Impulsivity toward food reward is related to BMI: Evidence from intertemporal choice in obese and normal-weight individuals

Brain and Cognition xxx (2015) xxx–xxx

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Impulsivity toward food reward is related to BMI: Evidence from intertemporal choice in obese and normal-weight individuals Sami Schiff a,⇑, Piero Amodio a, Giulia Testa a, Mariateresa Nardi b, Sara Montagnese a, Lorenza Caregaro a, Giuseppe di Pellegrino c, Manuela Sellitto c,d,⇑ a

Department of Medicine – DIMED, University of Padova, Italy Veneto Institute of Oncology – IOV IRCCS, Padova, Italy Centre for Studies and Research in Cognitive Neuroscience, Department of Psychology, University of Bologna, Italy d Justus-Liebig-Universität Giessen, Department of Biological Psychology, Germany b c

a r t i c l e

i n f o

Article history: Received 29 May 2015 Revised 14 October 2015 Accepted 15 October 2015 Available online xxxx Keywords: Temporal discounting Impulsivity Food reward Obesity BMI Executive functions Psychopathology

a b s t r a c t Obesity is a medical condition frequently associated with psychopathological symptoms and neurocognitive and/or personality traits related to impulsivity. Impulsivity during intertemporal choices seems to be typical of obese individuals. However, so far, the specific relationship between different types of reward and neuropsychological and psychopathological profile are yet to be unravelled. Here, we investigated impulsive choice for primary and secondary reward in obese individuals and normal-weight controls with comparable neuropsychological and psychopathological status. Participants performed three intertemporal choice tasks involving food, money, and discount voucher, respectively. Moreover, they completed a battery of neuropsychological tests and psychometric questionnaires assessing psychopathological state, impulsivity, and personality traits. Obese individuals showed increased preference for immediate food reward compared with controls, whereas no group difference emerged concerning money and discount voucher. Moreover, the higher the body mass index (BMI), the steeper the food discounting. These findings emerged in light of comparable neuropsychological and psychopathological profile between groups. Steeper food discounting in obese individuals appears to be related to BMI but not to psychopathological and neuropsychological profile. We suggest using intertemporal choice in the clinical practice as measure of the effectiveness of different types of intervention (e.g., educational, psychological, pharmacological or surgical) aimed at reducing impulsivity toward food and increasing cognitive control during food intake in obese individuals. Ó 2015 Elsevier Inc. All rights reserved.

1. Introduction The daily consumption of excessive quantity of food is typical of obesity and binge eating disorder (BED). Central to these pathologies is the exaggerate saliency of food reward at the expense of other rewards (Volkow, Wang, Fowler, & Telang, 2008). This results in increased engagement in impulsive behavior and decision toward immediate food outcome (Davis, Levitan, Muglia, Bewell, & Kennedy, 2004; Volkow, Baler, & addiction. Tics, in press). During intertemporal choice (i.e., decision between smaller-immediate outcome and larger-delayed outcome) the ability to postpone ⇑ Corresponding authors at: Department of Medicine – DIMED, Via Giustiniani 2, 37047 Padova, Italy (S. Schiff). Justus-Liebig-Universität Giessen, FB06 – Department of Biological Psychology, Otto-Behaghel-Straße 10, F2 Building, Room 133, 35394 Gießen, Germany (M. Sellitto). E-mail addresses: [email protected] (S. Schiff), Manuela.Sellitto@psychol. uni-giessen.de (M. Sellitto).

immediate gratification is crucial to achieve healthy long-term goals, including weight control and the cessation of drug misuse (Sellitto, Ciaramelli, & di Pellegrino, 2011). Humans typically devalue rewards as a function of time availability, a phenomenon known as temporal discounting (TD) of future rewards (Ainslie, 1974). Namely, the subjective value of a reward is greater when delivered immediately (e.g., the gratification coming from eating a chocolate praline) than when delivered in the future (e.g., losing weight by being on a diet for one month) (Cardinal, Pennicott, Sugathapala, Robbins, & Everitt, 2001; Green & Myerson, 2004; Kalenscher et al., 2005; Myerson & Green, 1995). The less individuals are able to override tempting immediate reward in favor of long-term gain, the more they are considered impulsive (Frederick, Loewenstein, & O’Donoghue, 2002; Sellitto et al., 2011). Several studies showed that obese individuals have increased preference for smaller-immediate gratification over largerdelayed reward as compared with healthy controls. Specifically,

http://dx.doi.org/10.1016/j.bandc.2015.10.001 0278-2626/Ó 2015 Elsevier Inc. All rights reserved.

Please cite this article in press as: Schiff, S., et al. Impulsivity toward food reward is related to BMI: Evidence from intertemporal choice in obese and normal-weight individuals. Brain and Cognition (2015), http://dx.doi.org/10.1016/j.bandc.2015.10.001

