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Psychoactive effects of tasting chocolate and desire for more chocolate
Physiology & Behavior 104 (2011) 117–121
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Physiology & Behavior j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p h b
Psychoactive effects of tasting chocolate and desire for more chocolate Jennifer A. Nasser a,⁎, Lauren E. Bradley a, Jessica B. Leitzsch a, Omar Chohan a, Kristy Fasulo a, Josie Haller a, Kristin Jaeger a, Benjamin Szulanczyk a, Angelo Del Parigi b a b
Department of Nutrition Sciences, Drexel University, Philadelphia, PA 19102, United States Department of Psychology, Drexel University, Philadelphia, PA 19102, United States
a r t i c l e
i n f o
Article history: Received 29 January 2011 Received in revised form 23 April 2011 Accepted 26 April 2011 Keywords: Addiction Research Center Inventory ARCI Food addiction Craving
a b s t r a c t The purpose of this study was to characterize the psychoactive effects of tasting chocolate and to evaluate the contribution of the main chocolate components to the desire to consume more of it. A total of 280 participants, (F-155; M = 125) ranging in age from 18–65, completed the study. Participants were randomly assigned to taste 12.5 g of either white chocolate (“control”) or one of four chocolate (“cocoa”) samples varying in sugar, fat and percent cocoa content, then answered the question: “Do you want more of this chocolate?” and “If yes, how many more pieces of this chocolate would you like to eat?” They completed pre- and post-consumption surveys, consisting of 30 questions derived from the Addiction Research Center Inventory (ARCI) subscales, Morphine–Benzedrine Group (MBG), Morphine (M) and Excitement (E). Significant decreases in post–pre consumption changes in MBG subscale were observed between the control sample and the 70% cocoa (p = 0.046) or the 85% cocoa sample (p = 0.0194). Proportionally more men than women wanted more of the tasted chocolate (p = 0.035). Participants were more likely to want more of the tasted chocolate if they displayed a greater change in the MBG scale, and if their chocolate sample had high sugar and cocoa content, as assessed by multiple logistic regression. Our results suggest that multiple characteristics of chocolate, including sugar, cocoa and the drug–like effects experienced, play a role in the desire to consume chocolate. © 2011 Elsevier Inc. All rights reserved.
1. Introduction Americans consume roughly 22 teaspoons (110 g) of added sugar per day [1]. Chocolate, a high sugar food, is considered to be the most craved substance in the U.S. [2,3]. Prior research suggests, however, that multiple components of chocolate, rather than just sugar, can potentially contribute to the desire to consume chocolate [4,5]. Theobromine and caffeine, (both methylxanthines contained in cocoa) are usually cited as the most salient contributors to chocolate craving [5]. However, Smit et al. [5] as well as Michener and Rozin [2] reported no role for the pharmacological content of methylxanthines in the oro-sensory relief of cravings for chocolate, most likely due to the lengthy post-ingestive time period (60–120 min) required for caffeine and theobromine blood levels to rise. Michener and Rozin [2] also reported that partial relief from craving for chocolate is observed even with the consumption of white chocolate (which does not contain cocoa, caffeine, and theobromine), and that an association exists between chocolate cravings and sensory properties of chocolate such as aroma, texture, and sweetness [2]. This suggests a prominent role for the sugar (sweetness) as well as for the fat (texture and
⁎ Corresponding author at: Drexel University, 245 N 15th Street, Mailstop #1030, Philadelphia, PA 19102, United States. Tel.: + 1 215 762 7363; fax: + 1 215 762 4080. E-mail address: [email protected] (J.A. Nasser). 0031-9384/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2011.04.040
aroma) components of chocolate in promoting desire for and consumption of chocolate. Animal studies on the consumption of food sources of fat and sugar other than chocolate, either as single components or in combination, demonstrate activation of multiple neurotransmitter systems [6–8], specifically dopaminergic and opioidergic circuits. Sustained increases in nucleus accumbens dopamine subsequent to consumption or sham feeding of sugar solutions [6] or corn oil solutions [7] can contribute to food wanting [9]. Neurobiological changes attributed to intake of sugar and fat combinations include increased release of dopamine in the cingulate cortex, hippocampus, nucleus accumbens, and locus ceruleus, in addition to increased gene expression of the endogenous opioid dynorphin in the arcuate nucleus of the hypothalamus [10] which can contribute to food liking [11]. The simultaneous activation of dopaminergic and opioidergic systems observed with ingestion and/or sham feeding of high fat and high sugar foods is similar to the pharmacodynamic effects exerted by combinations of a dopaminergic agonist (i.e. amphetamine, cocaine) and an opioidergic agonist, (i.e. morphine, heroin). These dopaminergic–opioidergic combinations are commonly referred to as “speedballs.” “Speedballs” are more reinforcing than either dopaminergic or opioidergic agonists used singularly, and produce a unique set of subjective effects [12] that can be measured using the Addiction Research Center Inventory (ARCI) subscales [13,14]. As a mixture of fat and sugar, chocolate might activate both the dopaminergic and
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opioidergic systems simultaneously, although, Naleid et al. [8] reported that when rats were given access to a vanilla flavored shake varying in fat and sugar, the sugar content was the most reinforcing component. In this human study, we characterized the psychoactive effects of tasting chocolate and investigated the contribution of the chocolate components to the desire to consume more of the specific chocolate tested. 2. Methods and materials 2.1. Methods 2.1.1. Participants This study was approved by the Institutional Review Board of Drexel University and met the requirements for exempt review; consequently, no written consent was required before participants took part in the experimental session. A “sample of convenience,” composed of 290 passersby at the Drexel University Student Center, volunteered to fill out a survey before and after tasting a single 12.5 g sample of chocolate varying in sugar, fat and percent cocoa content (Table 1). White chocolate was used as a “control” sample for chocolate, because it is similar in mouth feel and sweetness but does not contain cocoa, and a sorbitol-sweetened chocolate sample, similar in flavor and mouth feel to the other chocolate containing samples, was used to control for the contribution of sugar to the psychoactive effects of chocolate. We did not have access to a commercially available “fat-free” chocolate sample that had similar flavor and mouth feel properties as the other chocolate samples; therefore, no control for fat content effects was included in our study design. Volunteers were randomly assigned to taste 12.5 g of either white chocolate (i.e. control group) or one of four chocolate samples (i.e. cocoa groups) varying in sugar, fat and cocoa contents. Ten out of 290 participants failed to complete the study properly (either ate the chocolate before filling out the pre-consumption questionnaire or did not complete the post-consumption questionnaire); therefore, their data were not used in the analysis. 2.1.2. Data analysis Data were analyzed using SAS, ver. 8.2 (The SAS Institute, Cary, NC). General linear models were implemented to compare general characteristics (i.e. age, BMI, hunger, mood, chocolate liking and chocolate craving ratings) and ARCI subscale scores of each group (defined by the cocoa percentage of the chocolate sample tasted), and gender. ARCI subscale scores (pre- and post-chocolate consumption) were compared by paired t-Test. Segregation of desire to consume more chocolate by gender was assessed by chi-square test. Multiple logistic regression was employed to determine the individual variables contributing to the desire to consume more of the chocolate that was tasted. The threshold of significance was set at alpha = 0.05.
