Visual attentional bias for food in adolescents with binge-eating disorder
Introduction
Unlike previous research in adult binge-eating disorder (BED) indicating that adults with BED exhibit altered and clinically relevant attentional processing of food cues (Kessler et al., 2016), the precise nature of attentional processes in adolescent BED is yet to be determined. Elucidating these processes in adolescent BED is of particular importance because attentional biases for food, i.e. the phenomenon that food cues hold and grab selective attention in preference over other cues, are suggested to interfere with response inhibition and goal-focused behavior (Bunge et al., 2009), and may thus contribute to disinhibited and reward-driven eating behaviors in adolescent BED. The present study aimed therefore to identify characteristics of visual attention processing of food cues in adolescents with BED using an eye-tracking and visual search task.
Binge-eating disorder (BED), recently established as an eating disorder on its own (American Psychiatric Association; APA, 2013), is characterized by recurrent binge eating, defined as a loss of control over eating an unambiguously large amount of food that occurs without regular use of inappropriate compensatory behavior. Adolescents with BED show increased general and eating-disorder psychopathology (Swanson et al., 2011, Goossens et al., 2009, Goldschmidt et al., 2008) and are likely to be obese (Shomaker et al., 2010). Similar to anorexia nervosa (AN) and bulimia nervosa (BN), BED develops over adolescence, presenting the most prevalent eating disorder in youth (Swanson et al., 2011). Despite its high prevalence, factors concerning its etiology and maintenance are largely unclear.
Following evidence on the causal role of disorder-specific attentional biases regarding onset of a range of mental disorders, such as emotional (Mathews and MacLeod, 2005) and substance-use disorders (Field and Cox, 2008) that show high comorbidity with adolescent BED (Swanson et al., 2011), recent research has begun to examine attentional biases to food in BED (Kessler et al., 2016). Although few experimental evidence is currently available, experimental findings indicated that adults with BED showed delayed disengagement from food and body stimuli at long stimulus presentation durations (Schag et al., 2013, Popien et al., 2015, Svaldi et al., 2011) and rapid orienting to food stimuli at pre-attentive presentation durations (Schmitz et al., 2014, Schmitz et al., 2015, Svaldi et al., 2015), depending on paradigms used, including indirect and direct measures. A direct and presumably the most precise approach into visual attentional biases is continuous recording of participants’ eye movements, in order to assess overt visual attention. Generally, eye-tracking paradigms involve long stimulus presentation durations (several seconds) in order to facilitate multiple shifts of attention while participants are watching pairings of food and non-food stimuli or more complex visual scenes. In adult BED, eye-tracking revealed slower disengagement from food and body-related information as reflected by longer gaze duration on food stimuli and ugly body parts, respectively, compared to controls (Popien et al., 2015, Schag et al., 2013, Svaldi et al., 2011), while there was mixed evidence for an initial orientation bias to food cues (Popien et al., 2015, Schag et al., 2013).
Another paradigmatic approach infers visual attentional biases from participants’ response latencies during computer tasks, such as dot-probe, attentional cuing or lexical identification tasks (Schmitz et al., 2014, Schmitz et al., 2015, Shank et al., 2015, Svaldi et al., 2015). Typically, these reaction time-based tasks involve short stimulus presentation durations and instructions to respond as fast and correct as possible. For example, Schmitz et al. (2014) presented a pictorial (food or neutral) cue on the left or right side of the computer screen for 100 ms, followed by a visual probe that appeared in the previous location of either the food or neutral cue. Adults with BED were found to initially attend to food cues as indexed by shorter response latencies when the probe replaced the food compared to the neutral cue (Schmitz et al., 2014). However, the authors did not find impaired disengagement as indicated by slower responses when the probe replaced the neutral compared to the food cue (Schmitz et al., 2014, Schmitz et al., 2015). The only evidence in youth with loss of control eating, a precursor of BED (Hilbert and Brauhardt, 2014), showed neither facilitated attention to nor slowed disengagement from food stimuli compared to controls (Shank et al., 2015).
