before, but only when they were tested hungry

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T 3 Pleasantness of the taste of chocolate rated when hungry and full (test state) before and after eating chocolate for 2 weeks when either hungry or full (training state): data combined for cravers and non-cravers Training state

Test state

Pleasantness of taste (0=Extremely unpleasant; 100=Extremely pleasant) Before

After

Mean

SE

Mean

SE

Difference (After-Before) Mean SE

Differencea p

Hungry (N=16)

Hungry Full

76·9 76·1

4·5 5·1

76·2 68·9

6·6 7·2

−0·7 −7·1

4·9 7·7

NS NS

Full (N=13)

Hungry Full

80·7 68·3

4·7 5·6

58·0 50·7

6·6 6·7

−22·7 −17·6

7·4 5·2

<0·01 <0·005

Differences by paired t-test: hungry/hungry, t(15)=0·14; hungry/full, t(15)=0·93; full/hungry, t(12)=3·06; full/full, t(2)=3·39.

(Table 2). Conversely, subjects who ate chocolate for 2 weeks when full reported wanting to eat less chocolate at the end of the 2 weeks, whether they were tested hungry or full [Table 2: training state×test state, F<1, NS; training state×pre/post, F(1,27)=10·71, p<0·01; training state×test state×pre/post, F(1,27)=7·45, p<0·02]. However, when the results were analysed separately for hungry- and full-trained subjects and including craving status as a factor, the change in anticipated intake was only significantly affected by test state in full-trained subjects [Fig. 2: 3-way ANOVA, full-trained subjects: test state, F(1,11)=20·44, p<0·002; pre/post change, F(1,11)=8·90, p<0·02; test state×pre/post, F(1,11)=8·12, p<0·02]. In these fulltrained subjects, specifically hungry-tested cravers showed a particularly large reduction in anticipated intake after training, which was likely due to a high anticipated intake prior to training [Fig. 2: craving status×test state×pre/post, F(1,11)=7·83, p<0·02]. Rated pleasantness of taste Overall, pleasantness of taste was rated greater by cravers than non-cravers [mean=76·0 vs. 61·5, 4-way ANOVA, craving status effect, F(1,25)=4·91, p<0·05]. On average, pleasantness of taste was rated less when tested full than hungry [Fig. 3: 4-way ANOVA, test state, F(1,25)=6·33, p<0·02], and was rated less after the 2 weeks, with the greatest decrease tending to occur in full-trained subjects [Fig. 3: 4-way ANOVA, pre/post effect, F(1,25)=6·94, p<0·02; pre/post×training state, F(1,25)=3·62, p<0·07]. Indeed, no significant changes in pleasantness of taste occurred post-training for hungry-trained subjects, whether tested hungry or full [Table 3: 3-way ANOVA, combined data, training state×pre/post interaction, F(1,27)=3·75, p=0·06]. This result did not depend on craving status (Fig. 3: hungry-trained subjects, all Fs<1·30). Subjects who ate chocolate for 2 weeks when full rated the taste of chocolate as significantly less pleasant after the 2 week training period, whether tested hungry or full [Fig. 3: 3-way ANOVA, pre/post effect, F(1,11)=11·25, p<0·01; test state×pre/ post interaction, F<1, NS]. On average, taste was rated less pleasant when tested

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full than when tested hungry [test state, F(1,11)=6·52, p<0·05], while cravers and non-cravers were equally affected [Fig. 3: craving status×test state, F(1,11)=2·62, NS; all other interactions, FΖ1, NS].