was calculated from the self-reported height and weight. Chocolate craving and liking were assessed with a Likert Scale as follows: “On a scale from 1 to 10 how much would you say that you crave chocolate?” and “On a scale from 1 to 10 how much would you say that you like chocolate?” Current hunger status was assessed using an anchored visual analog scale (VAS) with labeled intervals from 0 to 100 displayed as follows: 0 = Not hungry at all; 20 = Slightly hungry; 40 = Moderately hungry; 60 = Quite hungry; 80 = Very hungry; and 100 = Extremely hungry. Current mood and alertness were assessed by anchored VAS with labeled intervals including 0 = Extremely sad and Extremely drowsy; 50 = Neutral; and 100 = Extremely happy and Extremely alert. 2.2.2. Addiction Research Center Inventory (ARCI) A pre- and post-chocolate consumption questionnaire, composed of the exact same questions, was used to ask the volunteers a series of questions drawn from the following subscales of the ARCI: Morphine– Benzedrine Group (MBG), Morphine (M) and Excitement (E). These subscales are a series of drug effect questions that describe subjective feelings of individuals after having taken particular drugs. According to Haertzen and Hickey, [14] the MBG subscale measures well-being, euphoria, and optimal functioning, while the M subscale refers to physical sensations of itching and tingling, and the E subscale relates to physical signs of excitement, such as a fast heartbeat and lightheadedness, as well as psychological feelings of well-being and thrill. Selective use of various ARCI subscales has been reported in drug studies [15,16]. Our questionnaire adapted the ARCI subscales (MBG, M, and E) by removing items that were redundant between scales (i.e., from the MBG subscale: “I would be happy all the time if I felt as I do now”) or were not applicable to the study requirement of completing the questionnaires immediately before and after tasting a small chocolate sample (i.e., from the MBG subscale: “Today I say things in the easiest possible way,” and “I feel high,” or from the M subscale: “My speech is not as loud as usual”). Described symptoms that could be related to other conditions rather than to tasting the chocolate (i.e., from the M subscale: “I have been scratching myself,” and “I have been dozing occasionally for seconds or minutes”) were also removed. Additionally, the question “My nose itches” was changed to “My nose itches and/or is running” as this is a possible reaction to food. Pre- and post-consumption portions of the survey asked a total of 30 ARCI questions. Answers to each ARCI question were true/false. Each subscale awarded one point to certain questions if they were answered with the correct expected response (true or false); the total score was then tallied to give the subscale score per Haertzen and Hickey [14]. Two additional questions were included on the post-consumption questionnaire: “Would you want to eat more of this chocolate?” and “If yes, how many more pieces of this chocolate would you like to eat?” These two additional questions were analyzed separately and were not included as part of any subscale score.
2.2. Materials 3. Results 2.2.1. Background information questionnaire Participants were given a background information questionnaire to complete. Height and weight were self-reported and BMI (kg/m2) Table 1 Characteristics of chocolate samples. Chocolate type
% Cocoa
Sugar (g)
Fat (g)
Lindt® white Lindt® milk Russell Stover® Lindt® dark Lindt® dark
0 38 60 70 85
7.0 7.0 7.0a 3.5 1.6
4.5 3.9 3.7 5.5 5.9
Content is per 12.5 g piece of chocolate. a As sorbitol.
3.1. Demographics Participant demographics are displayed in Table 2. There were no significant differences between groups (defined by cocoa content of chocolate sample tasted) with respect to number of subjects, gender, age, BMI, hunger, mood, chocolate liking, or chocolate craving. The average value (Mean±SD), for demographic variables across all participants were: Age (yrs) 25±11, BMI (kg/m2) 24±4, Hunger 33±26, Mood 63± 18, Liking 8.5±2, Craving 6.1±2. Male (M) differed from female (F) participants in chocolate craving (M: 5.5±2.4; F: 6.6±2.4; t=3.74, p=0.0002) and liking (M: 8.2±1.7; F: 8.7±1.8; t=2.45, p=0.015), as well as in BMI (M: 24.5±3.9; F: 22.9±3.7: t=3.48 p=0.0006), but not in hunger (M: 35±27; F: 31±25; p=0.15).
J.A. Nasser et al. / Physiology & Behavior 104 (2011) 117–121 Table 2 Demographics of participants grouped by% cocoa of sample tasted. Mean ± SD.
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Table 4 Logistic regression of contributors to “desire to consume more of the tasted chocolate”.a
Variable
0% Cocoa
38% Cocoa
60% Cocoa
70% Cocoa
85% Cocoa
Variable
O.R.
