Given the constantly evolving nature of our world, it is crucial to carefully choose the most suitable course of action to effectively achieve our objectives. In this context, inhibitory control is a pivotal component of executive functions, encompassing the capacity to successfully adapt to the environment to inhibit maladaptive behaviors, emotions, and thoughts (Diamond, 2013). Effective inhibitory processes are essential for healthy development in individuals from childhood through adulthood. Indeed, numerous studies have suggested that poor inhibitory control may be associated with a range of disorders, such as Attention-Deficit/Hyperactivity Disorder (ADHD) (Schachar et al., 2000; Woltering et al., 2013; Einziger et al., 2021), schizophrenia (Reilly et al., 2008; Galaverna et al., 2012), and Obsessive-Compulsive Disorder (OCD) (Penadés et al., 2007).

The maturation of the brain, particularly the frontal cortex, is closely linked with the development of inhibitory control (Wolfe and Bell, 2007a; Luna et al., 2015). As such, inhibitory control develops gradually from infancy to childhood and improves further during adolescence as the brain matures (Luna et al., 2004). Williams et al. (1999) conducted a study examining inhibitory processes across the lifespan (ages 6–81) using a task that required participants to stop prepotent responses. The authors reported that stopping speed becomes faster with increasing age throughout childhood, with limited evidence of slowing across adulthood. Their results were in good accordance with previous results where authors showed children with a mean age of 9.8 were 50 ms faster than the children with a mean age of 7.9 (Schachar and Logan, 1990) and 11 years old children were 40 ms faster at stopping than the 8-year-old children. Accordingly, the literature supports the notion that the inhibitory process improves from childhood to adolescence as a result of maturation (Schachar and Logan, 1990; Williams et al., 1999; Luna et al., 2004). However, it may gradually slow down across adulthood (see Williams et al., 1999). Keeping in mind these behavioral studies that show maturation-related differences in inhibitory processes, the current study will investigate how the maturation of inhibitory processes is reflected in event-related brain oscillations.

Although behavioral studies are commonly used to assess inhibitory control, studies have also been investigating electrophysiological markers of inhibition in infants and children. Inhibitory control could be investigated with EEG methodologies, among them; event-related potential (ERP) studies are highly used in the research of inhibitory control (see Ciesielski et al., 2004; Zinchenko et al., 2019; Einziger et al., 2021) ERPs have the advantage of identifying time during inhibitory control (Zinchenko et al., 2019; Einziger et al., 2021). However, it is also noted that ERPs could be hard to be studied in infants or early childhood; therefore, some researchers preferred to use task-related responses, where the precise time could not be followed, but this methodology could be used by comparing the baseline to task-related functions.

Studies utilizing ERP methods suggest that N2 and P3 responses observed in the frontal-central regions are indicative of inhibitory processes (Jonkman, 2006; Johnstone et al., 2007; Hämmerer et al., 2010; Huster et al., 2013; Knežević and Marinković, 2017; Richardson et al., 2018). More specifically, the N2 response is often linked with conflict monitoring, as its amplitude tends to increase in situations where two competing responses must be evaluated (e.g., requiring whether to respond to a stimulus or inhibit the response) (Donkers and van Boxtel, 2004; for review see Huster et al., 2013). The P3 response, on the other hand, is mainly linked to assessing the effectiveness of inhibitory performance (Bruin et al., 2001; for review see Huster et al., 2013). Based on the developmental process, studies have demonstrated that children exhibit higher levels of N2 response compared to young adults. The amplitude of N2 gradually decreases with increasing age (Todd et al., 2008; Buss et al., 2011; Richardson et al., 2018; Zinchenko et al., 2019), whereas the amplitude of P3 tends to increase with age (Jonkman, 2006; Richardson et al., 2018). Furthermore, studies have observed that N2 (Jonkman, 2006) and P3 responses (Hämmerer et al., 2010) in children are more prominent in the posterior regions of the brain. As the brain matures during development, these ERP components shift towards more frontal-central electrodes (Jonkman, 2006; Hämmerer et al., 2010). These posterior activations are interpreted as indicating additional neural activity due to the underdevelopment of the frontal cortex (Jonkman, 2006).