D Craving as an Expression of a Learned Appetite In general, the results support the interpretation of chocolate craving as a strong appetite for chocolate, since both the acquisition and the expression of chocolate craving can depend on concurrent appetitive state. Thus, the experience of eating chocolate for 2 weeks exclusively when hungry led to increased craving in both cravers and non-cravers. This increase in craving in hungry-trained eaters was expressed only when concurrently hungry, at least for cravers. Conversely, craving for chocolate was reduced by the experience of eating chocolate exclusively when full for 2 weeks. This effect was weaker in non-cravers, possibly because of a floor effect preventing sufficient reduction in craving. Unlike the influence of hunger, craving was reduced by this chronic association with fulness whether subjects were full or hungry when actually rating their craving, although again this effect was less clear in non-cravers. Weaker effects in non-cravers could be due to smaller intakes of chocolate at eating episodes over the 2-week training period by those subjects; this was not assessed. Even so, there was little statistical support for differential effects between cravers and non-cravers, other than for the average degree of craving. The argument that chocolate craving is an expression of appetite for chocolate dependent on appetitive state is strengthened by the evidence that changes in the amount of chocolate which subjects wished to eat showed a similar pattern to changes in craving. Thus, subjects who ate chocolate only when hungry wished to eat more chocolate following that experience, but only when hungry at the time: when full, these subjects showed no change in their anticipated intake. Again as with craving, anticipated intake was substantially reduced by the experience of eating chocolate exclusively when full, but this reduction in appetite for chocolate did not depend on the appetitive test state contingent with expressing the appetite, i.e. the desired amount declined at least as much when tested hungry as when tested full. These effects on anticipated intake were statistically independent of whether the subjects were cravers or non-cravers.

Incentive Learning and Motivational State Dependency One interpretation of the enhanced appetite for chocolate, as expressed by craving and anticipated intake, that results from pairing its consumption with hunger, is that the postingestive consequences such as energy absorption are more reinforcing in the depleted state. Thus, there is greater reinforcement of the action of eating chocolate, and then the value of just the thought of eating chocolate, i.e. the cognitive representation of that action and its outcome, is increased. Conversely, in this group of hungry-trained subjects, there is no new learning opportunity about the impact of a replete state on chocolate consumption, and so in that state their appetitive responses for chocolate remain unchanged.

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A similar interpretation, with valence reversed, could be placed on the reduction in appetite for chocolate seen in full-trained subjects when rating craving and anticipated intake in the full state, i.e. that the reinforcing effect of chocolate consumption is weakened by exclusive experience when already full. However, pari passu with the argument above for the hungry-trained group, in this full-trained group, no new learning would be expected concerning the value of chocolate consumed when hungry, and so no change in appetite for chocolate when hungry would be predicted for this group. By contrast, we found, especially in cravers, that appetite for chocolate was just as reduced in this group when tested hungry as when tested full: the devaluing of the outcome, or at least its representation, of eating chocolate appears to have transferred across drive states. A possible explanation for this transfer of appetite may be found in recent work on incentive learning using instrumental action-outcome paradigms. A number of experiments demonstrated that the incentive value of an outcome, for instance as measured by rate of lever pressing by rats (action) to procure food pellets (outcome), will remain unchanged from the trained state (say undeprived) to a new test state (say deprived) so long as the rats did not have the opportunity of learning a new value of the outcome by pre-test experience of the outcome in the new state (Balleine, 1992; Dickinson & Balleine, 1994). In other words, the motivational state in which an outcome is experienced can acquire control over its incentive value only if the outcome is previously experienced in different states. Here, craving and anticipated intake are taken to be measures of the incentive value assigned to a representation of the outcome (eating chocolate). In incentive learning terms, the appetitive motivational state in which the chocolate was experienced has determined the acquisition of incentive value: that is, hunger during training has increased the value while fulness decreased the value of eating chocolate. However, as well as determining the incentive value (and so the level of craving), in hungry-trained subjects hunger appears to exert control over the incentive so that it is assigned a greater value during concurrent hunger than when full. By contrast, fulness training did not result in any evidence of control, so that the incentive value remains equally low when assessed in the full and in the hungry state. The acquisition of control over incentive value by a motivational state is thought to depend upon the state giving rise to discriminable stimuli (Booth, 1985; Davidson, 1993; Dickinson & Balleine, 1994). Therefore, one interpretation of these results is that hunger gives rise to more salient stimuli than fulness (as defined here), so that only the former state allows discriminative control over chocolate’s incentive value. However, this difference in incentive control by hunger and fulness might also reflect an imbalance in subjects’ previous (pre-experimental) experience of eating chocolate when hungry or full. It seems likely (not least because of our results) that chocolate has been eaten far more often when hungry than well full, especially by cravers, and there are indeed experimental data which may suggest how this difference in experience could result in differential control by hunger and fulness. Thus, Dickinson et al. (1995) found that with more extensive repeated experience of procuring food in one state, and little or no experience of this action-outcome relation in another, the motivational value of the food became more susceptible to the current rather than trained deprivation state. Thus, it appeared that the influence of knowledge of the action-outcome relation had declined with training. This was interpreted as evidence for a dual-process theory of overtraining: that is, as training is repeated, the total strength of the instrumental behaviour is more and more