CI (95%)
Wald Chi-sq
P
N Women Men Age BMI Hunger Mood Liking Craving
57 33 24 24.9 ± 9.5 23.3 ± 4.3 31 ± 28 65 ± 20 8.2 ± 1.8 5.9 ± 2.7
57 31 26 23.8 ± 8.7 24.4 ± 3.2 31 ± 27 64 ± 17 8.4 ± 1.8 6.0 ± 2.2
55 26 29 28.2 ± 12.4 23.8 ± 3.5 33 ± 25 59 ± 18 8.7 ± 1.2 6.4 ± 2.5
57 31 26 24.8 ± 11.3 23.2 ± 3.6 39 ± 27 62 ± 16 8.3 ± 2.0 5.9 ± 2.3
54 34 20 26.4 ± 11.3 23.6 ± 4.8 29 ± 22 66 ± 18 8.6 ± 1.8 6.3 ± 2.5
Sugar grams Change in MBG Cocoa (percent) Fat grams BMI
3.789 1.413 1.037 7.681 0.973
1.394–10.298 1.210–1.650 1.002–1.073 0.875–67.460 0.885–1.069
6.818 19.126 4.314 3.382 0.334
0.009 b0.0001 0.038 0.066 0.6
3.2. Effect of sugar, fat and cocoa on ARCI subscale scores Cocoa groups differed from the control group in sugar, fat and cocoa contents of the sample. Significant within group increases were seen between pre- and post-chocolate ingestions in the MBG subscale for control and cocoa samples through 70% cocoa (Table 3). Between group (cocoa groups versus control) differences in MBG score changes were significant for the 70 and 85% cocoa groups (p = 0.041 and p = 0.019, respectively). These two groups had lower concentrations of sugar: (3.5 g for the 70% and 1.625 g for the 85%) compared to the control (7 g). In multiple regression models, including age, BMI, craving, liking, hunger, mood, grams of sugar, grams of fat, and percent of cocoa, changes in MBG score were associated with liking (p = 0.034), while changes in the E score were associated with age (p = 0.004), liking (p = 0.029), percent of cocoa (p = 0.015), and grams of sugar (0.042). Changes in the M score were not significantly associated with any variable, but the association with craving approached significance (p = 0.057). 3.3. Desire for more chocolate A significantly greater number of men reported a desire for “more of the chocolate tasted” compared to women (chi-square p = 0.0349). Among those reporting a desire for additional chocolate, the difference in amount of additional pieces of chocolate desired between men and women approached significance (M: 4.0 ± 3.5; F: 3.0 ± 2.5; F = 3.5, p = 0.064). Logistic regression analysis revealed that the desire to consume more of the chocolate sample (which had been tasted) was associated with a greater amount of sugar and cocoa in the sample, and with greater post = consumption increases in the MBG subscale (Table 4). 4. Discussion 4.1. Summary of findings Our data indicate that tasting chocolate has measurable psychoactive effects in humans, which in turn are associated with the desire to consume more of it. This desire is proportional to the chocolate's sugar and cocoa contents. This is the first demonstration in humans of such effects using a validated “drug effects” questionnaire. The association of changes in MBG subscale with desire to consume Table 3 Comparison of MBG changes: cocoa versus white chocolate control. Mean ± SD. Variable
0% Cocoa Control
38% Cocoa
60% Cocoa
70% Cocoa
85% Cocoa
N Pretaste MBG Posttaste MBG Change in MBG
57 5.0 ± 3.6a 7.0 ± 3.9a 2.0 ± 2.1ef
57 4.6 ± 3.5b 6.4 ± 3.9b 1.8 ± 2.9
55 5.1 ± 3.4c 6.8 ± 3.9c 1.7 ± 2.6
57 5.2 ± 3.6d 6.1 ± 3.7d 0.9 ± 2.6e
54 5.3 ± 3.5 5.8 ± 4.2 0.5 ± 3.1f
Items with similar letters/symbols are significantly different. Pre- and post- taste MBG scores are compared within column; change in MBG scores are compared between columns.
a
Analysis utilized data from samples containing cocoa.
more chocolate is consistent with responses of well-being, euphoria and optimal functioning obtained on the MBG subscale after dopaminergic–opioidergic drug administration [14], as is the positive correlation of MBG subscale with “liking” for chocolate, since “liking” is thought to be an opioid mediated phenomenon [11]. While changes in the E and M subscales didn't contribute to the desire to consume more chocolate, liking contributed to the interindividual variability in changes in the E and M scores. In addition, amount of sugar and percent cocoa contributed to changes in the E subscale score in response to tasting chocolate. We can interpret these associations as related to a dopamine-mediated response as the E subscale measures subjective signs of excitement (i.e. fast heartbeat and light-headedness) and psychological feelings of well-being and thrill [14], all thought to be dopaminergic-mediated responses. While our human data agree with the rat data of Naleid et al. [8] on the primacy of sugar content of a high fat/high sugar food in driving intake and motivation to acquire that food, we also demonstrate a significant contribution of % cocoa to the desire to consume more chocolate. This finding of a contribution of % cocoa to the desire to consume more chocolate is consistent with that of Willner et al. [17] who demonstrated (in humans) a differential effect of choosing milk chocolate versus carob (a sugar containing, non-cocoa chocolate-taste substitute) in an operant task performed after induction of a negative mood due to listening to “sad” sounding music. Willner et al. [17] note that this laboratory method of inducing negative mood, correlates with “real-life” chronic mild stress. Several recent studies have also demonstrated the association of depressed mood with chocolate craving [18–20]. The mood ratings reported in this study averaged 63 ± 18 on a scale of 0 (extremely sad) to 100 (extremely happy) which would suggest that our participants are generally in a happy mood; however, sadness and stress are not synonymous. Therefore, since we did not specifically ask about level of stress, this explanation is still speculative. On the other hand, the contribution of cocoa to the desire to consume more chocolate can be discussed in relation to a report by Naleid et al. [8], who found no added contribution to reinforcement from the vanilla flavoring of their high fat/high sugar shake. Differences between humans and rats in eating/feeding behavior are not surprising as they are based on multiple and robust biological and environmental grounds. However, the chemical nature of vanilla flavoring versus chocolate flavoring may also have contributed to this finding. The flavoring component of vanilla is an oil [21], which would most likely have been concentrated in the fat component of Naleid's high fat/high sugar milk shake, while chocolate flavoring is liquefied, water soluble chocolate bean (chocolate “liquor”) [22]. The water soluble chocolate “liquor” would have been concentrated in the sugar component of the chocolates used in our study. Since sugar was the more salient reinforcer of the fat–sugar mixture, association with the sugar content could have improved cocoa discrimination and promoted increased desire. Additionally, all of our participants reported consuming chocolate regularly, while the rats in Naleid et al.'s [8] study were naïve to the corn oil/sugar milkshake with vanilla flavoring. Consequently, it is plausible that learned association between chocolate and “pleasure” contributed to our results, or that habitual consumption of chocolate entrained a positive reward response in our participants similar to that reported by Ángeles-Castellanos et al. [23] in a rodent model.