In addition to examining the N2 and P3 components, research has also investigated the N450 component in the context of inhibitory processes, particularly conflict monitoring. The N450 component, originating from neural activity in the anterior cingulate cortex (ACC) and frontal brain regions, is believed to be observed in cognitive tasks involving conflict processing and the suppression of irrelevant information (West et al., 2004, 2005; Larson et al., 2009). Besides the N450 component, studies utilizing cognitive tasks that require the resolution of conflicting information have observed activation in later time windows (West, 2003; Coderre et al., 2011; Naylor et al., 2012 for review see Heidlmayr et al., 2020). This particular activation has been assigned different names, such as the late positive component (LPC) (see Coderre et al., 2011), the late sustained potential (LSP) (see Naylor et al., 2012) and the conflict slow-potential (conflict SP) (see Larson et al., 2012). Although the precise role of this component is still ambiguous, it seems to contribute to conflict resolution process (West, 2003; Coderre et al., 2011; Naylor et al., 2012; for review see Heidlmayr et al., 2020). Although there are limited studies focusing on N450 and conflict SP in children, Larson et al.’s (2012) study revealed that children demonstrate a higher N450 response and conflict SP compared to young adults. On the other hand, researchers examined conflict adaptation skills by investigating the difference between “incongruent trial preceded by an incongruent trial” and “incongruent trial preceded by a congruent trial,” and obtained similar results in children and adults (Larson et al., 2012).

One alternative approach to examining inhibitory control is through time-frequency decomposition, although the literature in this area remains limited. Assessing inhibitory control in laboratory settings commonly involves using paradigms such as Go/No-Go and Stop-Signal. Additionally, Stroop-like paradigms are also used in inhibition literature (Gerstadt et al., 1994). Stroop-like paradigms encompass variations of the original Stroop task that exhibit similar interference effects but employ different stimuli (such as the classic Stroop Interference task, day-night Stroop task, and Yes-No Stroop task). Although the specific stimuli may vary, the fundamental principle remains unchanged, where conflict emerges between the attributes of the stimulus (Stroop, 1935). While slight differences exist between Go/No-Go and Stop-Signal, they both require inhibiting a prepotent response. The Go/No-Go and Stop-Signal tasks are closely associated with behavioral inhibition, primarily focused on motor responses, as compared to Stroop-like tasks. On the other hand, Stroop paradigms differ from the other paradigms mentioned above by specifically requiring interference control, which involves inhibiting automatic responses and selectively attending to less automatic ones (e.g., saying “day” when the picture represents night). Furthermore, Stroop paradigms appear more ecologically valid due to their resemblance to real-life situations where individuals must navigate and resolve conflicting information (Montgomery and Koeltzow, 2010). Since the day-night Stroop task is preferred in this research, the studies that have employed Stroop-like paradigm in children will be summarized in the following paragraph.

As reviewed by Bhavnani et al. (2021), eight studies analyzed Stroop-like paradigms (Yes-No task, day-night task) in children. In these studies, the alpha power spectrum was investigated in a task-related paradigm. The researchers analyzed the difference between baseline power and task-related power. They found increased task-related alpha power compared to baseline during Stroop-like tasks. In a series of studies [Wolfe and Bell (2004), Bell and Wolfe (2007), Wolfe and Bell (2007a,b), Wolfe and Bell (2014); for review see Bhavnani et al. (2021)] showed the importance of alpha oscillations during inhibitory processes in infants and children. Studies showed that alpha power increased from baseline to task in children both eight months age infants and 3-to-5 years old children during Stroop-like day-night tasks (Wolfe and Bell, 2007a,b, 2013). Cuevas et al. (2016) later confirmed these results and also showed increased alpha power during Stroop-like versus Non-Stroop-like day-night tasks.