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influenced by a stimulus-response/reinforcer process and less and less by an actionoutcome process, the former process being more dependent on current motivational state (Dickinson et al., 1995). In our study, craving and anticipated intake may be regarded as proxy measures of intention to behave, i.e. predictors of the strength of the instrumental behaviour of procuring chocolate to eat. Our chocolate eaters could be regarded as “overtrained” in the hungry state, in which case, following the argument of Dickinson et al. (1995), these subjects would be susceptible to the current test state. Thus, we find that hungry-trained subjects, especially cravers (perhaps the most “overtrained”), show increased craving for, and anticipated intake of, chocolate when tested hungry but not full. Conversely, having to eat chocolate for 2 weeks only when full is probably a novel experience, and so subjects may depend more on action-outcome learning, such that the incentive value of chocolate is reduced both in the full and hungry state. Of course, it would be useful to determine in these full-trained subjects whether their independence from concurrent appetitive state persisted over subsequent experience of eating chocolate when hungry. The above findings suggest that appetite for chocolate would quite quickly become susceptible to current need state. Two other studies have looked at relationships between deprivation state and appetite for commonly craved foods, including chocolate confectionery (Lambert et al., 1991) and pizza and ice cream (Cornell et al., 1989). Cornell et al. (1989) found that subjects fed to satiety would subsequently eat more pizza or ice cream if first “primed” with a taste of the food. Lambert et al. (1991) found that both the sight and taste of chocolate M&Ms (Mars) increased the desire to eat the chocolate more than mere thoughts or no stimulation, to the same extent whether hungry or full (although actual intake was unaffected by stimulus condition). In contrast to our study, it is probable that the acute nature of these studies did not allow subjects to associate the consequences of eating these foods with, in particular, the satiated state, so that no satiety-dependent reduction in incentive value was learned. Pleasantness of Taste and Appetitive State The impact of internal need states on taste reactions would normally be expected to be under Pavlovian (i.e. stimulus or stimulus-reinforcer) associative control, or even unlearned (Grill & Norgren, 1978), rather than instrumental control (Booth, 1987; Holman, 1969; Weingarten & Kulikovsky, 1989); that is, hedonic taste reactions should be sensitive to current motivational state. Indeed, in rats, calorically conditioned flavour preferences are increased by deprivation, whether conditioning was established when deprived or fed ad libitum (Fedorchak & Bolles, 1987). Moreover, even if the consummatory behaviour involved in preference measures is considered a proximal instrumental act (i.e. the last in a chain of behaviours leading to ingestion), Balleine et al. (1995) showed that such proximal actions are susceptible to change by contingent deprivation state without incentive learning. Nevertheless, experience of eating the chocolate exclusively when hungry for 2 weeks made no difference to the pleasantness of chocolate’s taste, whether it was tasted when hungry or full. It is possible that this measure was insensitive to potential increases in pleasantness due to a ceiling effect, although the mean initial pleasantness ratings were similar to those for craving (for cravers), which still increased in hungry subjects. Moreover, non-cravers rated pleasantness as lower than cravers, and so were not likely to be constrained by such a ceiling.

