Abstract
Background
Executive functioning (EF) difficulties may be associated with problems regulating eating behaviors. Few studies have evaluated this question in youth using diverse measures of EF or objective measures of energy intake.
Methods
The current study used neuropsychological tasks and a laboratory test meal to evaluate the links between EF and youth’s disinhibited eating patterns. Two-hundred-five non-treatment seeking youth (M age=13.1±2.8y; M BMIz=0.6±1.0; 33.2% overweight; 54.1% female) completed tasks measuring decision-making; general and food-specific behavioral disinhibition; willingness to delay gratification for food and money; cognitive flexibility; and working memory. Age (children vs adolescents) was examined as a moderator. All analyses adjusted for demographic factors, pubertal status, lean mass (kg), fat mass (%), height, general intellectual functioning, and depressive symptoms.
Results
After adjusting for multiple comparisons, more general behavioral disinhibition was associated with greater total energy intake (p = .02), and poorer cognitive flexibility was associated with more fat intake (p = .03) across all ages. Poorer decision-making in children (p = .04), but not adolescents (p = .24), was associated with greater fat intake. Food-specific behavioral disinhibition, the ability to delay gratification for both food and monetary rewards, and working memory were not significantly associated with youth’s disinhibited eating patterns during a single meal.
Conclusions
Most domains of EF were not associated with youth’s disinhibited eating. Significant associations may highlight the need to target specific cognitive processes, particularly behavioral disinhibition, decision-making, and cognitive flexibility, in potential intervention strategies for children’s disinhibited eating.
Keywords: executive functioning, cognitive, disinhibited eating, energy intake, obesity, child
Introduction
Executive functioning (EF) refers to the higher-order cognitive processes implicated in self-regulation and includes working memory, behavioral inhibition, cognitive flexibility and delayed gratification (1). Extant studies indicate that youth with obesity perform significantly worse than their peers without obesity on measures of EF, particularly tasks measuring behavioral inhibition, or the ability to inhibit or stop prepotent impulses (2–4). These data have led to the hypothesis that poorer EF may predispose youth to have excessive weight gain. These differences persist even after adjusting for confounds, such as depressive symptoms (3) and general intellectual functioning (4). The association between EF and obesity is likely bidirectional. Obesity has been linked to diseases characterized by significant cognitive decline (e.g., dementia, Alzheimer disease) (5), and poorer performance on measures of delayed gratification (6, 7), behavioral inhibition (2), and cognitive flexibility (8) are associated with excess weight gain and obesity onset.
It is theorized that poorer EF performance is associated with excess weight gain through eating-related self-regulatory difficulties. Two unique but overlapping systems, referred to as the 2-systems model, are posited to guide eating behaviors, including automatic and reflective processes (9, 10). The automatic processes capture impulsive behaviors and are thought to be the result of basic learning mechanisms, through which rewarding properties are paired with specific food items. The reflective processes include the higher-order self-regulatory (or EF) abilities that allow individuals to override automatic processes and make eating decisions based on factors such as knowledge and long-term goals. Based on this theory, a weaker EF system would contribute to a pattern of disinhibited eating behaviors, or those characterized by a lack of restraint, such as loss of control (LOC) eating, emotional eating, and overeating (11). Extant limited data offer preliminary support for these associations.
In school-age children, worse performance on measures of working memory (12) and behavioral inhibition (13) are associated with LOC eating, a predictor of excess weight gain (14). Children and adolescents with (versus without) LOC eating also demonstrate poorer behavior regulation, including difficulties inhibiting impulsive responses and adjusting to changes in task demands, as well as poorer emotional control, per their parents/caregivers’ reports (15). Children with Attention-deficit/Hyperactivity Disorder (ADHD), a behavioral diagnosis characterized by decrements in EF (16), are 12 times more likely to report LOC eating (13). LOC eating has also been found to mediate the link for both ADHD and parent-reported impulsivity with increases in body mass index (BMI; kg/m2) (13). As such, LOC eating may represent one disinhibited eating pathway through which poor EF promotes excess weight gain, although all of this research has relied on self-report of eating behaviors.
In preschool-age children, poorer behavioral inhibition is associated with greater intake of carbohydrates and sugar (17), as well as parents’ report of their children’s tendency to overeat in response to emotions (18). Similarly, preschoolers with low scores on a measure of delayed gratification, as well as high emotional arousal, consumed more total energy and more energy from sweets in the absence of hunger (18). Like preschool-age children, school-age children who exhibit poor general behavioral inhibition are more likely to engage in a range of disinhibited eating behaviors, including self-reported emotional and external eating (19), parent-reported food responsiveness (20), and greater consumption of energy dense food both in hungry and sated states (21). Similarly, Riggs et al. found that 4th grade children who self-reported more difficulties with EF-related processes, including general behavioral inhibition, emotional control, and working memory, also reported consuming more snack foods (22). In this same sample, strong self-reported EF also predicted greater self-reported fruit and vegetable intake one year later (23).
Importantly, not all studies have identified the expected link between EF and disinhibited eating patterns. In preschool-age children, EF performance was not associated with observed or parent-reported eating behaviors (24). However, those who performed better on a measure of delayed gratification for food items consumed more energy in the absence of hunger (24). Similarly, in a sample of school-age children, delayed gratification performance using both food and non-food items was positively associated with emotional overeating (20). The unexpected positive association between delayed gratification and disinhibited eating in children has been posited to reflect greater motivation for food (25).
