Executive functions (also known as executive control or cognitive control) are top-down psychological processes required by individuals during attention or inhibiting irrational instinctual behavior (Diamond, 2013). Executive functions are closely related to academic achievement, social functioning, and emotional control in the development of individuals (Best et al., 2009; Liang et al., 2014). Inhibitory control is one of the most important components of executive functions. Inhibitory control usually refers to the ability to suppress automatic or dominant responses, but inhibition also requires interference control, directed forgetting, emotional control, and behavioral control (Nigg, 2000). Also, inhibitory control plays an important role in the development of individuals and can predict individual growth; for example, children with good inhibitory control are mentally and physically healthier in adulthood (Moffitt et al., 2011).

The development of inhibitory control continues after puberty. Previous behavioral studies have shown that the Stroop effect decreases when adolescence begins (Ikeda et al., 2011; Ordaz et al., 2013; Prencipe et al., 2011; Wu et al., 2011). Previous brain imaging studies have also reached relatively consistent conclusions. A study used functional magnetic resonance imaging (fMRI) techniques and the Stroop paradigm to examine 30 participants aged 7 to 22 years and found that activation in the frontal lobe increased with age; activation was significantly higher in young adults than in adolescents, who, in turn, showed significantly greater activation than children (Adleman et al., 2002). Another study used functional near-infrared spectroscopy (fNIRS) technology and the Stroop paradigm in 23 children and 14 adults to address this topic and revealed that brain activation (especially in the dorsolateral prefrontal cortex) caused by the Stroop effect increased with age from 7 to 29 years (Schroeter et al., 2004).

Executive function deficits are closely related to the prefrontal cortex. Clinical cases have shown that patients with prefrontal cortex lesions have difficulties with goal setting, planning, inhibition, and self-maintenance. Previous neuropsychological research has shown that the maturity of the frontal cortex parallels the development of executive functions (Garon et al., 2008; Luna et al., 2010; Ordaz et al., 2013; Prencipe et al., 2011; Shing et al., 2010; Wu et al., 2011). In the 1960s and 1970s, studies on human brain anatomy demonstrated that some brain regions, especially the prefrontal cortex, developed beyond childhood, and in the 1970s to 1980s, studies suggested that prefrontal cortex structure changed obviously in adolescence (Blakemore and Choudhury, 2006). In tasks that require the function of the frontal lobe, the performance of individuals followed a multi-polar developmental track, meaning that each subcomponent of the executive functions developed to maturity at a different time and in a different way. The most rapid period of development was from 6 to 8 years of age, during which abilities as concept formation, set-shifting, and rudimentary planning skills were present. Then, development tended be more gradual from late childhood and throughout adolescence continuing to develop into early adulthood (Ordaz et al., 2013; Tanaka et al., 2012). Previous studies have almost universally reached the consistent conclusion that executive functioning and the prefrontal cortex continue to develop after adolescence (Brown et al., 2005; Buttelmann and Karbach, 2017; Hsu et al., 2014; Luna et al., 2010; Prencipe et al., 2011; Satterthwaite et al., 2013; Shing et al., 2010).

In addition to age, obesity is another factor that influences the development of executive function. Previous studies have shown that obese children (or adolescents) exhibit lower inhibitory control than overweight children (or adolescents) (Pauli-Pott et al., 2010). The decline of cognitive function in children (or adolescents) is closely related to overweight (Li et al., 2008). Previous behavioral studies have shown that obese children have worse performance on the classical experimental task that is used to measure inhibitory control (Bruce et al., 2011; Wirt et al., 2014). A large number of executive function measurements have shown that obese children have significantly less control than healthy children, and obese adolescents have significant deficits in the structure of the prefrontal cortex (Liang et al., 2014). Brain imaging studies have also come to the same conclusion. For example, one study used functional magnetic resonance imaging (fMRI) and the Stroop paradigm to compare 54 obese participants and 37 healthy participants, and the results showed that the body mass index (BMI) was negatively correlated with Stroop interference and gray matter volume (Maayan et al., 2011). However, few imaging studies have addressed whether obesity damages the development of inhibitory control; hence, we used the Stroop task and fNIRS to explore the relationship between age and inhibitory control in obese individuals.

Inhibitory control is important for the development of individuals, and age and obesity are two factors that influence the development of inhibitory control. Inhibitory control and the prefrontal cortex, whose functioning is related to being overweight, develop to maturity after adolescence. The relationship between executive function and obesity may be bidirectional, that is to say, executive function deficits may be a potential factor in individual BMI increases, while weight loss is helpful to a certain extent in executive function improvement of obese individuals (Xianlin et al., 2015).