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S. Schiff et al. / Brain and Cognition xxx (2015) xxx–xxx

higher discount rate for hypothetical future money has been found in obese women compared to normal-weight women (Davis, Patte, Curtis, & Reid, 2010; Davis et al., 2004; Weller, Cook, Avsar, & Cox, 2008), and in obese smokers adolescents compared to their normal-weight peers (Field, Santarcangelo, Sumnall, Goudie, & Cole, 2006). In addition, impulsivity toward immediate monetary reward predicted the amount of caloric intake in obese individuals (Appelhans, Pagotom, Schneider, Whited, & Liebman, 2011). Impulsivity toward immediate reward has been recently associated with different psychopathological (i.e., addiction and anxiety), and neuropsychological conditions (i.e., executive disfunctioning), as well as personality traits (i.e., reward dependence and harm avoidance) (Bickel, Jarmolowicz, Mueller, Koffarnus, & Gatchalianm, 2012; Huckans et al., 2010; Jenks & Lawyer, 2015; MacKillop et al., 2011; Malesza & Ostaszewski, 2013; Rounds, Beck, & Grant, 2007; Sellitto et al., 2011; Story, Vlaev, Seymour, Darzi, & Dolan, 2014). All these factors may lead to misinterpretation of findings related to TD when the effect of obesity and BMI is assessed. For instance, depression has been suggested to be a moderator of impulsivity toward immediate palatable food reward in overweight/obese individuals (Privitera, McGrath, Windus, & Doraiswamy, 2015), thereby saliency attribution to food might be modulated by psychopathological factors. However, most obese people do not show clear psychopathological condition related to behavioral disinhibition, such as binge eating disorder or depression, and obesity is not classified as a mental disorder (Berkowitz & Fabricatore, 2011; Carpiniello et al., 2009; Fabricatore, Wadden, Sarwer, & Faith, 2005; Malik, Mitchell, Engel, Crosby, & Wonderlich, 2014). An alternative explanation may lay in the repeated stimulation of the reward system induced by prolonged exposure to the rewarding stimulus (i.e., food), which would lead to maladaptive stimulus-reward associations. This, in turn, would contribute to an enhancement of the incentive value of a reward at the expense of others (Berridge & Robinson, 1998). Thus, despite the absence of traits of impulsivity and alterations in response inhibition and cognitive control, an exaggerate saliency of food reward, at the expense of other rewards, could be hypothesized in obese individuals without binge eating. This may results in increased engagement in impulsive behavior and decision specifically toward immediate food outcome in this population (Davis et al., 2004). It has been also suggested that the preference for smaller but immediate rewards could be related to body mass index (BMI): The higher the BMI, the higher the degree of impulsivity toward immediate rewards (e.g., Ikeda, Kang, & Ohtake, 2010). However, most of TD research in humans focused on monetary reward (Critchfield & Kollins, 2001; Reynolds, 2006), and, to our knowledge, only two studies assessed discounting behaviour for both food and monetary rewards in participants with BMI raging from normal-weight to obesity (Manwaring, Green, Myerson, Strube, & Wilfley, 2011; Rasmussen, Lawyer, & Reilly, 2010). In one (Rasmussen et al., 2010), BMI was found not to be a predictor of discounting behaviour for neither food nor monetary reward. In the other (Manwaring et al., 2011), obese individuals with BED, characterized by compulsive eating, were more sensitive to immediate gratifications independently of reward type, whereas obese individuals without BED selectively showed greater sensitivity to immediate food reward as compared to normal-weight individuals. However, this latter study did not explore the relationship between the degree of discounting of future food reward and BMI. In the present study, we tried to reconcile previous discrepancies by investigating intertemporal choice for both primary (i.e., food) and secondary (i.e., money and discount voucher) reward in obese individuals and normal-weight controls in a more systematic manner. Participants made a series of hypothetical decisions between smaller-immediate amounts of rewards and

larger-delayed amounts of rewards, separately for each commodity. Furthermore, to avoid the possibility that differences between obese and normal-weight individuals in the TD tasks might depend on more general differences in neuropsychological and psychological factors related to impulsivity, we submitted participants to several tests. Neuropsychological evaluation focused on the assessment of major executive functions, frequently reported to be altered in obese compared to normal weight individuals (Prickett, Brennan, & Stolwyk, 2015). Thus, a series of paper and pencil as well as computerized measures were adopted to investigate different executive domains, as for instance cognitive control (through the Simon task), attention and switching ability (through the Trial Making Test A, B), and working memory (through the Sternberg test). Moreover, subjects filled out questionnaires assessing impulsivity, personality traits, and the presence of psychopathological state at the time of the study, which are variables that may be linked to discounting behavior (e.g., Ostaszewski, 1998). This, in order to: (i) replicate previous findings of increased discounting for future reward in obese population; (ii) to investigate whether obese people’s impulsivity is selective for food, independently from others psychopathological/neuropsychological factors. Thus, in line with the incentive sensitization theory, we hypothesized that even in absence of impulsivity traits, binge eating disorder, or other psychopathological and neuropsychological condition related to behavioral disregulation, obese individuals would be more impulsive than normal-weight controls when faced with food stimuli compared with money and discount voucher, and that this tendency would be positively related to BMI.