In summary, the majority of research with youth supports a link between lower EF and greater disinhibited eating patterns. However, there are significant limitations to our current understanding of these associations. First, there are issues in assessment of both EF and disinhibited eating. Much of the EF literature has been narrowly focused on tests of general behavioral inhibition. Moreover, measurements of both EF and disinhibited eating patterns have frequently relied on self- and parent-reports (26). Further complicating the situation, EF is a diverse construct; some studies have even found an unexpected positive association between EF, specifically willingness to delay gratification, and disinhibited eating patterns (20, 24). Mixed findings across studies underscores the importance of evaluating multiple dimensions of EF, and of distinguishing between tasks including food and non-food items. Importantly, the link between EF and obesity appears strongest when EF has been assessed with objective tasks versus surveys (2), highlighting the importance of using neuropsychological tasks in evaluating associations with disinhibited eating patterns. Second, few studies have evaluated specific facets of EF in relation to adolescents’ disinhibited eating patterns (26). Some data suggest that the link between obesity and EF is more pronounced among adolescents versus children (2). Adolescence is characterized by a period of heightened impulsivity and reward-related processing (27) which, according to the 2-systems theory, may make this a particularly vulnerable period for disinhibited eating patterns, such as LOC eating (28, 29). Finally, few studies consider potential confounding factors, like general intellectual functioning, body mass, and depressive symptoms, in their efforts to clarify whether specific domains of EF are uniquely associated with youth’s disinhibited eating patterns (26).
The goal of the current study was to evaluate the association between youths’ EF and their disinhibited eating patterns using neuropsychological tasks and a buffet test meal, respectively. It was hypothesized that, after adjusting for relevant demographic factors, body composition, depressive symptoms, and general intellectual functioning, poorer decision-making, general and food-specific behavioral inhibition, cognitive flexibility, and working memory, would be associated with greater total energy intake, fat intake, and sugar intake. Based on prior literature (20, 24), it was also expected that, paradoxically, greater willingness to delay gratification for food items would be positively associated with these disinhibited eating patterns. Age was examined as a potential moderator. It was hypothesized that the links between poor EF and disinhibited eating would be particularly strong among adolescents (vs children) who, because of their growth, heightened impulsivity and reward-sensitivity, and elevated risk for disinhibited eating (27–29), are expected to consume particularly large meals (30).
Methods
Participants
Boys and girls between the ages of 8–17 years were recruited to participate in a study on pediatric growth and health behaviors (Clinical Trials Identifier: NCT02390765). All participants were in good general health, as determined by a medical history and physical examination. Exclusion criteria included: 1) major medical illness or pregnancy; 2) BMI < 5th percentile; 3) regular use of medication known to affect appetite or body weight; 4) significant or recent brain injury; 5) regular use of illicit substances; 6) significant weight loss (>5% of body weight) in the past three months; 7) current psychiatric disorder; and 8) full scale intelligent quotient score ≤ 70 (31). The Institutional Review Board of the Eunice Kennedy Shriver National Institute of Child Health and Human Development approved all study procedures.
Procedures
Individuals completed two screening visits at an outpatient pediatric clinic at the National Institutes of Health Hatfield Clinical Research Center. During the first visit, youth provided written assent and parents/guardians gave written consent. Families then completed a medical history and youth underwent a physical examination that included determination of pubertal development (32, 33). Youth then completed several surveys, including the Children’s Depression Inventory (34), as well as two semi-structured psychiatric interviews to determine eligibility. During the second visit, participants arrived in a fasted state. Their height was measured in triplicate by stadiometer and their weight was measured by a calibrated scale. Participants were then asked to consume in its entirety a standard breakfast shake (21% of estimated daily energy needs; 17% protein, 16% fat, and 67% carbohydrate), the amount of which was determined using measured body weight, height, age, and an activity factor based on self-reported average physical activity during the previous week (35, 36). Participants then completed several cognitive tasks and had their fat and lean mass measured via dual-energy x-ray absorptiometry (GE Healthcare, Madison WI). At approximately 12:00PM, participants ate lunch from a large buffet test meal.
Measures – Cognitive functioning
General intellectual functioning
General intellectual functioning was evaluated with the Wechsler Abbreviated Scale of Intelligence, 2nd Edition (WASI-II) (31). The WASI-II is a standardized brief intellectual screening tool comprised of four subtests that provides reliable, valid estimates of general cognitive ability among individuals as young as 6 years (31).
Decision-making
The Iowa Gambling Task was used to assess participants’ decision-making (37). For this 15-minute computer task, participants are asked to select one of four decks of cards. Each time a deck is selected, a specified amount of play money is either awarded or lost. Two of the decks of cards – called the disadvantageous decks - produce high immediate gains and significant losses, resulting in less money over time. The other two decks are considered advantageous, as they result in small, immediate gains and losses, and thus will yield more money over time. Performance on this task is defined as the difference between the number of advantageous and disadvantageous selections across five blocks. Lower or more negative net scores are reflective of poorer decision-making characterized by a preference for immediate rewards and/or a stronger insensitivity to negative consequences. Previous studies have used the Iowa Gambling Task to assess decision making in youth with obesity (38).
General behavioral disinhibition
General behavioral disinhibition was measured with the Stop Signal Task (39). For this 15-minute computer task, participants are asked to respond as quickly as possible to a go-signal presented on a computer screen by pressing one of two corresponding buttons on the keyboard, but to inhibit their response if they hear a tone before the signal is presented (25% of items). The speed with which the tone (or stop signal) is presented changes depending on the participant’s performance; it becomes increasingly closer to the go signal as participants perform better, and further away as participants fail to inhibit. Using this tracking algorithm, the stop signal delay converges on the delay at which individuals are able to stop 50% of the time. The primary indicator of performance on this task is the stop-signal reaction time (SSRT), calculated by subtracting the mean stop-signal delay from the mean reaction time. A longer SSRT represents a poorer response inhibition. The SSRT has demonstrated effectiveness in distinguishing children with overweight (40) from those without.
Food-specific behavioral disinhibition
Food-specific behavioral disinhibition was measured with the Food Go/No-Go Task (41). Participants are asked to press a button when a target “go” image (e.g., toy) is presented in the center of the screen. These “go trials” are presented on the majority (~73%) of trials to create a learned, prepotent tendency to respond to the “go” target. Youth are also instructed to withhold their learned responses in the presence of any other “no-go” stimulus (e.g., food), which are infrequently presented (~27% of all trials). Images consisted of high-calorie foods, low-calorie foods, and neutral non-food toys. Each stimulus type serves as both “go” and “no-go” targets, depending on the block. Each block has 35 “go” trials and 13 “no-go” trials. There are four randomized blocks of “go/no-go” pairs, including: high-calorie food—toy, toy—high-calorie food, low-calorie food—toy, and toy—low-calorie food. Target stimuli are presented for 500-ms with 2000–4000-ms between trials. Similar go/no-go tasks have been used with children as young as 7 years (42). The measure of interest was the number of commission errors (or responses incorrectly made to ‘no-go’ trials) for each pair of images; higher scores represent worse behavioral inhibition.