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In contrast to the lack of hunger training, eating chocolate only when full considerably reduced the pleasantness of the taste of chocolate whether subjects were actually hungry or full when tasting the chocolate, i.e. a similar finding to the results for craving and anticipated intake. This is not, then, a simple reduction in attractiveness or pleasantness of chocolate stimuli as can occur to sensory stimuli following repletion (Cabanac, 1971), but a more complex acquired response. It is clear that learning has occurred over the fortnight’s eating experience because eating chocolate exclusively while full reduced its attractiveness even below the level at which it was rated when full at the start of the study. Although in these subjects the changes in pleasantness are similar to those for craving and anticipated intake, it seems unlikely that this merely reflects consistency in rating across variables due to cognitive dissonance or expectational effects: if that were the case, the changes in pleasantness ratings in hungry-trained subjects should also have mirrored their other appetitive ratings, which they did not. It is worth noting that strong flavour preferences conditioned in rats by extensive pairing with nutrient infusions show long-lasting resistance to extinction (Elizalde & Sclafani, 1990): perhaps the flavour of chocolate has been so strongly reinforced in our hungry-trained subjects, by this and past experience, that it resists not only further increase but also devaluing, or generalization decrement, by the presence of satiety. It is also possible that the sensory properties of chocolate have unconditioned reinforcing components that resist dependency. If the monotony of repeatedly eating the same brand of chocolate is to blame for the resistance to increased pleasantness, it must have affected pleasantness in a state-independent fashion. Conceivably, those subjects who were required to eat chocolate only when full eventually found this protocol so aversive that the taste of chocolate acquired negative associations which resisted changes in internal drive states. In any event, these effects on pleasantness of taste of pairing chocolate with hunger or satiety appear independent of current need state, and do not seem to be explicable either by configural conditioning of dietary and interoceptive state cues (Booth, 1985; Gibson & Booth, 1989) or by conditioned modulation of associative strength between conditioned and unconditioned stimuli by deprivation states (Davidson, 1993). Chocolate vs. other Food Cravings It is our contention that repeated consumption of (in particular) an energy-dense food when hungry will lead to a strong hunger-dependent appetite for that food which may be interpreted as a craving by some individuals. The fact that craving and anticipated intake were increased by such hunger-paired exposure to chocolate in both cravers and non-cravers strongly supports this contention. Our belief that chocolate craving is based on normal mechanisms of appetite that can apply to many foods is supported by the evidence that food cravings are in fact commonplace. Thus, Weingarten and Elston (1991) found in their samples of 1138 Canadian undergraduates that 97% of women and 68% of men reported having experienced food cravings. Furthermore, Hill et al. (1991) surveyed food cravings in 206 women, and found that 69% agreed that craving a food was the same as having a strong urge to eat a food: among the remaining 31%, most disagreement was represented as cravings being stronger, more specific, persistent and harder to resist. However, such findings raise two issues which should be addressed before our interpretation

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is readily accepted: why is chocolate far more commonly craved than any other single food, and why are food cravings more common in women than men? Chocolate has a number of qualities that may explain its dominance amongst craved foods. First, chocolate has orosensory textural and flavour properties that are quite unique: these may in large part be due to the special melt-in-the-mouth properties of cocoa butter, as well as the complex flavour components of processed cocoa beans (Hoskin, 1994; Morgan, 1994). Similar temporal and thermal changes in texture are thought to produce the “dynamic contrast” which appears to be essential to the pleasurable sensory experience of other foods considered highly palatable (Hyde & Witherly, 1993). Moreover, the special properties of cocoa butter together with the inherent bitterness of chocolate liquor may allow for a very high sugar:fat ratio in sweet chocolate, which is well above the hedonically ideal ratio for simpler sugar:cream mixtures (Drewnowski & Greenwood, 1983; Max, 1989) and may enhance its reinforcing potential. Such sensory uniqueness may resist generalization, so encouraging specificity of craving, as well as conveying salience, and so allowing representation of the sensory characteristics to be easily recalled. In addition, chocolate and chocolate-flavoured foods are mainly marketed and consumed as snack foods, i.e. they are most likely to be eaten between meals as signs of hunger return (Seligson et al., 1994). Also, chocolate flavour is almost invariably associated with energy-dense foods, which will therefore be strongly reinforcing when eaten hungry. It is notable that the majority of non-chocolate foods that are reputedly craved are also energy-dense snack items, and very often sweet (Hill & HeatonBrown, 1994; Weingarten & Elston, 1991). Sex Differences in Food Cravings The sex difference in prevalence of food cravings appears largely to reflect sex differences in attitudinal and emotional aspects of eating behaviour. For instance, men that report food cravings typically interpret these cravings as initiated by hunger, whereas women are more likely to attribute them to negative mood, stress and boredom (Weingarten & Elston, 1991). Interestingly, and perhaps equivalently, in opiate abusers, negative mood states appear to become conditioned cues for craving (Childress et al., 1994). Negative affect that follows indulgence in the craved food (Macdiarmid & Hetherington, 1995) also appears to be more frequent in women than men (Weingarten & Elston, 1991). Women more often report feelings of loss of control and conflict over their appetite for highly preferred but nutritionally less relevant foods such as chocolate, whether or not they are explicitly trying to lose weight (Macdiarmid & Hetherington, 1995; Rodin et al., 1991). Our finding that cravers were more emotional eaters but not significantly more concerned with dieting (restrained) than non-cravers agrees with previous literature (Hill & Heaton-Brown, 1994; Hill et al., 1991; Macdiarmid & Hetherington, 1995; Rodin et al., 1991), and suggests that such attitudes to eating “forbidden” foods like chocolate probably contribute to women labelling themselves cravers or “addicts”, and labelling urges to eat specific foods as craving. This addiction model allows the loss of control to be attributed to effects of the craved food (Rogers, 1994). The sex difference cannot be attributed to a greater appetite for sweet foods in women, since a number of studies report greater liking for sweet taste in men than women (Conner & Booth, 1988; Enns et al., 1979; Frye et al., 1994; Laeng et al., 1993). Changes in taste preferences and appetite due to hormonal fluctuations associated with the menstrual