These pioneering and essential studies showed the indispensable role of task-related alpha power during inhibition in children. Nonetheless, none of the studies have been able to investigate the direct differences in brain responses between children and young adults when confronted with a stimulus that should be inhibited. Because, unlike event-related designs, task-related designs involve continuous tasks over a certain period, which precludes the possibility of making such a comparison but investigates more like the status of the brain during the task. Accordingly, task-related approaches are limited in their ability to analyze event-related phase locking, event-related synchronization, and desynchronization. Having a precise zero point in EEG data, as in the event-related approach, is an important step in investigating neural correlates of inhibitory response to presented stimuli, directly. It gives us the opportunity to examine two important features of the stimulus-related time-locked brain signals; phase and power. Both features contribute valuable information about brain activity during event processing, but they capture different aspects of neural responses. Researchers often use these complementary approaches to gain a comprehensive understanding. By investigating phase-locking analysis, which measures the consistency of brain responses to stimuli and necessitates a precise zero point, we can infer the temporal precision of the brain’s response to the event. The phase-locked activity reflects the precise timing of neural responses relative to the event onset. The information related to phase and power represents distinct aspects of brain functioning, and as such, they may behave differently. For instance, Hanslmayr et al. (2005) demonstrated that visual discrimination performance was associated with a decrease in alpha power but an increase in phase locking. Consequently, the implementation of an event-related design to conduct event-related phase and power analysis can be essential in understanding how the brain processes sensory information or reacts to specific stimuli.

Therefore, along with the importance of task-related studies, event-related studies are quite needed in the field to achieve more robust results in this respect. To our knowledge, in all these studies, task-related alpha power was analyzed, but none of the studies investigated the event-related alpha power and phase locking in children with Stroop-like tasks by comparing with the young adults. Thus, the primary aim of this study is to evaluate the inhibitory process by comparing children and young adults using an event-related approach within the alpha frequency band. With this approach, it becomes possible to analyze phase-locking responses and synchronization/desynchronization in the alpha frequency band. In this regard, it is hypothesized that children and young adults would exhibit different brain topography in terms of event-related alpha dynamics. It is also expected to see differentiated alpha synchronization/desynchronization and phase-locking characteristics between children and young adults, reflecting the maturation-related developmental differences in inhibitory processes between the two groups.

The main aim of the current study was to investigate the differences in inhibitory processes between 6-to-7-year-old children and young adults represented by the event-related inter-trial coherence (phase locking analysis) and event-related synchronization/desynchronization (power analysis) specifically in the alpha frequency band. To achieve this goal, we recorded EEG signals from all participants during the day-night Stroop task. As far as we know, this is the first study to explore these differences using an event-related approach.

The current study has been able to reveal some main differences between children and young adults in inhibitory processes, as depicted in Figure 7. Accordingly, behavioral results of the study revealed that young adults exhibited fewer errors compared to children. This finding is consistent with earlier studies in which inhibitory processes across different ages were investigated (Schachar and Logan, 1990; Williams et al., 1999). The EEG results from our study corroborate the differences observed in behavioral findings between children and young adults, which will be elaborated and discussed in the following paragraphs.

In the early and late time windows, our EEG results showed that children exhibited greater event-related alpha power than young adults. In the late time window, this difference was due to decreased alpha power seen in adults, which was not observed in children. In line with our findings, the study conducted by Sato et al. (2018) also found increased alpha power in children during working memory paradigm. Specifically, they observed increased alpha power in the left inferior parietal lobe after stimulus onset, which decreased after the retention interval. The authors suggested that this increase in alpha power could be due to the suppression of the dorsal stream, consistent with the inhibition hypothesis, this may reflect top-down attentional and/or inhibitory control (Klimesch et al., 2007; Jensen and Mazaheri, 2010). According to the inhibition hypothesis, the increase in alpha is considered to be the suppression of processing that is not necessary to perform the given task, while the alpha suppression is construed as cortical engagement (Pfurtscheller and Da Silva, 1999; Klimesch et al., 2007; Jensen and Mazaheri, 2010). In our study, the higher alpha activation observed in the early time windows, followed by the absence of event-related desynchronization (ERD) in children, could also be explained in terms of the inhibition hypothesis. Thus, the higher alpha response observed in children compared to young adults may be attributed to their increased need for resources and/or effort in order to suppress internal and external distractions. Similarly, as a continuation of this, the alpha decrease observed in young adults as a sign of cortical engagement has not been observed in children, which may be due to insufficient maturity of the top-down attentional processes in children.