Delayed gratification
A 20-minute Delay Discounting Task was used to assess the ability to modulate desire for immediate gratification for the sake of long-term goals (43). Delayed gratification for both money and palatable food were examined. In the money version of the computerized task, participants are presented choices between a hypothetical monetary amount (e.g., $10) available after a specified delay (i.e., 1, 2, 7, 14, 30, 180, 365 days) and a smaller amount available immediately. Similarly, the food version presents youth with choices between one portion of their preferred palatable food (selected from a standard list before the task) available immediately and increasing portions of the food available at a delay. The Delay Discounting Task involves an adjusting amount procedure, whereby the amount of money or food portions offered increase at each delay interval. Indifference points are calculated for each participant at each delay and reflect the amount of money or food at which the immediate rewards became preferred over the delayed reward. These values were then used to calculate area-under-the-curve (AUC) values, separately for food and money, as outlined by Myerson et al (44). AUC values range from 0 to 1; smaller values indicate a steep discounting function (e.g., less willingness to wait for a larger reward as the delay increases). Previous research has identified no significant differences between real and hypothetical monetary rewards in outcomes for delayed discounting tasks (45). The Delay Discounting Task has been used successfully in children as young as 7 years of age (46).
Cognitive flexibility
Cognitive flexibility, or the ability to shift responses based on rules or contingencies, was assessed with the NIH Toolbox Dimensional Change Card Sort Test (47). For this 4-minute computer task, participants are asked to match a target visual stimulus to 1 of 2 choice stimuli according to shape or color. Performance is determined by the number of accurate responses. Normed scores are available for children as young as 3 years old and were created considering age, sex, race/ethnicity and maternal education (48).
Working memory
Working memory was assessed with the NIH Toolbox List Sorting Working Memory Test (47). For this 7-minute task, participants are placed at a computer and presented with a series of images, each for two seconds. For each item, an auditory cue accompanies the pictorial presentation. Participants are instructed to remember the stimuli and repeat them verbally to the examiner in order of size, from smallest to largest. The number and variety of objects in a series increases on successive items thereby taxing the working memory system when longer sequences need to be remembered. Performance is determined by the number of accurate responses. Normed scores are created considering age, sex, race/ethnicity and maternal education (48). This measure has demonstrated good test-retest reliability and convergent and divergent validity with children as young as 3 years (47).
Measures – Disinhibited Eating
Laboratory buffet test meal
At approximately 12:00PM, participants were escorted to a private room and exposed to a standardized buffet test meal (>10,000 kcal; 54% carbohydrate, 12% protein, 33% fat) comprised of diverse food items (49). They received tape-recorded instructions to “Let yourself go and eat as much as you want.” This test meal paradigm has been shown to induce disinhibited eating patterns, including greater total energy intake and palatable food intake, in children and adolescents (50, 51). All food items were weighed on electronic balance scales in gram weights to the nearest gram; foods consumed were determined by subtracting the food weights after the participant’s meal from initial weights. Food energy and macronutrient content were calculated using data from food labels. Total energy intake (kcal); percentage of energy intake from fat; and percentage of energy intake from sugar of the consumed meal were calculated with the ProNutra (Viocare Technologies, Princeton, NJ, USA) program. Total sugar intake refers to monosaccharides (glucose, fructose and galactose) and disaccharides (sucrose, lactose and maltose) and was reported as proportions of total energy consumed.
Data analysis
All analyses were conducted using IBM SPSS Statistics 24. Hierarchical multiple regression models were used to evaluate the association between youth’s EF and disinhibited eating. Age (children, 8–12y, versus adolescents, 13–17y) was a proposed moderator variable. All covariates were entered into the first level of each regression model (age when not examined as a moderator; sex; race coded as 0 = non-Hispanic white and 1 = other; pubertal status; lean mass in kg; percentage fat mass (arcsine transformed); height in cm; depressive symptoms; and general intellectual functioning (3, 4, 30, 52). Main effects of the EF indicator and age were entered into the second level of their own models. In the third and final level, a two-way interaction between the EF indicator and age were included. Separate models were conducted for each measure of EF and for each energy intake variable, including total energy intake (kcal); fat intake (percentage arcsine transformed); and sugar intake (percentage adjusted for total intake; arcsine transformed). To avoid concerns associated with multicollinearity, all EF indicators were centered based on the grand mean prior to being entered into each model (53). To reduce the likelihood of type I errors associated with multiple statistical tests, the Benjamini–Hochberg correction (54) was applied within families of planned contrasts and adjusted p-values are presented.
Results
Preliminary Analyses and Participants
Following a brief phone screen, 242 youth attended at least one of the two screening visits. Thirty-seven youth were not enrolled in the study or were deemed ineligible. The final sample for the current study included 205 participants (M age = 13.1±2.8y; 49.8% children 8–12y; M BMIz = 0.6±1.0; 54.1% female; 43.9% non-Hispanic white, 29.3% black/African American; 11.7% Asian/Asian American; 7.3% Hispanic/Latino/a; 7.8% multiple races). Missing data were minimal (< 5% for any variable); as such, listwise deletion was employed (55). One participant’s general behavioral inhibition score was not used because it was negative, which is indicative of significantly poor effort (56). One individual’s scores on the tasks measuring cognitive flexibility and working memory were winsorized (changed to three standard deviations above the mean) to reduce the effects of these outliers on the distributions. Percentage of breakfast shake consumed was considered as a covariate because 54 participants did not consume the shake in its entirety; however, this variable was not significant in any model nor did it change the significance or direction of any result and thus was excluded from all analyses. Table 1 shows bivariate correlations among the examined indicators of EF and disinhibited eating. The Supplementary table includes full results for the following hypothesis-testing analyses.