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It is possible that the physical form of our stimulus (solid chocolate) versus the liquid shake used by Naleid et al. [8] could have affected the sensitivity to experiencing psychoactive effects from our solid chocolate samples. In fact, the physical form of a drug is known to affect the reinforcing effects and addiction potential of stimulant and opioid drugs [24–26]. The physical form of foods is known to affect hunger and satiety in humans [27], and a similar phenomenon might also mediate sensory experiences from foods varying in physical form, especially when they can activate opioidergic and dopaminergic brain circuits. Drewnowski et al. [28] found that the perception of sweetness, fat content and creaminess was different when assessed in liquid compared to solid form, and that fat discrimination required higher fat concentrations in solid fat-containing food, compared to liquid fat-containing foods. Positive psychoactive responses elicited by sweet taste are also demonstrated by our finding that a sample (60% cocoa) containing sorbitol, rather than sugar, was able to produce changes in MBG scores equivalent to those produced by white chocolate and 38% cocoa samples (both containing an equivalent amount of sugar), possibly because sorbitol binds to the same taste receptors as sugar [29]. The similar responses from the sugar containing samples and the sorbitol containing sample suggest that it is potentially the binding to the sweet receptor, rather than the taste of sugar per se, that plays a major role in triggering the psychoactive effects of tasting chocolate. Studies using different classes of sweeteners would be needed to resolve this issue. Our most surprising result was that proportionally, more men than women reported a desire to consume more chocolate despite having significantly lower chocolate craving and liking scores. However, when asked to estimate “how much more chocolate” they would like to consume, the actual amount of additional chocolate desired by men, compared to that desired by women (4 pieces versus 3 pieces) merely approached significance (p = 0.064). A number of factors could possibly have contributed to the more frequent desire to consume more chocolate in men compared to women. On average, men had a higher BMI compared to the women, raising the possibility that women of our sample could have been more concerned with their body weight than the male participants and therefore more alert toward consumption of high energy = dense food [30], such as chocolate. Furthermore, women may not have admitted to desiring more chocolate due to social desirability bias [31]. Needless to say, these are hypotheses, given that we did not measure desired body weight or social desirability among our participants. 4.2. Limitations The current study has several limitations. As an observational study, we used commercially available chocolate samples in which fat, sugar and cocoa were varied simultaneously. While using commercially available chocolate gave a “real world” value to our observations, it hindered a direct assessment of the contribution of fat, sugar and cocoa individually to the MBG effects experienced and the “desire to consume more of this chocolate.” Additionally, since we did not measure changes in brain dopamine or opioids, the involvement of these neurotransmitters in experiencing MBG effects from tasting chocolate remains to be determined. Furthermore, because we collected data from passersby, we could not pre-select participants based upon characteristics that might have impacted the results, such as eating behavior phenotype, or family history of obesity. 4.3. Conclusions We have demonstrated that tasting chocolate has measurable psychoactive effects and that sugar and cocoa contents of chocolate are primarily related to the desire to consume more of it. To our knowledge this is the first report of use of a validated “drug-effect”
questionnaire to probe the psychoactive effects experienced from tasting a high sugar/high fat food. The data support our hypothesis that the psychoactive effects of chocolate are positively correlated with its sugar content. In addition, the data also support the hypothesis that cocoa content contributes to desirability of chocolate. Further studies assessing the time course of individual and interactive effects of fat, sugar and cocoa on psychoactive responses, activation of dopaminergic and opioidergic neurotransmitter circuits, and their contribution to overconsumption of high energy-dense food seem warranted. Role of funding sources This study was funded through start-up funds provided by the Office of the Provost of Drexel University. The Office of the Provost had no role in the study design, collection, analysis or interpretation of the data, writing the manuscript, or the decision to submit the paper for publication. Contributors JAN designed the study. LEB, JBL, OC, KF, JH, KJ, and BS drafted questionnaire items, collected the data and contributed to the writing of the manuscript. JAN and ADP conducted the statistical analysis, interpreted the data, and wrote the manuscript. Conflict of interest There are no conflicts of interest for any of the authors. Acknowledgments We thank Richard W Foltin, PhD for assistance in the use and interpretation of the ARCI, and Suzette M. Evans, PhD and Sami A Hasim, MD for their helpful suggestions in revising the manuscript. References [1] Van Horn L, Johnson RK, Flickinger BD, Vafiadis DK, Yin-Piazza S, Added Sugars Conference Planning Group. Translation and implementation of added sugars consumption recommendations: a conference report from the American Heart Association Added Sugars Conference 2010. Circulation 2010;122:2470–90. [2] Michener W, Rozin P. Pharmacological versus sensory factors in the satiation of chocolate craving. Physiol Behav 1994;56:419–22. [3] Osman JL, Sobal J. Chocolate cravings in American and Spanish individuals: biological and cultural influences. Appetite 2006;47:290–301. [4] Bruinsma K, Taren DL. Chocolate: food or drug? J Am Diet Assoc 1999;99:1249–56. [5] Smit HJ, Gaffan EA, Rogers PJ. Methylxanthines are the psycho-pharmacologically active constituents of chocolate. Psychopharmacology (Berl) 2004;176:412–9. [6] Avena NM, Rada P, Moise N, Hoebel BG. Sucrose sham feeding on a binge schedule releases accumbens dopamine repeatedly and eliminates the acetylcholine satiety response. Neuroscience 2006;139:813–20. [7] Liang NC, Hajnal A, Norgren R. Sham feeding corn oil increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol 2006;291:R1236–9. [8] Naleid AM, Grimm JW, Kessler DA, Sipols AJ, Aliakbari S, Bennett JL, et al. Deconstructing the vanilla milkshake: the dominant effect of sucrose on selfadministration of nutrient – flavor mixtures. Appetite 2008;50:128–38. [9] Berridge KC. Food reward: brain substrates of wanting and liking. Neurosci Biobehav Rev 1996;20:1–25. [10] Levine AS, Kotz CM, Gosnell BA. Sugars and fats: the neurobiology of preference. J Nutr 2003;133:831S–4S. [11] Davis CA, Levitan RD, Reid C, Carter JC, Kaplan AS, Patte KA, et al. Dopamine for “wanting” and opioids for “liking”: a comparison of obese adults with and without binge eating. Obesity 2009;17:1220–5. [12] Foltin RW, Fischman MW. The cardiovascular and subjective effects of intravenous cocaine and morphine combinations in humans. J Pharmacol Exp Ther 1992;261: 623–32. [13] Hill HE, Haertzen CA, Wolbach Jr AB, Miner EJ. The Addiction Research Center Inventory: standardization of scales which evaluate subjective effects of morphine, amphetamine, pentobarbital, alcohol, LSD-25, pyrahexyl and chlorpromazine. Psychopharmacologia 1963;4:167–83. [14] Haertzen CA, Hickey JE. Addiction Research Center Inventory (ARCI): measurement of euphoria and other drug effects. In: Bozarth MA, editor. Methods of assessing the reinforcing properties of abused drugs. New York: Springer-Verlag; 1987. p. 489–524.