On the other hand, in our previous study, increased alpha power and alpha phase locking values were shown in children during the visual and auditory item memory task (Güntekin et al., 2020). The authors discussed increased posterior alpha responses in children, as a compensation mechanism for immature top-down processes that coincide with overactive sensory processing. Additionally, several studies showed that alpha power can increase over parietal-occipital regions during tasks that require sensory processing, visual attention, or emotional processing (Güntekin and Basar, 2007; Başar, 2012; Başar and Güntekin, 2012). At this point, it is crucial to recognize that there are multiple alpha networks that may be related to different cognitive functions, including sensory processing, inhibition, memory processes, attention, and emotion. Since both above-mentioned studies (Sato et al., 2018; Güntekin et al., 2020) require sensory processing along with increased visual attention, even though the paradigms used in the two studies are different, it is possible that the increase in alpha power in parietal-occipital areas in children could be due to overly active sensory processing along with the visual attention during task performance. In accordance with these studies, in our study, the day-night Stroop task was presented to children through a computer as visual stimulation, which might have resulted in overactive perceptual processing and increased visual attention compared to healthy adults, potentially leading to increased parietal-occipital alpha responses in children. It remains unclear whether the observed increase in alpha power in children is solely attributable to overactive sensory processing, increased visual attention, or due to the suppression of the dorsal stream. A comparative investigation of different paradigms in children could shed light on the underlying mechanisms of these observed alpha dynamics, thereby advancing our understanding of the neural differentiations underlying sensory processes, visual attention, and cognitive control during development.

While the alpha power increased in children, as a complimentary of this finding, their alpha phase locking responses were lower than those observed in young adults. It seems that brain responses to the same type of stimulus are not consistent in children as reflected by lower alpha phase locking values. When we consider these main findings together, it can be said that the brain, children were not able to give a consistent response to the same type of stimuli that should be inhibited, as in young people, instead increased the strength of the EEG response as compensation. These findings also support a lack of maturation in inhibitory processes in children as required by the applied task.

The current study also indicates a topological shift from posterior to anterior regions during inhibitory processing from childhood to adulthood. Specifically, our results demonstrate greater alpha activation in the occipital and parietal regions in children compared to young adults. Our previous study reported not only increased activity over parietal and occipital areas for alpha responses but also similar results for theta responses during an item memory task (Güntekin et al., 2020). It was shown that young adults exhibited higher frontal theta power and phase-locking over frontal-central locations which were not observed in children who had reduced frontal responses (Güntekin et al., 2020). This posterior-to-anterior change appears to be due to the underdevelopment of the frontal areas or the heightened activity of the perceptual system in children, as discussed in the previous paragraph. As Jonkman (2006) suggested, the activation observed in posterior regions in children might indicate the need for additional neural activity due to the lack of maturation in the frontal cortex. On the other hand, Ofen and Shing (2013) have suggested that during childhood, episodic encoding may rely more on perceptual systems, while during adulthood, top-down frontal control becomes more prominent. It is possible that the perceptual system is more active in children than in adults, which could be reflected in increased alpha responses in children during inhibitory processes. Even though the exact mechanism remains a mystery, it appears that children have inverse frontal-occipital dynamics compared to young adults.

