Research reportDifferences in attention to food and food intake between overweight/obese and normal-weight females under conditions of hunger and satiety
Introduction
Evidence from neuroimaging studies suggests that an altered functioning of the brain reward system plays a similar important role in the etiology and maintenance of addiction and obesity (Volkow and Wise, 2005, Wang et al., 2001). One addiction theory that seems particularly applicable to obesity is the incentive sensitization theory (Robinson & Berridge, 1993). In short, this theory assumes that a sensitization of the dopaminergic reward system serves to increase the salience of reward-related cues (such as drugs or food) in the environment and to make them more “attention-grabbing”, thereby promoting craving and intake of the rewarding substance. Individuals with a high food cue-responsiveness (attentional bias, craving) are assumed to be more vulnerable to overeat and to become obese in the food-rich environment of today (Berridge, 2009, Polivy et al., 2008).
Starting from an incentive sensitization model of obesity, the present study primarily examines differences in the attentional processing of food-related stimuli between overweight/obese and normal-weight, hungry or satiated women. Whereas there is ample evidence that food-related attention is modulated by hunger and satiety in normal-weight individuals (Channon and Hayward, 1990, Lavy and van den Hout, 1993, Mogg et al., 1998, Placanica et al., 2001, Stockburger et al., 2008, Stockburger et al., 2009), surprisingly few studies have investigated this issue in overweight/obese persons, and even this evidence is inconclusive. For instance, Braet and Crombez (2003) found Stroop interference to food-related words in obese children, which was absent in their normal-weight peers. Using an imbedded word task, Soetens and Braet (2007), on the other hand, observed no preferential attentional processing of food-related words relative to neutral words, neither in normal-weight nor in overweight adolescents. Finally, Nijs, Franken, and Muris (2008) used event-related potentials (ERPs; i.e., stimulus-triggered electroencephalographic [EEG] brain activity) as indices of attention allocation, and found evidence for an enhanced attention towards food-related pictures relative to neutral pictures, in both obese and normal-weight adults, with no difference between both groups. In these three studies, participants were food-deprived for 2–3 h, and the modulation of food-related attention by hunger and satiety was not examined. In a recent study by Castellanos et al. (2009), a visual probe task was combined with the monitoring of eye movements to examine food-related attention in obese and normal-weight individuals under conditions of hunger and satiety. No between-group differences were found with regard to reaction time measures. However, obese individuals were found to demonstrate a similar bias in the initial orientation and maintenance of attention to food pictures, as assessed by means of gaze direction and duration, during conditions of hunger and satiety, whereas in normal-weight participants the food-related bias in attentional orientation and maintenance was clearly reduced (or even no longer existent) in a satiety as compared to a hunger state.
The above-mentioned studies illustrate some of the challenges attention research is dealing with, which may be the reason for the mixed results (for an overview, see e.g., Field & Cox, 2008). To study attentional processes, various behavioral and physiological, direct and indirect paradigms exist, which may measure different aspects of attention. In addition, results seem to depend on the type of stimuli, the duration of the stimulus presentation, and the choice of control stimuli. In the present study, different measures of attention, all including food-related and neutral control pictures, are employed. As direct behavioral measure, an eye-tracking procedure was applied: the eye movements of participants were directly monitored while they were exposed to pairs of food-related and neutral control pictures. By analogy with the study of Castellanos et al. (2009), a measure of gaze direction was employed as index of the automatic orientation of attention, and a measure of gaze duration was chosen as index of maintained attention. As an indirect behavioral measure, a visual probe task was chosen. During a visual probe task (Posner, Snyder, & Davidson, 1980), participants are exposed to pairs of target and neutral pictures, and requested to respond as fast as possible to a visual probe that appears on the location of one of the pictures after they disappear. Reaction times to the probes are assumed to be faster if the probe is located in the visual field where the attention is already drawn to, thereby reflecting attentional bias. In the paradigm as used in the present study, picture pairs were randomly presented for a short duration (100 ms) or a longer duration (500 ms), respectively reflecting the initial orientation of attention and maintained attention (Field & Cox, 2008). Finally, as an electrophysiological measure of attention, EEG was recorded during the exposure to pictures of food and neutral items to determine the P300 ERP. The P300 is a positive peak that appears at circa 300 ms after the presentation of a stimulus (Picton, 1992, Polich and Kok, 1995). The P300 amplitude reflects electrophysiological activity related to conscious attention allocation (Cuthbert, Schupp, Bradley, Birbaumer, & Lang, 2000), and is the most widely explored ERP index in selective attention paradigms (Olofsson et al., 2008, Schupp et al., 2006).