Table 1.
Correlations among Indicators of Executive Functioning and Disinhibited Eating
| M (SD) | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 | 12 | |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 1 Decision-Making | 0.82 (25.52) | ||||||||||||
| 2 General Behavioral Disinhibition | 284.32 (73.13) | −0.08 | |||||||||||
| 3 Delayed Gratification for Money | 0.46 (0.36) | 0.13 | −0.05 | ||||||||||
| 4 Delayed Gratification for Food | 0.42 (0.37) | 0.10 | 0.00 | **0.79 | |||||||||
| 5 Cognitive Flexibility | 47.89 (14.72) | 0.01 | −0.10 | −0.08 | −0.14 | ||||||||
| 6 Working Memory | 51.19 (10.09) | 0.10 | −0.05 | 0.04 | 0.03 | **0.24 | |||||||
| 7 High Calorie Foods vs Objects | 0.34 (0.23) | −0.05 | **0.21 | *−0.15 | −0.14 | *−0.15 | −0.06 | ||||||
| 8 Low Calorie Foods vs Objects | 0.33 (0.22) | **−0.25 | **0.23 | −0.13 | −0.03 | *−0.17 | −0.08 | **0.44 | |||||
| 9 Objects vs High Calorie Foods | 0.40 (0.23) | −0.11 | *0.16 | −0.13 | −0.04 | *−0.17 | −0.01 | **0.42 | **0.50 | ||||
| 10 Objects vs Low Calorie Foods | 0.43 (0.25) | −0.07 | **0.19 | 0.00 | −0.02 | −0.09 | −0.04 | **0.67 | **0.37 | **0.45 | |||
| 11 Total Calories Consumed | 972.89 (420.56) | *−0.15 | 0.10 | −0.10 | −0.10 | −0.04 | −0.01 | *0.19 | *0.22 | *0.23 | *0.15 | ||
| 12 Total Fat Consumed (%) | 0.65 (.08) | −0.10 | 0.02 | 0.03 | 0.00 | *−0.21 | −0.13 | 0.03 | 0.10 | 0.08 | 0.09 | **0.18 | |
| 13 Total Sugar Consumed (%) | 0.46 (.11) | 0.07 | 0.11 | 0.08 | 0.10 | 0.03 | −0.02 | −0.11 | −0.04 | −0.07 | −0.07 | −0.13 | **−0.53 |
Note.
p<.01
p<.05
Decision-making
In fully-adjusted models, co-varying for age, sex, race/ethnicity, pubertal status, lean mass, fat mass, height, depressive symptoms, and general intellectual functioning, the links between decision-making and all energy intake variables were non-significant (all ps = .28). However, age moderated the link between decision-making and the percentage of energy consumed from fat (β = .001, p = .04). In follow-up models conducted within each age group, among children age <13y, those who performed worse on a task measuring decision-making consumed a greater percentage of food from fat (β = −.001, p = .04; Figure 1a), while this association was non-significant in adolescents age ≥13y (p = .24; Figure 1b). Moderation models for total energy (p = .77) and total sugar intake were non-significant (p = .17).
Figure 1.
In fully-adjusted models, co-varying for age, sex, race/ethnicity, pubertal status, fat-free mass, fat mass, height, general intellectual functioning, and depressive symptoms, age moderated the link between decision-making and the percentage of calories consumed from fat (β = .001, p = .04). In a follow-up model conducted within each age group, children who performed worse on a task measuring decision-making consumed more food from fat (β = −.001, p = .04; Figure 1a) while this association was non-significant in adolescents (p = .24; Figure 1b).
General behavioral disinhibition
In fully adjusted models, general behavioral disinhibition was positively and significantly associated with total energy consumed (β = 1.14, p = .02); across all ages, youth who demonstrated more disinhibition consumed more energy during the test meal. Models for fat and sugar intake were non-significant and age did not moderate any associations (ps = .42 – .82).
Food-specific behavioral disinhibition
Adjusting for covariates, commission errors for high energy-density images (versus toys) were not significantly associated with energy intake and age did not moderate these associations (ps = .12 – .99). Commission errors for low energy-density images (versus toys) were not associated with energy intake and age did not moderate this association (ps = .12 – .99). Commission errors for toys (versus high energy-density food) images were not significantly associated with energy intake and age did not moderate these associations (ps = .12 – .99). Commission errors for toys (versus low energy-density food) images was not associated with energy intake and age did not moderate these association (ps = .24 – .99).
Delayed gratification
In fully adjusted models, the links between delayed gratification for money and energy intake were non-significant and age was not a significant moderator of any of these associations (ps = .44 – .81). Similarly, the links between delayed gratification for food and energy intake were also non-significant and age was not a significant moderator of these associations (ps = .48 – .97).
Cognitive flexibility
Adjusting for covariates, the link between cognitive flexibility and fat intake showed an inverse, significant relationship (β = −.001, p =.03); across all ages, participants who demonstrated greater cognitive flexibility consumed less fat during the test meal. Models with total energy (p = .74) and total sugar intake were non-significant (p = .50). Age did not significantly moderate any of these associations (ps = .12 – .79).
Working memory
In fully adjusted models, the links between working memory and energy intake were all non-significant and age did not moderate these associations (all ps = .39).
Discussion
The current study used diverse neuropsychological tasks and a validated test meal paradigm to evaluate the associations between EF and disinhibited eating in a sample of youth. General behavioral disinhibition was the only domain of EF associated with total energy intake. Across all ages, youth who demonstrated greater disinhibition consumed more total energy during a buffet test meal. Two domains of EF were associated with fat intake, and one of these associations differed by age. Across all ages, youth who demonstrated worse cognitive flexibility consumed more fat during the test meal. Moreover, children who demonstrated worse decision-making consumed a greater proportion of their food as fat; this association was not significant among adolescents. Food-specific behavioral disinhibition, the ability to delay gratification for both food and monetary rewards, and working memory were not significantly associated with youth’s disinhibited eating patterns during a single test meal.