2. Materials and methods 2.1. Participants Twenty-three obese subjects and 23 normal-weight subjects matched on age and education were enrolled in the study (Table 1). Inclusion criteria consisted of BMI > 30 kg/m2 (obese) or BMI ranging between 19 and 26 kg/m2 (normal-weight controls), and age ranging between 18 and 50 years (see Table 1 for demographic details). Exclusion criteria for all participants were the presence of clinical history of eating and/or other neurological/psychiatric disorders, history of alcohol and/or drug abuse, diabetes and arterial hypertension. Individuals with endocrine deregulation diseases were also excluded from the study. The DSM-IV TR criteria (American Psychiatric Association, 2000) to diagnose binge eating disorder were explored during the initial clinical interview. Participants were recruited in collaboration with the Clinical Nutrition and Diet Unit of the Padua University Hospital, whereby obese participants included patients under nutritional treatment to control weight. The study was approved by the local Hospital ethical committee, and was carried out according to the Helsinki Declaration

Table 1 Demographics. Demographic variables

Normal-weight Mean (SD)

Obese Mean (SD)

Gender (F/M) Age (years) Education (years) Height (m) Weight (kg) BMI (kg/m2)

18/5 33.8 (8.9) 15.1 (3.2) 1.64 (0.07) 60.6 (7.7) 22.4 (2.2)

18/5 36.2 (9.5) 13.2 (3.3) 1.68 (0.08) 102.9 (22.5)** 36.2 (5.7)**

Notes: SD = standard deviation; F = female; M = male, m = meter; kg = kilogram; BMI = Body Mass Index. ** p < .001.

Please cite this article in press as: Schiff, S., et al. Impulsivity toward food reward is related to BMI: Evidence from intertemporal choice in obese and normal-weight individuals. Brain and Cognition (2015), http://dx.doi.org/10.1016/j.bandc.2015.10.001

S. Schiff et al. / Brain and Cognition xxx (2015) xxx–xxx

(Statements from the International Committee of Medical Journal Editors). 2.2. Procedure All participants were tested between 2 pm and 3 pm. Since food deprivation might interact with food salience (Stockburger, Weike, Hamm, & Schupp, 2008) and obese individuals in a fed condition react differently to food image compared to normal-weight participants (Castellanos et al., 2009), in the present study, we did not require participants to abstain from eating prior to the experimental session. However, information about quality, quantity, and time since their last meal or snack were collected, as well as their subjective feeling of hunger was recorded, in order to control for macroscopic differences between subjects. After providing informed consent for participation, we collected participants’ weight and height, and BMI was calculated by dividing weight in kilograms by the square of height in meters (km/m2). Participants included in the study were submitted to three computerized TD tasks and to a neuropsychological evaluation including both computerized and paper and pencil tests. At the end of the experimental session, they also completed a series of questionnaires (see below for all details). The experiment lasted  2 h. 2.3. Temporal discounting (TD) task Participants performed three computerized TD tasks (based on Sellitto, Ciaramelli, & di Pellegrino, 2010) investigating intertemporal choice for three different rewards, respectively: food, money (€), and discount voucher. All rewards were hypothetical (e.g., Bickel, Pitcock, Yi, & Angtuaco, 2009; Sellitto et al., 2010). Before starting the TD tasks, participants were invited to select their preferred food and discount voucher by choosing them among four alternatives, respectively, displayed on a computer screen. The food options included two sweet (chocolate bar and cookie) and two salty snacks (breadstick and crackers); vouchers included discount for a museum tour, gym session, hairdresser/barber session, and book purchase. The preferred food and voucher were used as reward stimuli for the food TD task and the discount voucher TD task, respectively. Moreover, participants rated liking and wanting for the chosen food, with two 9-points Likert scales ranging from 1 (i.e., ‘‘I don’t like/want this food at all”) to 9 (i.e., ‘‘I extremely like/ want this food”), in order to avoid results to be driven by differences in preference for food (Berridge, 2009). Immediately after the reward selection phase, the three TD tasks were administered across participants separately, in a counterbalanced order. In each trial, participants choose between a smaller amount of reward that could be received immediately and a larger one that could be received after a specific time delay. Specifically, they were told that, on each trial, two amounts of a hypothetical reward would appear on the screen. One could be received right now, and one could be received after a delay. They were informed that there were no correct or incorrect choices, and were required to indicate the option they preferred by pressing one of two buttons. In each of the three TD tasks, volunteers made five choices at each of six delays: 2 days, 2 weeks, 1, 3, and 6 months, and 1 year. The order of blocks of choices pertaining to different delays was randomly determined across participants. Within each block of five choices, the delayed amount was always 40 units. The amount of the immediate reward, on the other hand, was adjusted based on the subject’s choices, using a titration procedure that converged on the amount of the immediate reward that was equal, in subjective value, to the delayed reward. The smallest amount for the immediate option could be 1 unit and the largest amount for the immediate option could be 39 units. In each block, the first choice was always between a delayed

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amount of 40 units (e.g., 40 bites or tastes of cookie) and an immediate amount of 20 units (e.g., 20 bites of cookie). If the participant chose the immediate reward, then the amount of the immediate reward was decreased on the next trial; if the subject chose the delayed reward, then the amount of the immediate reward was increased on the next trial. The size of the adjustment in the immediate reward decreased with successive choices: the first adjustment was half of the difference between the immediate and the delayed reward, whereas for subsequent choices it was half of the previous adjustment (Myerson, Green, Hanson, Holt, & Estle, 2003; Sellitto et al., 2010). This procedure was repeated until the subject had made her five choices at one specific delay, after which she began a new series of choices at another delay. For each trial in a block, the immediate amount represents the best guess as to the subjective value of the delayed reward. Thus, the immediate amount that would have been presented on the sixth trial of a delay block was taken as the estimate of the subjective value of the delayed reward at that delay (Sellitto & di Pellegrino, 2014; Sellitto et al., 2010). Participants were told that, on each trial, two amounts of hypothetical reward would appear on the screen. One could be received right now, and one could be received after a temporal delay. They were explicitly asked to imagine receiving and consuming the two amounts of reward at the due time, they were told that rewards did not cumulate trial after trial, and they were required to indicate the option they preferred by pressing one of two buttons on a keyboard (Estle, Green, Myerson, & Holt, 2007). They were also informed that there were no correct or incorrect choices. Fig. 1 illustrates the experimental paradigm. For each of the three TD task, the hyperbolic discounting function (see Sellitto et al., 2010) was fit to the data to determine the k constant of the best fitting TD function. The larger the value of k, the steeper the discounting function, the more participants were inclined to choose small-immediate rewards over larger-delayed rewards.

