Food cue-elicited brain potentials in obese and healthy-weight individuals
Introduction
In western societies, health organizations raise the alarm because of increasing prevalence rates of overweight (Body Mass Index [BMI] ≥ 25 kg/m2) and obesity (BMI ≥ 30 kg/m2) in the general population. For example, in the Netherlands – where the present study was conducted – an epidemiological study during the period 1998–2001 revealed that 40 to 50% of adults between the ages of 20 and 70 years are overweight, while circa 10% of them are obese (Visscher, Viet, Kroesbergen, & Seidell, 2006). Similar research, conducted between 2002 and 2004, led to the conclusion that about 15% of the Dutch children between 4 and 15 years are overweight, whereas 3% of them can be labelled as obese (van den Hurk et al., 2006). These figures have even doubled since the 1980s, and are expected to double once more in the upcoming two decades if no interventions are undertaken (Bemelmans et al., 2004, Schokker et al., 2007).
In essence, overweight is the result of a chronic imbalance between energy intake and energy expenditure: more kilocalories are ingested than necessary for the body's metabolism. Although this imbalance is the consequence of a complex interplay between genetic–biological and environmental–behavioral factors, it is the environment, promoting an unhealthy lifestyle and ‘obesogenic’ behavior, that is held largely responsible for the dramatic worldwide increase in the prevalence of overweight (Hill and Peters, 1998, Hill et al., 2003). More precisely, the abundant availability of rewarding, thus high-caloric and palatable, food is emphasized to contribute to overeating behavior (Hill and Peters, 1998, Speakman, 2007, Volkow and Wise, 2005). It has been suggested that there are individual differences in the sensitivity and reactivity to the rewarding properties of environmental food cues (Beaver et al., 2006, Franken and Muris, 2005). In sensitive individuals, the mere exposure to palatable food might induce excessive craving and a tendency to indulge in overeating behavior, even in the absence of physiological hunger or nutritional deficits (Berridge, 2007, Jansen, 1998, Wardle, 1990).
Individual differences in food cue responsiveness are assumed to depend considerably on classical conditioning mechanisms (Jansen, 1998, Wardle, 1990). Conditioning models for excessive eating propose that actual food cues and classically conditioned (external as well as internal) eating-related stimuli may become strong predictors for food intake and anticipatorily elicit physiological responses, which are associated with craving. Preliminary evidence suggests that conditioned food cue responsiveness is stronger in obese individuals than in normal-weight persons. For example, Jansen et al. (2003) investigated cue-elicited craving and overeating in obese and normal-weight children. After being exposed to the smell of tasty food or to the taste of an appetizing preload, obese children demonstrated a significantly increased food intake as compared to a control condition without food confrontation, whereas the food intake of normal-weight children generally decreased in the food exposure conditions.
Conditioned cue reactivity models for overeating behaviors have their roots in classical addiction theories, in which conditioned drug cue reactivity and drug craving are believed to contribute considerably to the development and maintenance of addictive disorders and the well-known tendency to relapse when abstinent (Franken, 2003, O'Brien et al., 1998, Robinson and Berridge, 1993). Moreover, overeating clearly exhibits other features of addictive behavior: it is characterized by the impulsive seeking and intake of a rewarding substance in spite of the negative health and psychosocial consequences, and attempts to control the behavior frequently result in relapse to initial overeating and intake of high-caloric food (Kramer et al., 1989, Stalonas et al., 1984, Wadden and Frey, 1997). In addition, similarly to addiction, empirical findings suggest that the overeating behavior of (at least a subgroup of) obese individuals might be the result of a substantially enhanced motivation for food, which may have its origins in the aberrant functioning of reward-related brain processes (Volkow et al., 2002, Wang et al., 2001).