Although some studies have reported hemispheric differences shifting from left to right with age (see Bunge et al., 2002; Johnstone et al., 2005), our current study did not find any significant hemispheric differences between children and young adults. However, regardless of group, we did observe right hemisphere dominance in the early time windows. As we progress into the subsequent time windows, the right hemisphere dominance appears to decrease. This change may be related to approaching the time of verbal response. Existing research indicates that during the inhibitory process, adults generally display greater activation in the right hemisphere compared to the left hemisphere (Garavan et al., 1999; Aron et al., 2004), suggesting a potential link between the right hemisphere and competence in inhibition. However, due to the nature of our experimental paradigm, involving semantic processing, a competitive interaction may arise between cognitive processes that require verbal responses and inhibitory processes during the late time windows. Consequently, the dominant activation observed in the right hemisphere during early time windows might result from the conflict arising from the attributes of the stimulus and the requirement to inhibit automatic responses, along with selective attention to less automatic ones. Conversely, once this conflict is resolved, it appears that the involvement of the left hemisphere increases, as it takes a more active role in generating verbal responses, such as uttering “day” or “night.” Our findings also revealed that irrespective of the participant group, the response in the right hemisphere exhibited greater phase-locking compared to the left hemisphere. This result is consistent with the known association of the right hemisphere with inhibitory processes and hence, not unexpected.

All in all, our findings of increased event-related alpha power in children during the inhibitory task are consistent with task-related studies (Wolfe and Bell, 2004, 2007a, b, 2014; Bell and Wolfe, 2007). The current study also provides insights into alpha event-related synchronization/desynchronization and phase-locking differences between 6 and 7 years-old children and young adults using an event-related approach during the inhibitory processing.

The present study also had some limitations. The day-night Stroop task involves multiple cognitive processes, including memory, visual attention, decision-making, response inhibition, and motor processes related to the verbal expression of the answer. These processes are combined within a swift time window, making it difficult to attribute the observed oscillatory dynamics to the inhibition process solely. While the main function is inhibition, attention, decision-making, and motor response may also play a role in the observed alpha synchronization and desynchronization. However, it is important to acknowledge that avoiding this trade-off is also challenging for many cognitive neuroscience studies, as almost all tasks used in this field require some level of attentional and perceptual mechanisms. Nevertheless, future research could compare paradigms that may separate and manipulate specific cognitive functions to understand the underlying processes better. Other points that should be mentioned are the relatively small sample size of the study and the small number of electrodes utilized, which were enough electrodes for the employed analysis methods here, but, insufficient for source localization analysis like LORETA and Beamformer analysis. Another limitation of the current study was the analysis that was limited to the alpha frequency band. Although we tried to test a specific hypothesis related to the alpha band, it would be highly informative to examine the results of other frequency bands to ascertain the potential involvement of other frequencies in this inhibition phenomenon. Future studies should take these points into consideration to explore how other frequencies and neural localizations are implicated in this inhibition phenomenon. This could be achieved by increasing the participant number to enhance statistical power and facilitate robust conclusions.

The current study was conducted to elucidate the neural processes underlying inhibitory control in children and young adults. This study reveals that, concerning the inhibitory process, alpha dynamics in children differ from those of young adults. These differences are represented by increased alpha power in early time windows, decreased event-related desynchronization (ERD) in later time window, and phase-locking characteristics of alpha oscillations in children. In addition to these, the observed shift in event-related alpha power from posterior to anterior regions with age appears to align with a progressive maturation of the frontal areas from childhood to adulthood (Luna et al., 2004; Wolfe and Bell, 2007a). However, the reason why additional posterior brain regions are involved in inhibitory processes is still not well understood. This may stem from the perceptual system being more active in children (Sato et al., 2018; Güntekin et al., 2020), as well as the need for additional neural activity due to the incomplete maturation of the frontal cortex (Jonkman, 2006). Even though further studies are required to fully comprehend the underlying reasons, our study clearly demonstrates that children exhibit an inhibitory mechanism that has not yet fully developed, as evidenced by both behavioral and electrophysiological outcomes when compared to young adults.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving humans were approved by Istanbul Medipol University Ethics Committee. The studies were conducted in accordance with the local legislation and institutional requirements. Written informed consent for participation in this study was provided by the participants’ legal guardians/next of kin.

ÖC, BG, TA, EY, FA, and EA initiated and planned the study and designed the protocol. BG, ÖC, SA, TA, EY, FA, and EA wrote, reviewed, and edited the paper. TA, EY, HU, and PÇ collected and analyzed the data. ÖC and BG supervised and controlled the study. All authors contributed to the manuscript revision, read and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.