2.4. Neuropsychological assessment 2.4.1. Trail-Making Test (TMT) The age and educational adjusted Italian version of the TMT (Amodio et al., 2008) task A (TMT-A) assesses visual search, selective attention, and psychomotor speed. The TMT task B (TMT-B) assesses psychomotor speed, visual search, working memory, and the ability to switch between series of numbers and letters. The time needed to connect the twenty-five circles printed on a paper sheet was collected separately for the TMT-A and TMT-B, respectively.

2.4.2. Frontal Assessment Battery (FAB) The FAB (Appollonio et al., 2005) is a short screening tool for the assessment of global executive functions. FAB consists of six subtests assessing cognitive and behavioral domains that are thought to be under the control of the frontal lobes: abstract reasoning, lexical verbal fluency and mental flexibility, motor programming and executive control of action, self-regulation and resistance to interference, inhibitory control, and environmental autonomy. A global score is calculated by summing the six individual FAB subtasks scores.

2.4.3. Simple Reaction Time (RTs) task Subjects were asked to press as fast as possible the spacebar of a computer keyboard every time an asterisk was presented on the centre of the screen. Accuracy and RTs were calculated.

Please cite this article in press as: Schiff, S., et al. Impulsivity toward food reward is related to BMI: Evidence from intertemporal choice in obese and normal-weight individuals. Brain and Cognition (2015), http://dx.doi.org/10.1016/j.bandc.2015.10.001

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Fig. 1. Example of a TD task trial with food reward. In every trial participants were invited to choose between two options: a small amount of reward delivered immediately and a larger amount of reward delivered after a delay. The two options appeared on the left and right side of the screen, and clearly indicated the food type, the amount of reward, and the delay of delivery of the reward. After participant’s choice, the non-preferred option disappeared, whereas the preferred option remained on the screen for 1 s, with a triangle underneath it (1000 ms), after which a fixation point (1000 ms) appeared and a new trial started.

2.4.4. Choice Reaction Time (RTs) task Two different numbers were presented on a computer screen in a random order, and subjects were asked to press the buttons of a numerical keypad according to the displayed number. Accuracy and mean RTs were calculated. 2.4.5. Sternberg task A digit recognition task based on the Sternberg paradigm (Montagnese et al., 2012; Sternberg, 1966) evaluates working memory capacity. Mean accuracy and RTs were calculated.

that are thought to be moderately heritable and stable throughout life. Four temperament dimensions were measured: Novelty Seeking, Harm Avoidance, Reward Dependence and Persistence. Character refers to self-concepts and individual differences in goals values, which influence voluntary choices, intentions, and the meaning of what is experienced in life. Three characters dimensions were measured: Cooperativeness, Self-Directedness and Self-Transcendence.

3. Results 2.4.6. Simon task The Simon task is a stimulus–response spatial interference task assessing the ability to control conflict in location. RTs are typically faster when the stimulus and response positions correspond spatially (Congruent condition), and slow down when the stimulus and response positions do not correspond (Incongruent condition). Accuracy and mean RTs were calculated for Congruent and Incongruent conditions separately. For more details on the Simon task adopted in the preset study see Vallesi, Mapelli, Schiff, Amodio, & Umiltà (2005) or Schiff et al. (2014). 2.5. Self-report scales 2.5.1. Barratt Impulsiveness Scale (BIS-11) The BIS-11 (Fossati, Di Ceglie, Acquarini, & Barratt, 2001) evaluates everyday behaviors reflecting impulsivity. Specifically, it assesses three facets of impulsivity: attentional impulsivity (AI sub-scale, e.g., ‘‘I am more interested in the present than the future”), motor impulsivity (MI subscale, e.g., ‘‘I do things without thinking”), and impulsive nonplanning (INP subscale, e.g., ‘‘I make up my mind quickly”). High BIS-11 scores indicate high levels of impulsivity. 2.5.2. Symptom checklist 90 Revised (SCL90-R) The SCL90-R (Derogatis & Unger, 2010) evaluates a broad range of psychopathological symptoms. Participants rated the frequency of symptoms in the last two weeks along ten dimensions: Somatization, Obsessive–Compulsive, Interpersonal Sensitivity, Depression, Anxiety, Hostility, Phobic-Anxiety, Paranoid Ideation and Psychoticism. Three global indices were calculated: Global Severity Index (GSI), Positive Symptom Total (PST), and Positive Symptom Distress Index (PDI). 2.5.3. Temperament Character Inventory (TCI) The TCI is a personality test assessing different personality traits related to temperament and character (Cloninger, 1994). Temperament refers to the automatic emotional response to experiences