To study the inhibitory control of obesity, we conducted experiments using fNIRS and the Stroop color-word task, which is the classic psychological task for measuring frontal cortex function (Adleman et al., 2002; Yennu et al., 2016). In the Stroop task, participants are instructed to name the color of font in which a word is printed and ignore the dominant tendency to read the meaning of the word (naming the color of the word is more difficult because it is not the habitual response); therefore, the task requires inhibitory control (Aron, 2010). Stroop interference is the difference between the congruent condition (in which the text color matches the meaning) and the incongruent condition (in which the word for one color is printed in another color) in the Stroop task. The greater the differences in reaction time and accuracy, the larger the Stroop effect was; the worse the inhibitory control ability, the lower the prefrontal cortex activation (Schroeter et al., 2007).

Brain imaging techniques like fNIRS use near-infrared light changes in living tissues to detect specific changes in the concentration of oxygen in the targeted brain regions. The advantage of fNIRS is that this technology is not very sensitive to head movement, and optical imaging is both readily accepted by participants and harmless to the human body (Timinkul et al., 2008). It also provides appropriate spatial and temporal resolution and is easily accepted even by children and obese participants.

To explore whether obesity would affect the development of inhibitory control, we used fNIRS to test 54 individuals while they performed a Stroop task. As BMI is negatively correlated with inhibitory control and its related brain region (the prefrontal cortex), we hypothesized that Stroop interference on behavioral tests would not decrease with age and that the accompanying frontal cortex brain activation would not increase with age in obese individuals.

2.2 Stimuli and procedures

We used E-Prime 2.0 (Psychology Software Tools, Pittsburgh, PA) to present the stimuli and to record the data. This study used a modified Stroop task for visual-cognitive stimulation to evoke event-related potentials (Ehlis et al., 2005). The stimuli consisted of four words: “red”, “green”, “blue” and “yellow”, and each word was printed in red, green, blue or yellow to produce interference between color words and their text colors. The congruent condition meant that the color of the word was congruent with the meaning of the word (e.g., the word “RED” was printed in red text); the incongruent condition meant that the color of the word was incongruent with the meaning of the word, e.g., the word “RED” was printed in blue text (see Fig. 1A). Stroop interference was measured as the difference between the incongruent and congruent conditions (the incongruent minus the congruent) (Chen et al., 2013; Xu et al., 2007). The experimental procedure is displayed in Fig. 1A. In each trial, a cross-shaped fixation point “+” was displayed for 1000 ms first, and then the stimulus was presented for 1000 ms, followed by a blank screen presented for 10000 ms. The participant was asked to press the button to indicate whether the meaning of the word was congruent with its printing color as quickly and accurately as possible. The order of the stimuli was random. The formal experiment consisted of 48 trials (24 congruent conditions and 24 incongruent conditions). Also, before the experiment, there was a practice session consisting of six trials to ensure that the participant understood the procedure.

Figure 1.

A. The design of the experimental runs and instance for the two conditions (congruent and incongruent conditions) of the modified Stroop task. Participants were instructed to decide whether the semantic meaning of the word corresponded to the color of the word. B. The fNIRS probe consisted of 8 dual-wavelength sources (●) and 7 optical detectors (○), and the numbers (1 to 20) indicate the fNIRS channels. Optical sources and detectors probe on the international 10-20 standard positions.

Our study suggested that the behavioral performance and prefrontal cortex activation of 38 obese participants in the Stroop task did not increase with age. We found that RT was significantly higher in the incongruent condition than in the congruent condition and that ACC was significantly lower in the incongruent condition than in the congruent condition. Thus, our study successfully elicited Stroop interference following previous literature (Ehlis et al., 2005). Then, we found that age was not associated with Stroop interference in RT or ACC. In other words, behavioral Stroop interference did not decrease throughout cognitive development. This result differed from those of previous research (Huizinga et al., 2006). Also, we found that prefrontal cortex activation did not increase with age. The neural result was also inconsistent with previous studies in normal-weight participants, which showed that inhibitory control developed after adolescence. For example, an fMRI study found a positive correlation between ages from 7 to 22 years and Stroop-related activation in the left lateral prefrontal cortex in normal-weight participants. They also found that Stroop-task-related functional development of the prefrontal cortex continues to develop into adulthood (Adleman et al., 2002).