In substance dependent individuals, electrophysiological research, using cue exposure paradigms, has yielded robust findings concerning the processing of drug-related information. When confronted with drug-related pictures, long-latency waves, such as the P3 and Late Positive Potential (LPP), in the event-related potential (ERP) pattern of addicted individuals were found to be significantly increased in centro-parietal regions as compared to non-addicted control subjects, suggesting an enhanced cortical processing of these stimuli (Herrmann et al., 2000, Herrmann et al., 2001, Littel and Franken, 2007, Lubman et al., 2007, Warren and McDonough, 1999). Long-latency ERPs are thought to reflect the allocation of attention and cognitive effort (Kok, 1997). It is assumed that more cognitive resources are allocated to motivationally salient (positive and negative) stimuli. In emotional contexts, there is general agreement that long-latency ERP amplitudes are modulated by the motivational salience of cognitively processed information (Schupp et al., 2000). A sustained selective processing bias, reflecting the activation of the brain's motivation system, would induce an appropriate behavioral (approach or avoidance) response to motivational salient stimuli (Cuthbert et al., 2000, Franken et al., 2003). Interestingly, in addiction-related ERP-studies the amplitude of LPPs appears to be positively correlated with self-reported drug craving, which supports the idea that LPP amplitude reflects motivational tendencies (Franken et al., 2004, Franken et al., 2003, Lubman et al., 2007, van de Laar et al., 2004).
The present study addresses the processing of food cues in normal-weight and obese individuals. The aims of the present study are twofold. The first aim is to investigate whether palatable food-related stimuli result in enhanced processing as compared to non-food stimuli. We expected larger P3 and LPP amplitudes when individuals are exposed to food stimuli as compared to control stimuli (i.e., office items). The second aim was to examine whether obese individuals display enhanced processing of food-related information as compared to normal-weight controls. In other words, this study investigated whether there is a general processing bias for food-related information and whether this bias is enhanced in obese individuals as compared to normal-weight individuals. If obesity indeed is the result of an abnormally enhanced motivation for food, which is characterized by an excessive reactivity towards food cues, larger P3 and LPP amplitudes for food cues would be expected in the obese group. Furthermore, as LPP and P3 amplitudes reflect motivational tendencies, it can be expected that these measures correlate positively with self-report measures of food craving and hunger.
So far, few studies have addressed cortical processing of food information by means of ERPs. These studies were primarily concerned with the influence of hunger and satiety on food-related information processing (e.g., Carretié et al., 2000, Hachl et al., 2003, Plihal et al., 2001). However, for a number of reasons, the results of these studies are rather difficult to interpret when it comes to the mere processing of food stimuli. First of all, actual processing of stimuli was influenced by other cognitive tasks, which the participants had to perform simultaneously, such as stimulus identification or stimulus matching. Second, stimuli were not shown explicitly to participants (as is the case in real world), but presented as words or in a subliminal or deformed way. Third, the focus of these studies was the influence of food deprivation on brain activity in general. With this in mind, the present study adopts a more straightforward approach: participants are passively exposed to pictures of palatable foods as well as neutral control pictures while recording their EEG activity. Further, we not only examine the relation between hunger and ERPs, but are also interested in the influence of food craving on the processing of food-related information, because this process is thought to play a primary role in the origins of overeating behavior. Exploratively, we will also investigate the hemispheric distribution of ERPs: appetitive food cues are expected to predominantly activate left-hemispheric brain areas, since electro-cortical activation in the left hemisphere is believed to be associated with approach behavior towards emotionally pleasant stimuli (Davidson et al., 1990, Sutton and Davidson, 2000).
Section snippets
Participants
Via advertisements, healthy obese (BMI ≥ 30 kg/m2) and healthy normal-weight (BMI 20–25 kg/m2) men and women between the ages of 18 and 50 years were approached to volunteer in a study concerning brain activity and body weight. Participants were screened during a telephone interview and were excluded from the study for the following reasons: (1) presence of a psychiatric or physical illness within the past four weeks; (2) current use of any medication that might influence eating behavior, body
Self-report measures
No between-group difference was found with regard to the elapsed time since last eaten (t = 1.18, p > .05). Mean hunger and food craving scores for obese and normal-weight participants are displayed in Table 1. Main time effects were found for food craving, F(1,37) = 31.66, p < .001, as well as hunger scores, F(1,38) = 17.31, p < .001. This result indicates that participants generally reported significantly more food craving and hunger at posttest (after the food picture exposure) as compared to pretest.
Discussion
This study investigated brain processing of food-related information in a passive exposure paradigm by means of event-related potentials (ERPs). In line with our expectations, significant larger P3 and LPP amplitudes were found for food stimuli as compared to office stimuli, which were particularly observed at posterior and central electrode clusters. Emotion and addiction researchers agree on the notion that long-latency ERP amplitudes at centro-parietal brain sites are modulated by the
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