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Physiology & Behavior j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p h b
Psychoactive effects of tasting chocolate and desire for more chocolate Jennifer A. Nasser a,⁎, Lauren E. Bradley a, Jessica B. Leitzsch a, Omar Chohan a, Kristy Fasulo a, Josie Haller a, Kristin Jaeger a, Benjamin Szulanczyk a, Angelo Del Parigi b a b
Department of Nutrition Sciences, Drexel University, Philadelphia, PA 19102, United States Department of Psychology, Drexel University, Philadelphia, PA 19102, United States
a r t i c l e
i n f o
Article history: Received 29 January 2011 Received in revised form 23 April 2011 Accepted 26 April 2011 Keywords: Addiction Research Center Inventory ARCI Food addiction Craving
a b s t r a c t The purpose of this study was to characterize the psychoactive effects of tasting chocolate and to evaluate the contribution of the main chocolate components to the desire to consume more of it. A total of 280 participants, (F-155; M = 125) ranging in age from 18–65, completed the study. Participants were randomly assigned to taste 12.5 g of either white chocolate (“control”) or one of four chocolate (“cocoa”) samples varying in sugar, fat and percent cocoa content, then answered the question: “Do you want more of this chocolate?” and “If yes, how many more pieces of this chocolate would you like to eat?” They completed pre- and post-consumption surveys, consisting of 30 questions derived from the Addiction Research Center Inventory (ARCI) subscales, Morphine–Benzedrine Group (MBG), Morphine (M) and Excitement (E). Significant decreases in post–pre consumption changes in MBG subscale were observed between the control sample and the 70% cocoa (p = 0.046) or the 85% cocoa sample (p = 0.0194). Proportionally more men than women wanted more of the tasted chocolate (p = 0.035). Participants were more likely to want more of the tasted chocolate if they displayed a greater change in the MBG scale, and if their chocolate sample had high sugar and cocoa content, as assessed by multiple logistic regression. Our results suggest that multiple characteristics of chocolate, including sugar, cocoa and the drug–like effects experienced, play a role in the desire to consume chocolate. © 2011 Elsevier Inc. All rights reserved.
1. Introduction Americans consume roughly 22 teaspoons (110 g) of added sugar per day [1]. Chocolate, a high sugar food, is considered to be the most craved substance in the U.S. [2,3]. Prior research suggests, however, that multiple components of chocolate, rather than just sugar, can potentially contribute to the desire to consume chocolate [4,5]. Theobromine and caffeine, (both methylxanthines contained in cocoa) are usually cited as the most salient contributors to chocolate craving [5]. However, Smit et al. [5] as well as Michener and Rozin [2] reported no role for the pharmacological content of methylxanthines in the oro-sensory relief of cravings for chocolate, most likely due to the lengthy post-ingestive time period (60–120 min) required for caffeine and theobromine blood levels to rise. Michener and Rozin [2] also reported that partial relief from craving for chocolate is observed even with the consumption of white chocolate (which does not contain cocoa, caffeine, and theobromine), and that an association exists between chocolate cravings and sensory properties of chocolate such as aroma, texture, and sweetness [2]. This suggests a prominent role for the sugar (sweetness) as well as for the fat (texture and
⁎ Corresponding author at: Drexel University, 245 N 15th Street, Mailstop #1030, Philadelphia, PA 19102, United States. Tel.: + 1 215 762 7363; fax: + 1 215 762 4080. E-mail address: [email protected] (J.A. Nasser). 0031-9384/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2011.04.040
aroma) components of chocolate in promoting desire for and consumption of chocolate. Animal studies on the consumption of food sources of fat and sugar other than chocolate, either as single components or in combination, demonstrate activation of multiple neurotransmitter systems [6–8], specifically dopaminergic and opioidergic circuits. Sustained increases in nucleus accumbens dopamine subsequent to consumption or sham feeding of sugar solutions [6] or corn oil solutions [7] can contribute to food wanting [9]. Neurobiological changes attributed to intake of sugar and fat combinations include increased release of dopamine in the cingulate cortex, hippocampus, nucleus accumbens, and locus ceruleus, in addition to increased gene expression of the endogenous opioid dynorphin in the arcuate nucleus of the hypothalamus [10] which can contribute to food liking [11]. The simultaneous activation of dopaminergic and opioidergic systems observed with ingestion and/or sham feeding of high fat and high sugar foods is similar to the pharmacodynamic effects exerted by combinations of a dopaminergic agonist (i.e. amphetamine, cocaine) and an opioidergic agonist, (i.e. morphine, heroin). These dopaminergic–opioidergic combinations are commonly referred to as “speedballs.” “Speedballs” are more reinforcing than either dopaminergic or opioidergic agonists used singularly, and produce a unique set of subjective effects [12] that can be measured using the Addiction Research Center Inventory (ARCI) subscales [13,14]. As a mixture of fat and sugar, chocolate might activate both the dopaminergic and
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opioidergic systems simultaneously, although, Naleid et al. [8] reported that when rats were given access to a vanilla flavored shake varying in fat and sugar, the sugar content was the most reinforcing component. In this human study, we characterized the psychoactive effects of tasting chocolate and investigated the contribution of the chocolate components to the desire to consume more of the specific chocolate tested. 2. Methods and materials 2.1. Methods 2.1.1. Participants This study was approved by the Institutional Review Board of Drexel University and met the requirements for exempt review; consequently, no written consent was required before participants took part in the experimental session. A “sample of convenience,” composed of 290 passersby at the Drexel University Student Center, volunteered to fill out a survey before and after tasting a single 12.5 g sample of chocolate varying in sugar, fat and percent cocoa content (Table 1). White chocolate was used as a “control” sample for chocolate, because it is similar in mouth feel and sweetness but does not contain cocoa, and a sorbitol-sweetened chocolate sample, similar in flavor and mouth feel to the other chocolate containing samples, was used to control for the contribution of sugar to the psychoactive effects of chocolate. We did not have access to a commercially available “fat-free” chocolate sample that had similar flavor and mouth feel properties as the other chocolate samples; therefore, no control for fat content effects was included in our study design. Volunteers were randomly assigned to taste 12.5 g of either white chocolate (i.e. control group) or one of four chocolate samples (i.e. cocoa groups) varying in sugar, fat and cocoa contents. Ten out of 290 participants failed to complete the study properly (either ate the chocolate before filling out the pre-consumption questionnaire or did not complete the post-consumption questionnaire); therefore, their data were not used in the analysis. 2.1.2. Data analysis Data were analyzed using SAS, ver. 8.2 (The SAS Institute, Cary, NC). General linear models were implemented to compare general characteristics (i.e. age, BMI, hunger, mood, chocolate liking and chocolate craving ratings) and ARCI subscale scores of each group (defined by the cocoa percentage of the chocolate sample tasted), and gender. ARCI subscale scores (pre- and post-chocolate consumption) were compared by paired t-Test. Segregation of desire to consume more chocolate by gender was assessed by chi-square test. Multiple logistic regression was employed to determine the individual variables contributing to the desire to consume more of the chocolate that was tasted. The threshold of significance was set at alpha = 0.05.