Behavioral disinhibition is the construct most consistently and robustly associated with obesity in youth (57) and it was also the only variable in the current study associated with total energy intake during the test meal across all ages. These findings are consistent with other studies linking worse general behavioral disinhibition with greater snack food intake and LOC eating in children (13, 19–22). Difficulties inhibiting a desired behavioral response, such as consuming additional portions of palatable foods, may contribute to a consistent pattern of overeating associated with excess weight gain. However, from this perspective, it is unclear why the link between food-specific behavioral disinhibition, as assessed with the Food Go/No-Go Task (41), and energy intake was non-significant in adjusted models. This pattern of findings may suggest that broad behavioral control difficulties are associated with disinhibited eating patterns when youth are presented with an array of palatable and non-palatable food options, such as in the current study’s protocol. Our measure of food-specific behavioral inhibition used images that did not correspond with the same foods presented during the test meal. It is possible that greater correspondence between behavioral difficulties and disinhibited eating might have been observed if craved foods were used in both contexts. Nonetheless, in school-aged children, general behavior disinhibition is associated with more time spent in sedentary behavior as measured with accelerometers (58), while greater physical activity is associated with better behavioral inhibition (59). As such, general behavioral inhibition difficulties and unhealthy energy patterns may function to maintain one another and contribute to excess weight gain. Indeed, work from Riggs et al. (60) identified a high-risk pediatric obesity phenotype characterized by greater behavioral disinhibition, high sedentary behavior, and high energy intake. Additional studies are needed to better understand whether context-specific inhibitory difficulties have unique implications for youth’s health behaviors and obesity risk.
The only additional significant associations between EF and energy intake were observed for fat consumption. Specifically, children (but not adolescents) who performed worse on a measure of decision-making consumed a greater proportion of their meal as fat during the buffet meal, as did participants who demonstrated less cognitive flexibility. The non-significant link between decision-making and fat intake in adolescents was unexpected, given the heightened impulsivity and sensitivity to rewards observed during this development period (27). According to prospective data, performance on the Iowa Gambling Task improves linearly from childhood to adulthood (61). As such, a link between decision-making and fat intake may only be evident in younger children, before significant neural improvements in decision-making occur. Additional studies are needed to determine how these changes are associated with disinhibited eating patterns over time, and whether certain developmental periods represent critical points for health risk. For instance, from adolescence to adulthood, decision-making processes appear to transition from approaching risk to avoiding it (61). In the context of dietary decision-making, individuals with poorer decision-making may consume more fat as a younger child, and then rigidly avoid it as an adult, which may inadvertently promote disinhibited eating (62) and associated weight gain. Prospective data are needed to clarify whether developments in decision-making have differential effects on disinhibited eating patterns over time.
Poorer cognitive flexibility was also associated with greater fat intake, and this association was not moderated by age. Our data suggest that it may be an important domain of EF to consider in youth’s fat consumption. Given the demonstrated link between a high-fat diet and both acute and chronic declines in cognitive functioning (63), poorer cognitive flexibility and greater fat intake may reinforce one another over time. Importantly, both working memory and behavioral inhibition are considered integral components of cognitive flexibility (64). Given the non-significant link between working memory and energy intake, findings from the current study suggest that behavioral inhibition and cognitive flexibility may be particularly relevant to the disinhibited eating of youth. Concurrent difficulties inhibiting a behavioral response and greater inflexibility in thinking may contribute to a rigid pattern of responding to high-fat foods in which disinhibition inevitably occurs.
The lack of significant associations for delayed gratification and working memory with energy intake were unexpected. One possible explanation is that these domains of EF, while associated with obesity (2–4, 12, 19, 40), are less relevant to youth’s disinhibited eating patterns. They may be associated with excess weight gain through other behavioral and/or physiological mechanisms, or represent consequences of poor dietary choices and/or obesity. Additionally, prospective data suggest that the association between EF and disinhibited eating patterns may become more evident later in life. Specifically, there is a significant interaction between body mass and age for EF performance, indicating that the inverse association between EF and body mass increases with age (65). Finally, the fact that the majority of indicators of EF were not associated with disinhibited eating may be an artifact of measurement limitations. A single observation of disinhibited eating was used in the current study. Likewise, different domains of EF may only be relevant to youth’s disinhibited eating behaviors in certain contexts. For instance, the potential negative effects of weaker EF systems on disinhibited eating risk may only become evident in stressful situations, when youth’s cognitive and coping systems are further taxed (66). Including methods such as ecological momentary assessments in longitudinal studies would enhance our understanding of how EF abilities interact with environmental and state-level psychological changes to affect eating decisions.
Strengths of the current study address significant limitations of prior work by using an extensive neuropsychological battery to assess distinct domains of EF, as well as the inclusion of a buffet test meal to capture youth’s disinhibited eating. Although there are limitations to generalizing the findings from a single test meal to youths’ daily eating habits, intake patterns during this meal are correlated with body mass, adiposity, eating in the absence of hunger (67), binge eating, and emotional eating (68), suggesting these results may have implications for youths’ broader disinhibited eating habits and health risk. The current study also adjusted for confounding factors rarely considered in prior work, including body composition (so that the potential impact of obesity itself was mitigated), general intellectual functioning, and depressive symptoms. The primary limitations of the current study include its use of a convenience sample and cross-sectional design. This approach may limit our understanding of the link between EF and disinhibited eating in higher risk samples. EF and eating patterns also change over time and in different contexts. Results from the current study only represent correlations between performance on several EF tasks and energy intake at a single meal. Longitudinal studies with multiple assessments of both EF and disinhibited eating would greatly clarify optimal targets for obesity prevention in youth.