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cycle have also been invoked to explain chocolate craving in women (Rozin et al., 1991). However, although there is good evidence that appetite and food intake varies with menstrual cycle (Buffenstein et al., 1995; Rogers et al., 1992), prospective studies of food choice in women have not supported a relationship between menstrual phase and preference for chocolate (Hill & Heaton-Brown, 1994; Rogers & Jas, 1994). Even so, it seems plausible that menstrual phase-dependent enhanced cravings or appetite for certain foods could be learned. That is, a habit of eating those foods could be acquired and controlled by a particular hormonal state if increased appetitive drive and sufficiently salient internal stimuli were present. Summary In conclusion, craving for chocolate can be increased, or even established, by repeated experience of eating chocolate when hungry: conversely, when chocolate is eaten repeatedly only when satiated, craving is substantially reduced. A similar pattern is seen for anticipated intake of chocolate, and it is argued that the findings support interpretation of cravings for chocolate, or other foods, as an expression of a strong appetite elicited by hunger that has been acquired by repeated experience of eating the craved food when hungry. The results appear to be compatible with recent findings on incentive learning explanations of appetite behaviour. We would define food craving mechanistically as a strong urge to obtain a specific food, or its representation, which is elicited by internal and external cues whose confluence bestows the memory of the food with an irresistible salience. Although we argue against explanations of the acquisition of food craving in terms of pharmacological models of reinforcement, it is nonetheless likely that food and drug cravings share neurochemical and psychological mechanisms (Wise, 1997). Indeed, the evidence that drug craving and taking depends on the acquisition of incentive salience by drug-associated stimuli (Robinson & Berridge, 1993; Stewart et al., 1984) suggests that drug and food cravings may arise from similar learning processes. Furthermore, the apparent dissociation between motivational control of subjective pleasure (e.g. pleasantness of taste) and craving seen here in hungry-trained subjects is predicted by the Incentive-Sensitisation theory of drug addiction (Robinson & Berridge, 1993). That theory explicity distinguishes between “wanting” (e.g. craving) and “liking” (e.g. sensory pleasure), and suggests that addictive drugs selectively sensitize pathways mediating incentive salience of stimuli controlling drug “wanting”, but not “liking” of drug-associated sensory stimuli. Finally, our findings have implications for food choice and dietary health: we would predict that uncontrolled appetites for highly desired but often unhealthy (e.g. high fat) foods may be ameliorated by changing eating habits so that such foods are eaten shortly after the ends of meals, but avoided when hungry. Such restructuring of eating habits may contribute to interventions that attempt to substitute less healthy confectionery with healthier snacks such as fruits and vegetables. R Balleine, B. (1992). Instrumental performance following a shift in primary motivation depends on incentive learning. Journal of Experimental Psychology: Animal Behavior Processes, 18, 236–250.

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