Besides studying differences in food-related attention between overweight/obese and normal-weight women, the present study also aims to investigate the association between attention to food and direct measures of food motivation, i.e., subjective hunger level and food intake. The idea that the desire to eat and food intake are triggered by the exposure to external food cues is not new (Herman and Polivy, 2008, Sobik et al., 2005). In the 1960s, Schachter already proposed his externality theory, positing that the food intake of obese individuals was more determined by salient external food cues than the food intake of normal-weight individuals (Schachter, 1971). Support for this perspective has been provided by, for instance, Jansen et al. (2003), who demonstrated that overweight children had a stronger desire for food and ate more than normal-weight children after exposure to snack foods. Nowadays, with the growing obesity epidemic, which seems strongly related to the increased availability of rewarding food in Westernized environments, Schachter's theory seems to revive, forming the basis of new models, which integrate elements of incentive salience with new knowledge regarding the neural regulation of eating behavior and body weight.
To our knowledge, this is the first study that combines the elements of food-related attention, hunger/satiety state, body weight, subjective hunger levels, and also food intake, within one and the same study, in order to examine the relations among these variables. In line with an incentive sensitization model, the central hypotheses are as follows. First, it was expected that the attentional bias to food cues, subjective hunger level, and food intake would be enhanced during hunger as compared to a satiety state in both overweight/obese and normal-weight participants. Second, it was expected that overweight/obese individuals would demonstrate an enhanced attentional bias towards food stimuli, report more hunger, and eat more during a bogus taste task as compared to normal-weight participants. Third, positive correlations were expected between measures of food-related attentional bias, hunger levels, and food intake.
Rather than directly with obesity, enhanced food cue-reactivity has been more often associated with dietary restraint (Green and Rogers, 1993, Polivy et al., 2005, Polivy et al., 2008, Tapper et al., 2008) and external eating (Brignell et al., 2009, Johansson et al., 2004, Newman et al., 2008, Nijs et al., in press). For this reason, an additional purpose of the study was to explore the associations between various attention-related measures, indices of food motivation, and (over)eating styles (i.e., dietary restraint, emotional eating, and external eating) in both weight groups. In line with an incentive sensitization model of obesity, differences between overweight/obese and normal-weight participants were particularly expected with regard to the general tendency to (over)eat in response to food-related cues, i.e., external eating.
Section snippets
Participants
Because gender differences have been reported with regard to food craving and (over)eating styles (e.g., Braet et al., 2008, Burton et al., 2007), only female participants were recruited to participate in the present study. Through campus flyers and e-mail, female students of Erasmus University Rotterdam were informed about the present study and asked to contact us by telephone if they were interested in participation. A short telephonic screening interview was conducted during which students
Manipulation check
As can be observed in Table 1, there was an immediate significant decrease in hunger reports of participants of the satiety condition after milk shake consumption (VAS1 vs. VAS2), F(1,31) = 2.04, p < .001. No significant time × weight group interaction was observed, so the satiety effect appeared to be similar for normal-weight and overweight/obese women.
When comparing VAS1 with VAS3 hunger scores, a significant time × condition interaction was found, F(1,62) = 117.10, p < .001. Post-hoc t-tests revealed
Discussion
The main objective of the present study was to examine differences in attention to food pictures between normal-weight and overweight/obese, food-deprived and satiated females. Various attention-related tasks unanimously demonstrated that a bias in the oriented and maintained attention to food pictures was present in all participants, irrespective of weight group or hunger/satiety condition. From an evolutionary perspective, this could have been expected: a selective detection of (high-caloric)
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