was calculated from the self-reported height and weight. Chocolate craving and liking were assessed with a Likert Scale as follows: “On a scale from 1 to 10 how much would you say that you crave chocolate?” and “On a scale from 1 to 10 how much would you say that you like chocolate?” Current hunger status was assessed using an anchored visual analog scale (VAS) with labeled intervals from 0 to 100 displayed as follows: 0 = Not hungry at all; 20 = Slightly hungry; 40 = Moderately hungry; 60 = Quite hungry; 80 = Very hungry; and 100 = Extremely hungry. Current mood and alertness were assessed by anchored VAS with labeled intervals including 0 = Extremely sad and Extremely drowsy; 50 = Neutral; and 100 = Extremely happy and Extremely alert. 2.2.2. Addiction Research Center Inventory (ARCI) A pre- and post-chocolate consumption questionnaire, composed of the exact same questions, was used to ask the volunteers a series of questions drawn from the following subscales of the ARCI: Morphine– Benzedrine Group (MBG), Morphine (M) and Excitement (E). These subscales are a series of drug effect questions that describe subjective feelings of individuals after having taken particular drugs. According to Haertzen and Hickey, [14] the MBG subscale measures well-being, euphoria, and optimal functioning, while the M subscale refers to physical sensations of itching and tingling, and the E subscale relates to physical signs of excitement, such as a fast heartbeat and lightheadedness, as well as psychological feelings of well-being and thrill. Selective use of various ARCI subscales has been reported in drug studies [15,16]. Our questionnaire adapted the ARCI subscales (MBG, M, and E) by removing items that were redundant between scales (i.e., from the MBG subscale: “I would be happy all the time if I felt as I do now”) or were not applicable to the study requirement of completing the questionnaires immediately before and after tasting a small chocolate sample (i.e., from the MBG subscale: “Today I say things in the easiest possible way,” and “I feel high,” or from the M subscale: “My speech is not as loud as usual”). Described symptoms that could be related to other conditions rather than to tasting the chocolate (i.e., from the M subscale: “I have been scratching myself,” and “I have been dozing occasionally for seconds or minutes”) were also removed. Additionally, the question “My nose itches” was changed to “My nose itches and/or is running” as this is a possible reaction to food. Pre- and post-consumption portions of the survey asked a total of 30 ARCI questions. Answers to each ARCI question were true/false. Each subscale awarded one point to certain questions if they were answered with the correct expected response (true or false); the total score was then tallied to give the subscale score per Haertzen and Hickey [14]. Two additional questions were included on the post-consumption questionnaire: “Would you want to eat more of this chocolate?” and “If yes, how many more pieces of this chocolate would you like to eat?” These two additional questions were analyzed separately and were not included as part of any subscale score.
2.2. Materials 3. Results 2.2.1. Background information questionnaire Participants were given a background information questionnaire to complete. Height and weight were self-reported and BMI (kg/m2) Table 1 Characteristics of chocolate samples. Chocolate type
% Cocoa
Sugar (g)
Fat (g)
Lindt® white Lindt® milk Russell Stover® Lindt® dark Lindt® dark
0 38 60 70 85
7.0 7.0 7.0a 3.5 1.6
4.5 3.9 3.7 5.5 5.9
Content is per 12.5 g piece of chocolate. a As sorbitol.
3.1. Demographics Participant demographics are displayed in Table 2. There were no significant differences between groups (defined by cocoa content of chocolate sample tasted) with respect to number of subjects, gender, age, BMI, hunger, mood, chocolate liking, or chocolate craving. The average value (Mean±SD), for demographic variables across all participants were: Age (yrs) 25±11, BMI (kg/m2) 24±4, Hunger 33±26, Mood 63± 18, Liking 8.5±2, Craving 6.1±2. Male (M) differed from female (F) participants in chocolate craving (M: 5.5±2.4; F: 6.6±2.4; t=3.74, p=0.0002) and liking (M: 8.2±1.7; F: 8.7±1.8; t=2.45, p=0.015), as well as in BMI (M: 24.5±3.9; F: 22.9±3.7: t=3.48 p=0.0006), but not in hunger (M: 35±27; F: 31±25; p=0.15).
J.A. Nasser et al. / Physiology & Behavior 104 (2011) 117–121 Table 2 Demographics of participants grouped by% cocoa of sample tasted. Mean ± SD.
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Table 4 Logistic regression of contributors to “desire to consume more of the tasted chocolate”.a
Variable
0% Cocoa
38% Cocoa
60% Cocoa
70% Cocoa
85% Cocoa
Variable
O.R.