3.1. TD task Fig. 2A shows that the hyperbolic discounting curve for food of obese individuals is significantly steeper than that of normalweight individuals. Conversely, discounting curves for money and discount voucher did not differ between the two groups (Fig. 2B and C). Please, note that the k value for each curve reflects the geometric mean of the group, which corresponds to mean of the logtransformed values. The above impressions were confirmed by statistical analyses. Since the hyperbolic k constants were normally distributed after log-transformation (Kolmogorov–Smirnov d < .17, p > .20 in all cases), and therefore, comparisons were performed using parametric statistical tests. An ANOVA on log-transformed k values with group (obese, normal-weight) as between-subject factor, and reward type (money, food, discount voucher) as within-subject factor was run. This analysis yielded a significant effect of group (F1,44 = 10.8, p = .002; l2p = .20), indicating that obese individuals were overall more prone to choose smaller-immediate reward over larger-delayed ones compared with normal-weight controls ( 1.306 vs. 2.013, p = 0.002). Moreover, there was a significant effect of reward type (F2,88 = 3.5, p = .03; l2p = .07). Newman–Keuls post hoc comparison indicated that overall food was discounted more steeply than money ( 1.341 vs. 1.871, p = .036) and discount voucher ( 1.341 vs. 1.766, p = .047), whereas no significant difference emerged between TD of money and discount voucher (p = .619). Furthermore, a significant group  reward type interaction emerged (F2,88 = 5.4, p < .006; l2p = .11). Newman–Keuls post hoc comparisons showed that obese individuals were more impulsive when making intertemporal food choices as compared to the other group ( 0.5884 vs. 2.094) and the others rewards (all ps < .003), whereas no other significant comparison emerged (all ps > .53) (see Table 2 for detailed ks and SE for each group). These results indicate that, as predicted, obese individuals show increased impulsivity toward edible outcomes as compared to healthy subjects, whereas the discount rate for secondary outcomes is comparable between groups.

Please cite this article in press as: Schiff, S., et al. Impulsivity toward food reward is related to BMI: Evidence from intertemporal choice in obese and normal-weight individuals. Brain and Cognition (2015), http://dx.doi.org/10.1016/j.bandc.2015.10.001

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3.2. TD and BMI Pearson correlations were computed to better investigate the relation between sensitivity for immediate food reward – logarithmic transformed hyperbolic k values – and BMI of all participants included in the study (i.e., both obese and normal-weight individuals). The analysis yielded a positive linear relation between BMI and degree of discounting (r = .52; p < .0001). This result confirms that increased level of impulsivity for immediate amount of food (i.e., impulsivity) corresponds to increased level of BMI. 3.3. Liking, wanting and impulsivity toward food reward We investigated whether obese individuals and healthy controls differed in liking and wanting measures of the food selected for food TD task. The two groups did not differ in any of these ratings (Mann–Whitney U test; U < 518, all ps > 0.08). Spearman correlations were computed to investigate the relationship between impulsivity for immediate food reward – logarithmic transformed hyperbolic k values – and both liking and wanting scores of all participants included in the study (both obese and normal-weight individuals). The analysis yielded a positive linear relation between wanting and the degree of discounting (Spearman R = .34; p < .02); in contrast, no relation was found between liking and impulsivity toward immediate food reward (Spearman R = .001; p = .89). These results suggest that impulsivity toward immediate food reward is related to the degree of motivation (i.e., wanting), but not with the degree of pleasure (i.e., liking) associated with the selected food item. 3.4. Neuropsychological assessment A series of t-tests for independent variables were applied on the scores derived from neuropsychological assessment. The analysis showed that the two groups did not differ in the computerized tests assessing psychomotor speed (i.e., simple and choice RTs), working memory capacity (i.e., Sternberg task), and cognitive control on competing spatial information (i.e., Simon task) (all ps > .05; see Table 3). As well, no difference between groups emerged in paper-and-pencil psychometric tests (TMT-A, TMT-B and FAB; all ps > .05; see Table 3). These results suggest that obese

Table 3 Mean (SD) scores at neuropsychological tests. Neuropsychological tests

Fig. 2. Temporal discounting functions by participant group and type of reward: food (2A), money (2B), and discount voucher (2C). The hyperbolic curves describe the discounting of subjective value (expressed as a proportion of the delayed amount) as a function of time (days). The discounting parameter k reflects the geometric mean of the group (mean of the log-transformed values).

Table 2 Mean (SD) of log-transformed k values. Food Obese Normal-weight

0.53 (0.31) 2.09 (0.26)

Notes: SD = standard deviation.

Money 1.73 (0.2) 2.01 (0.17)

Discount voucher 1.59 (0.23) 1.93 (0.18)

Normal-weight Mean (SD)

Obese Mean (SD)

Paper and pencil tests TMT-A (sec) TMT-B (sec) FAB score

29 (11.4) 51.3 (14.1) 17.1 (1.6)

26 (6) 53 (19) 16.5 (1.7)

Computerized tests Simple RTs – RTs (ms) Simple RTs – Acc (%) Choice RTs – RTs (ms) Choice RTs – Acc (%)

353.1 (76.2) 99.7 (1) 489.3 (110.1) 99.4 (1.6)

348.9 (51.7) 99.4 (1.3) 478.5 (62) 98.4 (2.4)

Sternberg task – RTs (ms) Sternberg task – Acc (%)

1256.4 (279) 86.2 (18.5)

1359.5 (249.4) 91.2 (7.3)

Simon Simon Simon Simon Simon Simon

472.1 (91.6) 518.1 (85) 46 (26.5) 97.4 (2.2) 90.6 (6.6) 6.8 (6.7)

495.3 (71.8) 530.9 (66.5) 35.6 (29.9) 96.6 (2.5) 90.3 (5.1) 6.3 (4.6)

task – Congruent RTs (ms) task – Incongruent RTs (ms) effect – RTs (ms) task – Congruent Acc (%) task – Incongruent Acc (%) effect – Acc (%)

Notes: SD = standard deviation; RT = reaction time; Acc = accuracy expressed in percentage; TMT = Trial Making Test; FAB = Frontal Assessment Battery; sec = seconds; ms = milliseconds.