Importantly, reaction time-based measures tap into different components of visual attention compared to eye-tracking paradigms. Due to very short stimulus presentation times and performance orientation, reaction time measures are suggested to assess earlier stages of attention, and are likely to assess covert attention. A second concern is the lack of a direct response conflict of food and non-food stimuli (Mogg and Bradley, 1998), leaving ambiguity about precise mechanisms of selective attention. In this context, visual search tasks allow to specifically examine processes related to detecting disorder-specific targets in the presence of attention-competing stimuli (Weierich et al., 2008). According to visual search tasks that required participants to indicate whether an array of stimuli belong to the same or to a different category, individuals with AN and BN showed greater difficulties to disengage from high-calorie food distractors, but did not show speeded detection of these stimuli (Smeets et al., 2008). In BED, visual search tasks have not yet been conducted.
Overall, the results provided support for the relevance of cognitive-motivational mechanisms in visual attention processing of food cues in adult BED as predicted by incentive sensitization theories of addictive disorders (Robinson and Berridge, 2001, Field et al., 2009). These models posit that a food stimulus “grabs attention, becomes attractive and ‘wanted,’ and thus guides behavior to the incentive” (p. 261, Robinson and Berridge, 1993) as a consequence of conditioned dopamine responses to repeated exposure to rewarding food and subjective craving (Robinson and Berridge, 2001). In contrast to other eating disorders, particularly AN, that were found to exhibit an attentional approach-avoidance strategy, i.e. rapid orienting to, but facilitated disengagement from food (Brooks et al., 2011), adults with BED were thus characterized by an attentional approach-approach pattern. Based on evidence that attentional biases for food stimuli were positively associated with current craving (Werthmann et al., 2011, Meule et al., 2014, Smeets et al., 2009), there is reason to suggest that individuals with BED show greater attentional biases to foods that generally elicit high levels of craving, for example, binge food or foods that have high personal valence, respectively.
Regarding adolescent BED, findings from adult studies have been limited in elucidating attentional processes because the duration of BED that is likely to be longer in adult than youth samples may have an impact on attentional biases (Loeber et al., 2009). The present study aimed to close this gap through comprehensively evaluating attentional orienting and disengagement processes in a sample of adolescents with BED. Therefore, a free exploration paradigm was used to record initial gaze direction and overall gaze duration on pairings of food and non-food stimuli. A visual search task was designed to assess visual detection processes in BED by presenting multiple attention-competing stimuli. It was hypothesized that adolescents with BED would show initial orienting to food stimuli as indexed by a gaze direction bias on food stimuli (eye-tracking) and detection bias for food targets (visual search task) as well as delayed disengagement from food stimuli as indicated by an overall gaze duration bias for food stimuli (eye-tracking task) compared to controls. Finally, exploratory analyses addressed whether attentional biases for food would be affected by participants’ valence rating of food stimuli and whether bias scores would show associations with eating-disorder psychopathology and hunger ratings.
Section snippets
Participants
A total of 50 adolescents (n = 25 with BED, n = 25 control group, CG) participated in both an eye-tracking and visual search task. Youth with BED were recruited at the time of admission to outpatient cognitive-behavioral therapy for adolescents with BED (Hilbert, 2013). The BED group fulfilled the DSM (American Psychiatric Association, 1994, American Psychiatric Association, 2013) diagnostic criteria for BED adapted to age, i.e. objectively and subjectively large binge-eating episodes were
Gaze direction bias
Both the BED group and CG did not differ in their initial gaze direction bias in trials presenting food stimuli in general (p = 0.369) and trials including attractive (p = 0.359) and unattractive food stimuli only (p = 0.241), see Table 2. Additional one-sample t tests indicated that direction bias scores did not significantly differ from a test score of 50% for each group (BED, t(23) = −1.19, p = 0.852; CG, t(23) = 0.23, p = 0.821).