CI (95%)
Wald Chi-sq
P
N Women Men Age BMI Hunger Mood Liking Craving
57 33 24 24.9 ± 9.5 23.3 ± 4.3 31 ± 28 65 ± 20 8.2 ± 1.8 5.9 ± 2.7
57 31 26 23.8 ± 8.7 24.4 ± 3.2 31 ± 27 64 ± 17 8.4 ± 1.8 6.0 ± 2.2
55 26 29 28.2 ± 12.4 23.8 ± 3.5 33 ± 25 59 ± 18 8.7 ± 1.2 6.4 ± 2.5
57 31 26 24.8 ± 11.3 23.2 ± 3.6 39 ± 27 62 ± 16 8.3 ± 2.0 5.9 ± 2.3
54 34 20 26.4 ± 11.3 23.6 ± 4.8 29 ± 22 66 ± 18 8.6 ± 1.8 6.3 ± 2.5
Sugar grams Change in MBG Cocoa (percent) Fat grams BMI
3.789 1.413 1.037 7.681 0.973
1.394–10.298 1.210–1.650 1.002–1.073 0.875–67.460 0.885–1.069
6.818 19.126 4.314 3.382 0.334
0.009 b0.0001 0.038 0.066 0.6
3.2. Effect of sugar, fat and cocoa on ARCI subscale scores Cocoa groups differed from the control group in sugar, fat and cocoa contents of the sample. Significant within group increases were seen between pre- and post-chocolate ingestions in the MBG subscale for control and cocoa samples through 70% cocoa (Table 3). Between group (cocoa groups versus control) differences in MBG score changes were significant for the 70 and 85% cocoa groups (p = 0.041 and p = 0.019, respectively). These two groups had lower concentrations of sugar: (3.5 g for the 70% and 1.625 g for the 85%) compared to the control (7 g). In multiple regression models, including age, BMI, craving, liking, hunger, mood, grams of sugar, grams of fat, and percent of cocoa, changes in MBG score were associated with liking (p = 0.034), while changes in the E score were associated with age (p = 0.004), liking (p = 0.029), percent of cocoa (p = 0.015), and grams of sugar (0.042). Changes in the M score were not significantly associated with any variable, but the association with craving approached significance (p = 0.057). 3.3. Desire for more chocolate A significantly greater number of men reported a desire for “more of the chocolate tasted” compared to women (chi-square p = 0.0349). Among those reporting a desire for additional chocolate, the difference in amount of additional pieces of chocolate desired between men and women approached significance (M: 4.0 ± 3.5; F: 3.0 ± 2.5; F = 3.5, p = 0.064). Logistic regression analysis revealed that the desire to consume more of the chocolate sample (which had been tasted) was associated with a greater amount of sugar and cocoa in the sample, and with greater post = consumption increases in the MBG subscale (Table 4). 4. Discussion 4.1. Summary of findings Our data indicate that tasting chocolate has measurable psychoactive effects in humans, which in turn are associated with the desire to consume more of it. This desire is proportional to the chocolate's sugar and cocoa contents. This is the first demonstration in humans of such effects using a validated “drug effects” questionnaire. The association of changes in MBG subscale with desire to consume Table 3 Comparison of MBG changes: cocoa versus white chocolate control. Mean ± SD. Variable
0% Cocoa Control
38% Cocoa
60% Cocoa
70% Cocoa
85% Cocoa
N Pretaste MBG Posttaste MBG Change in MBG
57 5.0 ± 3.6a 7.0 ± 3.9a 2.0 ± 2.1ef
57 4.6 ± 3.5b 6.4 ± 3.9b 1.8 ± 2.9
55 5.1 ± 3.4c 6.8 ± 3.9c 1.7 ± 2.6
57 5.2 ± 3.6d 6.1 ± 3.7d 0.9 ± 2.6e
54 5.3 ± 3.5 5.8 ± 4.2 0.5 ± 3.1f
Items with similar letters/symbols are significantly different. Pre- and post- taste MBG scores are compared within column; change in MBG scores are compared between columns.
a
Analysis utilized data from samples containing cocoa.
more chocolate is consistent with responses of well-being, euphoria and optimal functioning obtained on the MBG subscale after dopaminergic–opioidergic drug administration [14], as is the positive correlation of MBG subscale with “liking” for chocolate, since “liking” is thought to be an opioid mediated phenomenon [11]. While changes in the E and M subscales didn't contribute to the desire to consume more chocolate, liking contributed to the interindividual variability in changes in the E and M scores. In addition, amount of sugar and percent cocoa contributed to changes in the E subscale score in response to tasting chocolate. We can interpret these associations as related to a dopamine-mediated response as the E subscale measures subjective signs of excitement (i.e. fast heartbeat and light-headedness) and psychological feelings of well-being and thrill [14], all thought to be dopaminergic-mediated responses. While our human data agree with the rat data of Naleid et al. [8] on the primacy of sugar content of a high fat/high sugar food in driving intake and motivation to acquire that food, we also demonstrate a significant contribution of % cocoa to the desire to consume more chocolate. This finding of a contribution of % cocoa to the desire to consume more chocolate is consistent with that of Willner et al. [17] who demonstrated (in humans) a differential effect of choosing milk chocolate versus carob (a sugar containing, non-cocoa chocolate-taste substitute) in an operant task performed after induction of a negative mood due to listening to “sad” sounding music. Willner et al. [17] note that this laboratory method of inducing negative mood, correlates with “real-life” chronic mild stress. Several recent studies have also demonstrated the association of depressed mood with chocolate craving [18–20]. The mood ratings reported in this study averaged 63 ± 18 on a scale of 0 (extremely sad) to 100 (extremely happy) which would suggest that our participants are generally in a happy mood; however, sadness and stress are not synonymous. Therefore, since we did not specifically ask about level of stress, this explanation is still speculative. On the other hand, the contribution of cocoa to the desire to consume more chocolate can be discussed in relation to a report by Naleid et al. [8], who found no added contribution to reinforcement from the vanilla flavoring of their high fat/high sugar shake. Differences between humans and rats in eating/feeding behavior are not surprising as they are based on multiple and robust biological and environmental grounds. However, the chemical nature of vanilla flavoring versus chocolate flavoring may also have contributed to this finding. The flavoring component of vanilla is an oil [21], which would most likely have been concentrated in the fat component of Naleid's high fat/high sugar milk shake, while chocolate flavoring is liquefied, water soluble chocolate bean (chocolate “liquor”) [22]. The water soluble chocolate “liquor” would have been concentrated in the sugar component of the chocolates used in our study. Since sugar was the more salient reinforcer of the fat–sugar mixture, association with the sugar content could have improved cocoa discrimination and promoted increased desire. Additionally, all of our participants reported consuming chocolate regularly, while the rats in Naleid et al.'s [8] study were naïve to the corn oil/sugar milkshake with vanilla flavoring. Consequently, it is plausible that learned association between chocolate and “pleasure” contributed to our results, or that habitual consumption of chocolate entrained a positive reward response in our participants similar to that reported by Ángeles-Castellanos et al. [23] in a rodent model.