Please cite this article in press as: Schiff, S., et al. Impulsivity toward food reward is related to BMI: Evidence from intertemporal choice in obese and normal-weight individuals. Brain and Cognition (2015), http://dx.doi.org/10.1016/j.bandc.2015.10.001

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individuals and normal-weight controls did not differ in the overall executive functioning. Spearman correlations did not reveal any significant relations between neuropsychological tests and BMI (all ps > .05). 3.5. Self-report scales A series of t-tests for independent variables were used to evaluate whether obese individuals differ from normal-weight controls in impulsivity traits, personality traits and the presence of psychopathological states. The results did not reveal any significant difference between the two groups in any of the scales of the BIS-11, SCL90-R and TCI (all ps > .05; see Table 4). Spearman correlations did not reveal any significant relation between self-report scale scores and BMI (all ps > .05).

4. Discussion The present study investigated hypothetical intertemporal choice for primary and secondary reward in obese and normalweight individuals. Sensitivity to immediate reward was measured using three TD tasks in which three different types of reward were used (i.e., food, money, discount voucher), separately. Results revealed that obese individuals were more prone to choose immediate smaller reward (i.e., increased discounting of future reward) compared to normalweight controls, and that this tendency was selective for edible reward, thereby indicating that impulsivity for immediate reward was greater in obese individuals compared to normal-weight controls only when food was offered as reward. Conversely, when choosing among amounts of money or discount voucher, obese participants and normal-weight controls did not differ in their discount rate. Additionally, the higher the BMI (taking into account all participants included in the study, i.e., both obese and normalweight individuals), the larger the impulsivity toward food reward, further supporting the idea, already tested in previous literature, that this weight measure is linked to the desire for edible outcome.

Table 4 Mean (SD) scores at psychological questionnaires. Questionnaires

Normal-weight Mean (SD)

Obese Mean (SD)

BIS-11 BIS-11 BIS-11 BIS-11

15.8 19.1 26.7 61.7

(2.7) (3.5) (4.2) (8.6)

15.5 (2.8) 18.2 (3.4) 25.3 (5.9) 60 (10.1)

45.2 50.6 66.9 52.4 74.2 78.6 37.9

(10.4) (15.8) (14) (17.5) (11.9) (16.6) (15.9)

48.4 43.9 59.7 63.5 69.6 76.9 30.5

TCI TCI TCI TCI TCI TCI TCI

Inattentional impulsivity Motor Impulsivity No Planning Impulsivity Total Score

Novelty Seeking Harm Avoidance Reward Dependence Persistence Self-Directedness Cooperativeness Self-Transcendence

SCL90-R SCL90-R SCL90-R SCL90-R SCL90-R SCL90-R SCL90-R SCL90-R SCL90-R SCL90-R SCL90-R SCL90-R

Somatization Obsessive–Compulsive Interpersonal Tolerance Depression Anxiety Hostility Phobic Anxiety Paranoid Ideation Psychoticism Sleep GSI PST

0.6 (0.4) 0.9 (0.6) 0.8 (0.5) 0.6 (0.4) 0.6 (0.3) 0.6 (0.5) 0.2 (0.5) 0.9 (0.5) 0.4 (0.5) 0.7 (0.6) 0.7 (0.3) 47.1 (22.4)

(12.6) (17.5) (20.2) (20.6) (17.6) (12.6) (14.9)

0.6 (0.5) 0.6 (0.6) 0.7 (0.8) 0.6 (0.5) 0.5 (0.5) 0.5 (0.5) 0.2 (03) 0.6 (0.6) 0.4 (0.4) 0.6 (0.8) 0.5 (0.5) 64 (36)

Notes: SD = standard deviation; BIS-11 = Barratt impulsiveness scale; TCI = Temperament Character inventory; SCL90-R = Symptom check list-90-R.