Our pattern of findings highlights the need to be clear about which EF domain is being studied when discussing EF in the context of health and health behaviors, particularly because prior work has spurred the development of interventions targeting EF as a means of reducing obesity risk in children (69). Our data suggest a rationale for studies targeting general behavioral inhibition, decision-making, and cognitive flexibility, to determine if improvements in these domains of EF can reduce disinhibited eating patterns and chronic disease risk in youth. The need to take a targeted approach to intervening with EF is reinforced by the lack of significant correlations between most of the indicators of EF that we evaluated (other than those stemming from the same task; see Table 1). Consistent with prior investigations (70), these findings indicate that EF is comprised of various related but distinct cognitive processes. Future research needs to determine whether modifying these cognitive processes has specific consequences for youth’s disinhibited eating patterns. For instance, some data suggest that targeting behavioral inhibition may be more relevant to reducing palatable food consumption versus promoting healthy food consumption (71). Although research related to targeting specific EF domains to improve youth’s eating habits is in its infancy, intervening early may prove to be prudent to minimize the potential harmful consequences of disinhibited eating on immediate and long-term cognitive functioning. Although the optimal strategies for strengthening decision-making, behavioral inhibition, and cognitive flexibility are unclear, these particular domains of EF continue to improve through adulthood (72), suggesting intervention approaches likely need to be developmentally tailored. Prospective studies are needed to determine if intervening with youth’s EF can serve as a means of reducing their disinhibited eating.
Supplementary Material
Acknowledgements
NRK, MTK and JAY contributed to study design; all authors contributed to data collection; NRK conducted data analysis and interpretation, completed the literature search, generated the figures and together with MTK and JAY wrote the first draft of the manuscript. All authors were involved in writing the paper and had final approval of the submitted and published versions. This work was supported by Intramural Research Program (NICHD grant number ZIA-HD00641; Yanovski); Supplemental funding (OBSSR, NIH; Yanovski); National Research Service Award (grant number 1F32HD082982; NICHD, NIH; Kelly)
Conflict of Interest Statement: The authors report no conflicts of interest for the present work. J.A.Y. reports grant support for unrelated projects examining pharmacological treatments of rare syndromes causing obesity from Rhythm Pharmaceuticals Inc. and Soleno Therapeutics, Inc.
Footnotes
Disclaimers: Dr. Yanovski is a Commissioned Officer in the United States Public Health Service. The opinions and assertions expressed herein are those of the authors and are not to be construed as reflecting the views of the DHHS, USU, the Public Health Service, or the U.S. Department of Defense.
References
- 1.Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD. The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: A latent variable analysis. Cognitive Psychol. 2000;41(1):49–100. [DOI] [PubMed] [Google Scholar]
- 2.Pearce AL, Leonhardt CA, Vaidya CJ. Executive and Reward-Related Function in Pediatric Obesity: A Meta-Analysis. Child Obes. 2018;14(5):265–79. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Bozkurt H, Ozer S, Yilmaz R, Sonmezgoz E, Kazanci O, Erbas O, et al. Assessment of Neurocognitive Functions in Children and Adolescents with Obesity. Appl Neuropsychol Child. 2017;6(4):262–8. [DOI] [PubMed] [Google Scholar]
- 4.Reinert KR, Po’e EK, Barkin SL. The relationship between executive function and obesity in children and adolescents: a systematic literature review. J Obes. 2013;2013:820956. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Kivipelto M, Ngandu T, Fratiglioni L, Viitanen M, Kareholt I, Winblad B, et al. Obesity and vascular risk factors at midlife and the risk of dementia and Alzheimer disease. Arch Neurol-Chicago. 2005;62(10):1556–60. [DOI] [PubMed] [Google Scholar]
- 6.Schlam TR, Wilson NL, Shoda Y, Mischel W, Ayduk O. Preschoolers’ delay of gratification predicts their body mass 30 years later. J Pediatr. 2013;162(1):90–3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Graziano PA, Kelleher R, Calkins SD, Keane SP, Brien MO. Predicting weight outcomes in preadolescence: the role of toddlers’ self-regulation skills and the temperament dimension of pleasure. Int J Obes (Lond). 2013;37(7):937–42. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Groppe K, Elsner B. Executive function and weight status in children: A one-year longitudinal perspective. Child Neuropsychol. 2017;23(2):129–47. [DOI] [PubMed] [Google Scholar]
- 9.Strack F, Deutsch R. Reflective and impulsive determinants of social behavior. Personality and Social Psychology Review. 2004;8(3):220–47. [DOI] [PubMed] [Google Scholar]
- 10.Jones A, Hardman CA, Lawrence N, Field M. Cognitive training as a potential treatment for overweight and obesity: A critical review of the evidence. Appetite. 2018;124:50–67. [DOI] [PubMed] [Google Scholar]
- 11.Shomaker LB, Tanofsky-Kraff M, Yanovski JA. Disinhibited Eating and Body Weight in Youth In: Preedy VR, Watson R, Martin CR, editors. Handbook of Behavior, Food and Nutrition. New York, NY: Springer; 2011. p. 2183–200. [Google Scholar]
- 12.Goldschmidt AB, O’Brien S, Lavender JM, Pearson CM, Le Grange D, Hunter SJ. Executive functioning in a racially diverse sample of children who are overweight and at risk for eating disorders. Appetite. 2018;124:43–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Reinblatt SP, Mahone EM, Tanofsky-Kraff M, Lee-Winn AE, Yenokyan G, Leoutsakos JM, et al. Pediatric loss of control eating syndrome: Association with attention-deficit/hyperactivity disorder and impulsivity. Int J Eat Disord. 2015;48(6):580–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Tanofsky-Kraff M, Yanovski SZ, Schvey NA, Olsen CH, Gustafson J, Yanovski JA. A prospective study of loss of control eating for body weight gain in children at high risk for adult obesity. Int J Eat Disord. 2009;42(1):26–30. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Gowey MA, Lim CS, Dutton GR, Silverstein JH, Dumont-Driscoll MC, Janicke DM. Executive Function and Dysregulated Eating Behaviors in Pediatric Obesity. J Pediatr Psychol. 2018;43(8):834–45. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders: Fifth Edition. Arlington, VA: American Psychiatric Association; 2013. [Google Scholar]