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It is possible that the physical form of our stimulus (solid chocolate) versus the liquid shake used by Naleid et al. [8] could have affected the sensitivity to experiencing psychoactive effects from our solid chocolate samples. In fact, the physical form of a drug is known to affect the reinforcing effects and addiction potential of stimulant and opioid drugs [24–26]. The physical form of foods is known to affect hunger and satiety in humans [27], and a similar phenomenon might also mediate sensory experiences from foods varying in physical form, especially when they can activate opioidergic and dopaminergic brain circuits. Drewnowski et al. [28] found that the perception of sweetness, fat content and creaminess was different when assessed in liquid compared to solid form, and that fat discrimination required higher fat concentrations in solid fat-containing food, compared to liquid fat-containing foods. Positive psychoactive responses elicited by sweet taste are also demonstrated by our finding that a sample (60% cocoa) containing sorbitol, rather than sugar, was able to produce changes in MBG scores equivalent to those produced by white chocolate and 38% cocoa samples (both containing an equivalent amount of sugar), possibly because sorbitol binds to the same taste receptors as sugar [29]. The similar responses from the sugar containing samples and the sorbitol containing sample suggest that it is potentially the binding to the sweet receptor, rather than the taste of sugar per se, that plays a major role in triggering the psychoactive effects of tasting chocolate. Studies using different classes of sweeteners would be needed to resolve this issue. Our most surprising result was that proportionally, more men than women reported a desire to consume more chocolate despite having significantly lower chocolate craving and liking scores. However, when asked to estimate “how much more chocolate” they would like to consume, the actual amount of additional chocolate desired by men, compared to that desired by women (4 pieces versus 3 pieces) merely approached significance (p = 0.064). A number of factors could possibly have contributed to the more frequent desire to consume more chocolate in men compared to women. On average, men had a higher BMI compared to the women, raising the possibility that women of our sample could have been more concerned with their body weight than the male participants and therefore more alert toward consumption of high energy = dense food [30], such as chocolate. Furthermore, women may not have admitted to desiring more chocolate due to social desirability bias [31]. Needless to say, these are hypotheses, given that we did not measure desired body weight or social desirability among our participants. 4.2. Limitations The current study has several limitations. As an observational study, we used commercially available chocolate samples in which fat, sugar and cocoa were varied simultaneously. While using commercially available chocolate gave a “real world” value to our observations, it hindered a direct assessment of the contribution of fat, sugar and cocoa individually to the MBG effects experienced and the “desire to consume more of this chocolate.” Additionally, since we did not measure changes in brain dopamine or opioids, the involvement of these neurotransmitters in experiencing MBG effects from tasting chocolate remains to be determined. Furthermore, because we collected data from passersby, we could not pre-select participants based upon characteristics that might have impacted the results, such as eating behavior phenotype, or family history of obesity. 4.3. Conclusions We have demonstrated that tasting chocolate has measurable psychoactive effects and that sugar and cocoa contents of chocolate are primarily related to the desire to consume more of it. To our knowledge this is the first report of use of a validated “drug-effect”
questionnaire to probe the psychoactive effects experienced from tasting a high sugar/high fat food. The data support our hypothesis that the psychoactive effects of chocolate are positively correlated with its sugar content. In addition, the data also support the hypothesis that cocoa content contributes to desirability of chocolate. Further studies assessing the time course of individual and interactive effects of fat, sugar and cocoa on psychoactive responses, activation of dopaminergic and opioidergic neurotransmitter circuits, and their contribution to overconsumption of high energy-dense food seem warranted. Role of funding sources This study was funded through start-up funds provided by the Office of the Provost of Drexel University. The Office of the Provost had no role in the study design, collection, analysis or interpretation of the data, writing the manuscript, or the decision to submit the paper for publication. Contributors JAN designed the study. LEB, JBL, OC, KF, JH, KJ, and BS drafted questionnaire items, collected the data and contributed to the writing of the manuscript. JAN and ADP conducted the statistical analysis, interpreted the data, and wrote the manuscript. Conflict of interest There are no conflicts of interest for any of the authors. Acknowledgments We thank Richard W Foltin, PhD for assistance in the use and interpretation of the ARCI, and Suzette M. Evans, PhD and Sami A Hasim, MD for their helpful suggestions in revising the manuscript. References [1] Van Horn L, Johnson RK, Flickinger BD, Vafiadis DK, Yin-Piazza S, Added Sugars Conference Planning Group. Translation and implementation of added sugars consumption recommendations: a conference report from the American Heart Association Added Sugars Conference 2010. Circulation 2010;122:2470–90. [2] Michener W, Rozin P. Pharmacological versus sensory factors in the satiation of chocolate craving. Physiol Behav 1994;56:419–22. [3] Osman JL, Sobal J. Chocolate cravings in American and Spanish individuals: biological and cultural influences. Appetite 2006;47:290–301. [4] Bruinsma K, Taren DL. Chocolate: food or drug? J Am Diet Assoc 1999;99:1249–56. [5] Smit HJ, Gaffan EA, Rogers PJ. Methylxanthines are the psycho-pharmacologically active constituents of chocolate. Psychopharmacology (Berl) 2004;176:412–9. [6] Avena NM, Rada P, Moise N, Hoebel BG. Sucrose sham feeding on a binge schedule releases accumbens dopamine repeatedly and eliminates the acetylcholine satiety response. Neuroscience 2006;139:813–20. [7] Liang NC, Hajnal A, Norgren R. Sham feeding corn oil increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol 2006;291:R1236–9. [8] Naleid AM, Grimm JW, Kessler DA, Sipols AJ, Aliakbari S, Bennett JL, et al. Deconstructing the vanilla milkshake: the dominant effect of sucrose on selfadministration of nutrient – flavor mixtures. Appetite 2008;50:128–38. [9] Berridge KC. Food reward: brain substrates of wanting and liking. Neurosci Biobehav Rev 1996;20:1–25. [10] Levine AS, Kotz CM, Gosnell BA. Sugars and fats: the neurobiology of preference. J Nutr 2003;133:831S–4S. [11] Davis CA, Levitan RD, Reid C, Carter JC, Kaplan AS, Patte KA, et al. Dopamine for “wanting” and opioids for “liking”: a comparison of obese adults with and without binge eating. Obesity 2009;17:1220–5. [12] Foltin RW, Fischman MW. The cardiovascular and subjective effects of intravenous cocaine and morphine combinations in humans. J Pharmacol Exp Ther 1992;261: 623–32. [13] Hill HE, Haertzen CA, Wolbach Jr AB, Miner EJ. The Addiction Research Center Inventory: standardization of scales which evaluate subjective effects of morphine, amphetamine, pentobarbital, alcohol, LSD-25, pyrahexyl and chlorpromazine. Psychopharmacologia 1963;4:167–83. [14] Haertzen CA, Hickey JE. Addiction Research Center Inventory (ARCI): measurement of euphoria and other drug effects. In: Bozarth MA, editor. Methods of assessing the reinforcing properties of abused drugs. New York: Springer-Verlag; 1987. p. 489–524.
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