The relation between impulsivity for different types of reward and obesity has been investigated recently (Manwaring et al., 2011; Rasmussen et al., 2010). Overall, our finding of steeper discounting for food than for money in obese individuals is in line with these previous studies. However, there are also several discrepancies. First, we found a positive correlation between BMI and impulsive preference for food, which Rasmussen et al. (2010) failed to detect in their study. This may depend on the wider BMI distribution of our sample: Rasmussen (2010) recruited participants ranging from overweight to moderate obesity (BMI ranging from 29 to 39), whereas our obese participants had a BMI ranging from 30 to 54, and included five severe obese participants with a BMI over 40 kg/m2. Second, Manwaring et al. (2011) found that, while obese women without BED had increased discounting for food reward selectively as compared to normal-weight controls, obese women with BED showed increased impulsivity for immediate reward independently of reward type (i.e., food, money, massage, sedentary activity). By contrast, in the present study we excluded individuals with a diagnosis of BED or other psychopathological symptoms from our sample in order to avoid possible confounding effects of psychopathology over intertemporal decision-making. Even though executive dysfunction, as well as psychopathological symptoms, and personality traits related to behavioral impulsivity have been frequently associated to overeating, weight gain, obesity, and steeper discounting rates for both monetary and food rewards, contrasting findings are present in the extant literature (Davidson & Martin, 2014; Fitzpatrick, Gilbert, & Serpell, 2013; Vainik, Dagher, Dubé, & Fellows, 2013; Davis et al., 2011). For example, in a recent review, Meule (2013) suggested that higher scores of impulsivity in obese individuals, as measured through the BIS scale, are more related with BED, than BMI. In the present study, we excluded participants with previous history of neurological and psychiatric illness, and we further assessed the two samples for: 1. The neuropsychological profile, by including measures of executive functioning; 2. The psychopathological state; 3. Traits of personality, including cognitive and behaviour impulsivity. This procedure allowed us to rule out the possibility that these factors, known to influence discount rates, would affect our findings. Since no differences between groups were observer when these important variables where considered, it is reasonable to think that our finding of impulsivity specifically directed toward immediate food reward is related to obesity and BMI, and should not be related to other variables of interest. Finally, statistical difference between our study and previous ones (Manwaring et al., 2011; Rasmussen et al., 2010) needs to be considered. In those studies, separate analysis for different rewards were carried out, whereas in the present one we made a direct comparison between groups and reward types (i.e., money, food, discount vouchers) with a unique analysis by adopting comparable tasks, which enabled us to discuss the interaction between groups and reward types. As final remark, we are aware that our sample mainly includes women. So far, a link between TD and overweight/obesity has been reported in women especially, and several previous studies investigating this issue mainly recruited female participants (e.g., Appelhans et al., 2011; Davis et al., 2010; Manwaring et al., 2011; Rasmussen et al., 2010; Weller et al., 2008). Moreover, gender differences have been found also in the neural response to food-related images in women, whereby they behaved more impulsively toward food-cues (e.g., Frank et al., 2010; Wang et al., 2009). Thus, further investigation is needed in the future to replicate the present findings in men as well. Overall, present study corroborates the idea that in obese individuals, impulsivity toward immediate reward, as measured through intertemporal choice, is specific for food, even when neu

Please cite this article in press as: Schiff, S., et al. Impulsivity toward food reward is related to BMI: Evidence from intertemporal choice in obese and normal-weight individuals. Brain and Cognition (2015), http://dx.doi.org/10.1016/j.bandc.2015.10.001

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ropsychological/psychopathological conditions and traits of personality related to general impulsivity were excluded. Neuroimaging studies highlighted that obese individuals manifest alteration within the brain reward system. In particular, a negative correlation between the number of dopamine (DA) DRD2 receptors within the striatum and BMI has been described (Volkow, Wang, & Baler, 2011; Wang et al., 2001). Furthermore, the decreased availability in striatal DRD2 receptors is associated with reduced metabolism in prefrontal regions related to inhibitory control and executive functions, such as the dorsolateral prefrontal cortex, the anterior cingulate cortex, and the medial orbitofrontal cortex. The dopaminergic system is involved in the formation of stimulusreward associations and in the representation of reward value. Thus, the correlation between BMI and impulsivity toward food reward seems to be a behavioral counterpart of the striatal DRD2 receptors reduction previously observed in obese individuals (Volkow et al., 2008; Wang et al., 2001). In addition, the finding that obese individuals, compared in normal-weight controls, show higher discount rate for food reward, but not for money or discount vouchers is consistent with the incentive salience theory (Berridge, 2007). This theory suggests a link between the repeated stimulation with particular rewarding stimuli (i.e., palatable and high caloric foods) and the formation of stable stimulus-reward associations, even if maladaptive. Thus, the habits of consuming food for pleasure may reinforce its incentive salience, thereby encouraging the frequency of approach behavior toward this kind of stimuli. This in turn would easily justify the development and maintenance of obesity, even in absence of particular psychopatho logical/neuropsychological condition or personality traits related to impulsivity. The altered stimulus-specific reward association in obese individuals might have determined the increased temporal discounting for future edible outcome in a stimulus-specific way (Volkow et al., 2008, 2011). This would explain why our obese participants failed to resist to the urge of choosing (if not consuming) immediate amounts of food, but not the other rewards adopted in the present study (i.e., money and discount voucher). This idea is supported also by neuropsychological assessment, including tests for executive functions and cognitive control, which failed to reveal any difference between obese participants and the normal-weight group. The deficiency in striatal DRD2 receptors reported in obese people (Volkow et al., 2008) might have apparently reduced sensitivity to rewards, due to the predominant roles of DA in assigning incentive salience to reward (e.g., Berridge, 2007, 2012; Schultz, 2010). More specifically, this DA reduction would result in a reduced sensitivity to relative differences in the value of food rewards (Goldstein et al., 2006). Such ‘flattening’ of the perceived reinforcer gradient may underlie biased attention or over-valuation of immediate rewards and abnormal discounting of larger but delayed food rewards, thus inducing pathological eating behavior as a means to compensate for decreased activation of reward network (Goldstein & Volkow, 2011; Volkow et al., 2008, 2011; Wang et al., 2001). 4.1. Summary and future implications To summarize, we found that obese individuals discount future amounts of hypothetical food reward more steeply than healthy controls, whereas no difference between groups emerged when the reward at stake was hypothetical money or discount voucher. These results emerged (i) in light of no difference between groups on the psychopathological, neuropsychological, and personality profile, and (ii) in the absence of any difference in the degree of desire (i.e., wanting measure) for the chosen food. Thus, the difference emerged between the two groups in the degree of impulsivity toward immediate food reward seems to be ascribed to the difference in the BMI of our participants.