Another fNIRS study (Schroeter et al., 2004) found that the brain activation due to Stroop interference significantly increased with age (from 7 to 29 years) in the DLPFC in normal-weight participants. In the present study, activation during the Stroop task did not increase with age from childhood to young adulthood, implying that the neural mechanisms used to suppress the Stroop effect did not develop in obese individuals as it does in normal-weight people. This inconsistency might be explained by the fact that we included obese individuals as our participants, unlike Schroeter et al. (2004) or others did, since obesity might affect the association between age and the Stroop interference-effect. Although not consistent with the current literature about the non-obese population, the findings of obese participants in our study can be regarded as a novel, but a meaningful phenomenon that warrants further study. As a review points out, the heavy burden of overweight and obesity during childhood and adolescence and its effects on cognitive control development (Esteban-Cornejo et al., 2018).

Executive function deficits are closely related to the prefrontal cortex. Clinical cases have shown that patients with prefrontal cortex lesions have difficulties with goal setting, planning, inhibition and self-maintenance, and previous neuropsychological research has shown that the maturity of the frontal cortex parallels the development of the executive functions (Leon-Carrion et al., 2004). Studies using non-invasive brain stimulation procedures have found that the DLPFC implicated in inhibitory control. One study found that repeated tDCS for 5 days over the right DLPFC may induce a more persistent decrease in self-reported craving, probably because enhancing the right DLPFC activity may strengthen inhibitory control (Ljubisavljevic et al., 2016).

Overweight or obese individuals often show deficits in executive function compared to normal-weight individuals. In childhood, obese individuals have more difficulty in response inhibition than lean individuals (Nederkoorn et al., 2007). A systematic literature review showed that obese adolescent individuals (from 13 to 18 years of age) had poorer performance than healthy individuals in tasks that depend on inhibitory control and, furthermore, had smaller OFC volume (Reinert et al., 2013). In an adult population, Willeumier et al. (2011) found that high BMI might be a risk factor for decreased prefrontal cortex function and potentially impaired executive function. Our study found that in obese subjects, brain activation during the Stroop task did not increase with age and decreased in the right DLPFC and the OFC, implying that obesity affected the development of those two areas.

Obesity itself has a compounding negative impact on the brain via mechanisms currently attributed to low-grade systemic inflammation, elevated lipids, and/or insulin resistance (Smith et al., 2011). Components of the immune system involved in inflammation can alter neural, cognitive, and motivational processes that lead to impaired self-regulation and poor health (Shields et al., 2017). Therefore, we recommend early prevention of impaired executive function. A previous study showed that the performance of participants on a Stroop task improved after dieting (Makris et al., 2013). Also, aerobic exercise helped improve executive functions (Kamijo et al., 2012). Furthermore, regular exercise can affect brain plasticity and increase the volumes of gray matter and white matter in the brain (Dupuy et al., 2015). Therefore, exercising to lose weight might be a good way for young people to improve their executive function ability and promote the healthy development of the prefrontal cortex.

We did not find a correlation between BMI and brain activation during the Stroop task. One possible explanation is that, although BMI is commonly used to measure obesity, it is not a very accurate predictor of cognitive processes and does not represent body fat percentage very well (Nuttall, 2015). If we could find a better index of obesity that predicted cognitive processes more accurately, then we could examine the relationship between obesity and various health risks through functional neuroimaging. For example, waist circumference is a more sensitive indicator of obesity, particularly in females, for potentially determining the adverse effects of obesity and overweight on the brain and associated risks to health (Kurth et al., 2013). Another reason might be the design of the present study procedure; the difficulty of the Stroop task was lowered to adapt the test to child participants. Research on developmental inhibitory control may be affected by the flexibility of the task, and complex cognitive tasks can reflect those small changes (Buttelmann and Karbach, 2017).

Inhibitory control plays a very important developmental role but obesity impairs its development. In healthy individuals, inhibitory control continues to develop into adulthood. However, in obese individuals, inhibitory control does not follow the same developmental trajectory, possibly because obesity impairs prefrontal cortex function (Willeumier et al., 2011). Therefore, we recommend early prevention of impaired executive function.

We thank all the participants for their participation. This research was supported by the Science Fund for Hubei Superior Discipline Groups of Physical Education and Health Promotion, National Natural Science Foundation of China (Grant No. 81971661), the project from General Administration of Sport of China (Grant No. 2014B094), and Natural Science Foundation of Hubei Province (Grant No. 2016CFA098).

The authors declare no competing interests.