- 17.Levitan RD, Rivera J, Silveira PP, Steiner M, Gaudreau H, Hamilton J, et al. Gender differences in the association between stop-signal reaction times, body mass indices and/or spontaneous food intake in pre-school children: an early model of compromised inhibitory control and obesity. Int J Obes (Lond). 2015;39(4):614–9. [DOI] [PubMed] [Google Scholar]
- 18.Pieper JR, Laugero KD. Preschool children with lower executive function may be more vulnerable to emotional-based eating in the absence of hunger. Appetite. 2013;62:103–9. [DOI] [PubMed] [Google Scholar]
- 19.Maayan L, Hoogendoorn C, Sweat V, Convit A. Disinhibited Eating in Obese Adolescents Is Associated With Orbitofrontal Volume Reductions and Executive Dysfunction. Obesity. 2011;19(7):1382–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Groppe K, Elsner B. Executive function and food approach behavior in middle childhood. Front Psychol. 2014;5:447. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Nederkoorn C, Dassen FC, Franken L, Resch C, Houben K. Impulsivity and overeating in children in the absence and presence of hunger. Appetite. 2015;93:57–61. [DOI] [PubMed] [Google Scholar]
- 22.Riggs NR, Spruijt-Metz D, Sakuma KL, Chou CP, Pentz MA. Executive cognitive function and food intake in children. J Nutr Educ Behav. 2010;42(6):398–403. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Riggs N, Chou CP, Spruijt-Metz D, Pentz MA. Executive Cognitive Function as a Correlate and Predictor of Child Food Intake and Physical Activity. Child Neuropsychology. 2010;16(3):279–92. [DOI] [PubMed] [Google Scholar]
- 24.Hughes SO, Power TG, O’Connor TM, Orlet Fisher J. Executive functioning, emotion regulation, eating self-regulation, and weight status in low-income preschool children: How do they relate? Appetite. 2015;89:1–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Tan CC, Lumeng JC. Associations Between Cool and Hot Executive Functions and Children’s Eating Behavior. Curr Nutr Rep. 2018;7(2):21–8. [DOI] [PubMed] [Google Scholar]
- 26.Egbert AH, Creber C, Loren DM, Bohnert AM. Executive function and dietary intake in youth: A systematic review of the literature. Appetite. 2019;139:197–212. [DOI] [PubMed] [Google Scholar]
- 27.Ernst M, Fudge JL. A developmental neurobiological model of motivated behavior: anatomy, connectivity and ontogeny of the triadic nodes. Neurosci Biobehav Rev. 2009;33(3):367–82. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Swanson SA, Crow SJ, Le Grange D, Swendsen J, Merikangas KR. Prevalence and correlates of eating disorders in adolescents. Results from the national comorbidity survey replication adolescent supplement. Arch Gen Psychiatry. 2011;68(7):714–23. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Spurrell EB, Wilfley DE, Tanofsky MB, Brownell KD. Age of onset for binge eating: are there different pathways to binge eating? Int J Eat Disord. 1997;21(1):55–65. [DOI] [PubMed] [Google Scholar]
- 30.Shomaker LB, Tanofsky-Kraff M, Savastano DM, Kozlosky M, Columbo KM, Wolkoff LE, et al. Puberty and observed energy intake: boy, can they eat! Am J Clin Nutr. 2010;92(1):123–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Wechsler D, editor. Wechsler Abbreviated Scale of Intelligence–Second Edition (WASI-II). San Antonio, TX: Pearson; 2011. [Google Scholar]
- 32.Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969;44(235):291–303. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Marshall WA, Tanner JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970;45(239):13–23. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Kovacs M Children’s Depression Inventory 2nd Edition Technical Manual. Ontario, Canada: Multi-Health Systems, Inc.; 2011. [Google Scholar]
- 35.Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE, et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003;35(8):1381–95. [DOI] [PubMed] [Google Scholar]
- 36.Medicine Io. Dietary Reference Intakes: The Essential Guide to Nutrient Requirements. Washington, DC: The National Academies Press; 2006. [Google Scholar]
- 37.Bechara A, Damasio AR, Damasio H, Anderson SW. Insensitivity to future consequences following damage to human prefrontal cortex. Cognition. 1994;50:7–15. [DOI] [PubMed] [Google Scholar]
- 38.McNally KA, Shear PK, Tlustos S, Amin RS, Beebe DW. Iowa Gambling Task Performance in Overweight Children and Adolescents at Risk for Obstructive Sleep Apnea. J Int Neuropsych Soc. 2012;18(3):481–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Verbruggen F, Logan GD. Response inhibition in the stop-signal paradigm. Trends Cogn Sci. 2008;12(11):418–24. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Verbeken S, Braet C, Claus L, Nederkoorn C, Oosterlaan J. Childhood Obesity and Impulsivity: An Investigation With Performance-Based Measures. Behav Change. 2009;26(3):153–67. [Google Scholar]
- 41.Teslovich T, Freidl EK, Kostro K, Weigel J, Davidow JY, Riddle MC, et al. Probing behavioral responses to food: development of a food-specific go/no-go task. Psychiatry Res. 2014;219(1):166–70. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Folkvord F, Veling H, Hoeken H. Targeting implicit approach reactions to snack food in children: Effects on intake. Health Psychol. 2016;35(8):919–22. [DOI] [PubMed] [Google Scholar]
- 43.Odum AL, Baumann AA, Rimington DD. Discounting of delayed hypothetical money and food: effects of amount. Behav Processes. 2006;73(3):278–84. [DOI] [PubMed] [Google Scholar]
- 44.Myerson J, Green L, Warusawitharana M. Area under the curve as a measure of discounting. J Exp Anal Behav. 2001;76(2):235–43. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Madden GJ, Begotka AM, Raiff BR, Kastern LL. Delay discounting of real and hypothetical rewards. Exp Clin Psychopharmacol. 2003;11(2):139–45. [DOI] [PubMed] [Google Scholar]