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Recently, neural correlates of higher behavioral impulse control (i.e., reduced impulsivity) toward immediate food rewards has been found to predict weight loss and weight regain after a short-term diet in obese individuals, corroborating the idea that the evaluation of decision-making toward food-related reward might be useful to monitor the outcome of intervention (i.e., dietary, psychological, pharmacological, or surgical) oriented to manage weight in obese individuals (Weygandt et al., 2013, 2015). Moreover, several imagery techniques, such as episodic future thinking and mindful eating, were successfully adopted to increase self-control and reduce impulsivity toward immediate reward in obese individuals (Daniel, Stanton, & Epstein, 2013; Hendrickson & Rasmussen, 2013). Interestingly, one of these studies demonstrated that when the training focused on food and healthy eating, impulsivity reduction became food-specific (Hendrickson & Rasmussen, 2013). Therefore, TD tasks, which have already been already successfully used as measure of food sensitivity in paradigms aimed at reducing impulsivity (e.g., Sellitto & di Pellegrino, 2014), might be adopted in future research or clinical trials in obese individuals in order to measure the effectiveness of weight-management interventions in reducing sensitivity for edible stimuli. Acknowledgments The authors thank Debora Vego Scocco, Maria De Salvo and Gina Boffo for helping during participants’ recruitment and data collection. S.S. and G.D. designed the study. S.S. and T.N. collected the data. S.S., M.S., G.D. and G.T. wrote the paper. All authors read and approved the paper. The study was carried on under the auspices of CIRMANMEC – University of Padova, Italy. The authors have no competing interests. References Ainslie, G. W. (1974). Impulse control in pigeons. Journal of the Experimental Analysis of Behavior, 2, 485–489. Amodio, P., Campagna, F., Olianas, S., Iannizzi, P., Mapelli, D., Penzo, M., ... Gatta, A. (2008). Detection of minimal hepatic encephalopathy: Normalization and optimization of the Psychometric Hepatic Encephalopathy Score. A neuropsychological and quantified EEG study. Journal of Hepatology, 49, 346–353. American Psychiatric Association (2000). Diagnostic and statistical manual of mental disorders, Fourth Edition text revised: DSM-IV-TR. Washington, D.C. Appelhans, B. M., Pagotom, S. L., Schneider, K. L., Whited, M. C., & Liebman, R. (2011). Inhibiting food reward: Delay discounting, food reward sensitivity, and palatable food intake in overweight and obese women. Obesity, 19, 2175–2182. Appollonio, I., Leone, M., Isella, V., Piamarta, F., Consoli, T., Villa, M. L., ... Nichelli, P. (2005). The Frontal Assessment Battery (FAB): Normative values in an Italian population sample. Neurological Sciences, 26, 108–116. Berkowitz, R. I., & Fabricatore, A. N. (2011). Obesity, psychiatric status, and psychiatric medications. Psychiatric Clinics of North America, 34, 747–764. Berridge, K. C. (2007). The debate over dopamine’s role in reward: The case for incentive salience. Psychopharmacology (Berl), 191, 391–431. Berridge, K. C. (2009). Wanting and liking: Observations from the Neuroscience and Psychology Laboratory. Inquiry, 52, 378. Berridge, K. C. (2012). From prediction error to incentive salience: Mesolimbic computation of reward motivation. European Journal of Neuroscience, 35, 1124–1143. Berridge, K. C., & Robinson, T. E. (1998). What is the role of dopamine in reward: Hedonic impact, reward learning, or incentive salience? Brain Research Reviews, 28, 309–369. Bickel, W. K., Jarmolowicz, D. P., Mueller, E. T., Koffarnus, M. N., & Gatchalianm, K. M. (2012). Excessive discounting of delayed reinforcers as a trans-disease process contributing to addiction and other disease-related vulnerabilities: Emerging evidence. Pharmacology & Therapeutics, 134, 287–297. Bickel, W. K., Pitcock, J. A., Yi, R., & Angtuaco, E. J. (2009). Congruence of BOLD response across intertemporal choice conditions: Fictive and real money gains and losses. Journal of Neuroscience, 29, 8839–8846. Cardinal, R. N., Pennicott, D. R., Sugathapala, C. L., Robbins, T. W., & Everitt, B. J. (2001). Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science, 292, 2499–2501. Carpiniello, B., Pinna, F., Pillai, G., Nonnoi, V., Pisano, E., Corrias, S., ... Loviselli, A. (2009). Obesity and psychopathology. A study of psychiatric comorbidity among patients attending a specialist obesity unit. Epidemiologia e psichiatria sociale, 18, 119–127.

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Please cite this article in press as: Schiff, S., et al. Impulsivity toward food reward is related to BMI: Evidence from intertemporal choice in obese and normal-weight individuals. Brain and Cognition (2015), http://dx.doi.org/10.1016/j.bandc.2015.10.001