Gaze duration bias
Repeated measures ANOVA of overall gaze duration bias scores
Discussion
The primary objective of this study was to provide evidence for the presence of visual attentional biases for food in adolescents with BED, as they have been found in adult BED (Kessler et al., 2016), and to specify these biases in terms of orienting and disengagement processes. As hypothesized, eye-tracking data indicated an overall delayed disengagement from food stimuli in adolescents with BED compared to controls, but no initial orienting bias for food stimuli. Importantly, we provided
Role of the funding source
The funding source (German Federal Ministry of Education and Research) was not involved in the study design, in the collection, analysis and interpretation of data, in the writing of the report, and in the decision to submit the article for publication.
Contributors
Conceived and designed the experiments: PL AH. Performed the experiments: RS. Analyzed the data: RS PL. Involved in recruitment: RS RK AT. Wrote the paper: RS PL RK AT AH. All authors have approved the final manuscript.
Conflict of interest
None of the authors declared any biomedical financial interests or potential conflicts of interest.
Acknowledgments
This research was supported by the German Federal Ministry of Education and Research (BMBF) (grant number 01EO1001). We thank Joseph Krummenacher, Ph.D. and Claudia Ruf, M.Sc. for their support in the preparation of the eye-tracking paradigm.
The results of the study have been presented as a poster at the 21st Annual Meeting of the Eating Disorder Research Society (September 17–19, 2015), in Taormina, Sicily.
References (63)
- et al.
A pilot study evaluating a one-session attention modification training to decrease overeating in obese children
Appetite
(2014) - et al.
A systematic review and meta-analysis of cognitive bias to food stimuli in people with disordered eating behaviour
Clin. Psychol. Rev.
(2011) - et al.
Eating disorder pathology among overweight treatment-seeking youth: clinical correlates and cross-sectional risk modeling
Behav. Res. Ther.
(2007) - et al.
Slow rates of habituation predict greater zBMI gains over 12 months in lean children
Eat. Behav.
(2011) - et al.
Attentional bias in addictive behaviors: a review of its development, causes, and consequences
Drug Alcohol Depend.
(2008) - et al.
The relationship between eating-related individual differences and visual attention to foods high in added fat and sugar
Eat. Behav.
(2012) - et al.
Responsivity to food stimuli in obese and lean binge eaters using functional MRI
Appetite
(2006) - et al.
Loss of control eating and psychological maintenance in children: an ecological momentary assessment study
Behav. Res. Ther.
(2009) - et al.
Eating behavior and familial interactions of children with loss of control eating: a laboratory test meal study
Am. J. Clin. Nutr.
(2010) - et al.
Components of attentional bias for food cues among restrained eaters
Appetite
(2010)
The neurobiological basis of binge-eating disorder
Neurosci. Biobehav. Rev.
Impulsive reactions to food-cues predict subsequent food craving
Eat. Behav.
A cognitive-motivational analysis of anxiety
Behav. Res. Ther.
All I saw was the cake. Hunger effects on attentional capture by visual food cues
Appetite
Eye gaze tracking reveals heightened attention to food in adults with binge eating when viewing images of real-world scenes
Appetite
The neural basis of drug craving: an incentive-sensitization theory of addiction
Brain Res. Rev.
Binge-eating disorder: reward sensitivity and brain activation to images of food
Biol. Psychiatry
Attentional bias for food cues in binge eating disorder
Appetite
Gating of attention towards food stimuli in binge eating disorder
Appetite
Attentional bias to food cues in youth with loss of control eating
Appetite
Attentional bias for body and food in eating disorders: increased distraction, speeded detection, or both?
Behav. Res. Ther.
Experimentally induced chocolate craving leads to an attentional bias in increased distraction but not in speeded detection
Appetite
Information processing of food pictures in binge eating disorder
Appetite.
Attentional avoidance of high-fat food in unsuccessful dieters
J. Behav. Ther. Exp. Psychiatry
Food selection and intake of obese women with binge-eating disorder
Am. J. Clin. Nutr.
Diagnostic and Statistical Manual of Mental Disorders
Diagnostic and Statistical Manual of Mental Disorders
Brain changes underlying the development of cognitive control and reasoning
Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: the BIS/BAS scales
J. Pers. Soc. Psychol.
Statistical Power Analysis for the Behavioral Sciences
Neural mechanisms of selective visual attention
Annu. Rev. Neurosci.
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