- 46.Wilson VB, Mitchell SH, Musser ED, Schmitt CF, Nigg JT. Delay discounting of reward in ADHD: application in young children. J Child Psychol Psychiatry. 2011;52(3):256–64. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Weintraub S, Dikmen SS, Heaton RK, Tulsky DS, Zelazo PD, Bauer PJ, et al. Cognition assessment using the NIH Toolbox. Neurology. 2013;80:S54–S64. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48.Casaletto KB, Umlauf A, Beaumont J, Gershon R, Slotkin J, Akshoomoff N, et al. Demographically Corrected Normative Standards for the English Version of the NIH Toolbox Cognition Battery. J Int Neuropsychol Soc. 2015;21(5):378–91. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Shomaker LB, Tanofsky-Kraff M, Zocca JM, Courville A, Kozlosky M, Columbo KM, et al. Eating in the absence of hunger in adolescents: intake after a large-array meal compared with that after a standardized meal. American Journal of Clinicial Nutrition. 2010;92(4):697–703. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.Mirch MC, McDuffie JR, Yanovski SZ, Schollnberger M, Tanofsky-Kraff M, Theim KR, et al. Effects of binge eating on satiation, satiety, and energy intake of overweight children. Am J Clin Nutr. 2006;84(4):732–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51.Tanofsky-Kraff M, McDuffie JR, Yanovski SZ, Kozlosky M, Schvey NA, Shomaker LB, et al. Laboratory assessment of the food intake of children and adolescents with loss of control eating. Am J Clin Nutr. 2009;89(3):738–45. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Goulding A, Taylor RW, Gold E, Lewis-Barned NJ. Regional body fat distribution in relation to pubertal stage: a dual-energy X-ray absorptiometry study of New Zealand girls and young women. Am J Clin Nutr. 1996;64(4):546–51. [DOI] [PubMed] [Google Scholar]
- 53.Cohen J, Cohen P, West S, Aiken L. Applied multiple regression/correlation analysis for the behavioral sciences. 3rd ed. Mahwah, NJ: Lawrence Earlbaum Associates; 2003. [Google Scholar]
- 54.Benjamini Y, Hochberg T. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Statist Soc Series B (Methodological). 1995;57(1):289–300. [Google Scholar]
- 55.Buhi ER, Goodson P, Neilands TB. Out of sight, not out of mind: strategies for handling missing data. Am J Health Behav. 2008;32(1):83–92. [DOI] [PubMed] [Google Scholar]
- 56.Congdon E, Mumford JA, Cohen JR, Galvan A, Canli T, Poldrack RA. Measurement and reliability of response inhibition. Front Psychol. 2012;3:37. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Liang J, Matheson BE, Kaye WH, Boutelle KN. Neurocognitive correlates of obesity and obesity-related behaviors in children and adolescents. Int J Obes (Lond). 2014;38(4):494–506. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58.van der Niet AG, Smith J, Scherder EJ, Oosterlaan J, Hartman E, Visscher C. Associations between daily physical activity and executive functioning in primary school-aged children. J Sci Med Sport. 2015;18(6):673–7. [DOI] [PubMed] [Google Scholar]
- 59.Verburgh L, Konigs M, Scherder EJ, Oosterlaan J. Physical exercise and executive functions in preadolescent children, adolescents and young adults: a meta-analysis. Br J Sports Med. 2014;48(12):973–9. [DOI] [PubMed] [Google Scholar]
- 60.Riggs NR, Huh J, Chou CP, Spruijt-Metz D, Pentz MA. Executive function and latent classes of childhood obesity risk. J Behav Med. 2012;35(6):642–50. [DOI] [PubMed] [Google Scholar]
- 61.Almy B, Kuskowski M, Malone SM, Myers E, Luciana M. A longitudinal analysis of adolescent decision-making with the Iowa Gambling Task. Dev Psychol. 2018;54(4):689–702. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62.Stice E A prospective test of the dual-pathway model of bulimic pathology: mediating effects of dieting and negative affect. J Abnorm Psychol. 2001;110(1):124–35. [DOI] [PubMed] [Google Scholar]
- 63.Freeman LR, Haley-Zitlin V, Rosenberger DS, Granholm AC. Damaging effects of a high-fat diet to the brain and cognition: a review of proposed mechanisms. Nutr Neurosci. 2014;17(6):241–51. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64.Friedman NP, Miyake A. Unity and diversity of executive functions: Individual differences as a window on cognitive structure. Cortex. 2017;86:186–204. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65.Stanek KM, Strain G, Devlin M, Cohen R, Paul R, Crosby RD, et al. Body mass index and neurocognitive functioning across the adult lifespan. Neuropsychology. 2013;27(2):141–51. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Hill DC, Moss RH, Sykes-Muskett B, Conner M, O’Connor DB. Stress and eating behaviors in children and adolescents: Systematic review and meta-analysis. Appetite. 2018;123:14–22. [DOI] [PubMed] [Google Scholar]
- 67.Kelly NR, Shomaker LB, Radin RM, Thompson KA, Cassidy OL, Brady S, et al. Associations of sleep duration and quality with disinhibited eating behaviors in adolescent girls at-risk for type 2 diabetes. Eat Behav. 2016;22:149–55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 68.Vannucci A, Tanofsky-Kraff M, Crosby RD, Ranzenhofer LM, Shomaker LB, Field SE, et al. Latent profile analysis to determine the typology of disinhibited eating behaviors in children and adolescents. J Consult Clin Psychol. 2013;81(3):494–507. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 69.Hayes JF, Eichen DM, Barch DM, Wilfley DE. Executive function in childhood obesity: Promising intervention strategies to optimize treatment outcomes. Appetite. 2018;124:10–23. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 70.Duan X, Wei S, Wang G, Shi J. The relationship between executive functions and intelligence on 11- to 12-year-old children. Psychol Test Assess Model. 2010;52(4):419–31. [Google Scholar]
- 71.Dohle S, Diel K, Hofmann W. Executive functions and the self-regulation of eating behavior: A review. Appetite. 2018;124:4–9. [DOI] [PubMed] [Google Scholar]
- 72.Anderson P Assessment and development of executive function (EF) during childhood. Child Neuropsychol. 2002;8(2):71–82. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.

