Emotion recognition and executive functions in school children born term and preterm

Reconocimiento de emociones y funciones ejecutivas en estudiantes nacidos a término y prematuros

Each year about 15 million preterm births (PB) take place, that is, one in every 10 births. PB is the main cause of death of children under five years of age (World Health Organization [WHO] 2022), responsible for 35% of the 3.1 million deaths globally each year (Blencowe et al., 2013). When birth occurs before 37 weeks, it is considered preterm. It can still be classified as extremely preterm (less than 28 weeks), very preterm (28 to 32 weeks), and moderate (32 to 37 weeks; WHO, 2022).

It is possible to identify which stages of brain development have been completed or are in progress through the gestational age. In this sense, preterm leads to anatomical and structural alterations of the brain due to the interruption of prenatal development stages with damage to brain maturation (Peterson Zomignani et al., 2009). For example, it is a predictor of the following factors: (1) motor impairment (Oliveira et al., 2011; Synnes & Hicks, 2018), (2) worse cognitive scores in early childhood (Beauregard et al., 2018), (3) damages in social and discipline issues (Guardiano et al., 2017), (4) increased difficulty in early childhood social communication, development and implementation of social cognition (Scott et al., 2012), (5) impact on the understanding of decision-making activities by emotional ambivalence (Wong et al., 2014), (6) presence of deficits in emotion recognition, cognitive control (Twilhaar et al., 2019) problems of socialization in adolescence, problems associated with changes in the brain network of emotional processing, with greater vulnerability to psychiatric disorders (Healy et al., 2013), and (7) deficit in executive functions (EFs; Brydges et al., 2018; Lowe et al., 2019).

In this sense, EFs refers to the skills that assist in reasoning, planning, problem-solving and managing the individual's life. It covers cognitive skills that allow one to store information, inhibit responses, and change the focus of attention on a given task or problem (Blair, 2017). For Diamond (2013), EFs also includes working memory, inhibition, and cognitive flexibility. Inhibitory control involves the ability to control one's attention, behavior, thought, and emotions to counteract a strong internal predisposition or external attraction and do what is appropriate or necessary. Cognitive flexibility includes being flexible to adjust to altered demands or priorities, admitting errors, and taking advantage of unexpected opportunities. Working memory refers to being able to keep information in mind and manipulate it.

The EFs plays a fundamental role in the self-regulation capacity of the individual (Correia & Navarrete, 2017). Its different components affect the processing of social and emotional information (Van Nieuwenhuijzen et al., 2017). EFs, like inhibitory control, are needed in social activities to perceive the environment, people and emotions. That said, the study involving visual tracking tasks can be developed for evaluation, identifying the way the individual extracts information from the environment, which in turn influences the way they act on this context (Orsati et al., 2008).

Recognizing emotions with precision is an essential aspect of social functioning, bearing in mind that facial expressions are an important indication of emotional state (Orgeta & Phillips, 2007). According to Mancini et al. (2013), the ability to distinguish and interpret emotions from facial expressions is a major component of the nonverbal communication system and a crucial skill for human relationships.

The research found on the subject involves the emotion recognition and inhibitory control in people with Huntington's disease (Hünefeldt et al., 2020), emotion recognition and EFs in bipolar patients (David et al., 2014), emotion recognition, and cognitive flexibility after brain injury (Milders et al., 2008), EFs and emotion recognition in young people as challenging opposition and conduct disorder (Kleine Deters et al., 2020), EFs and emotion recognition in borderline personality disorder (Baez et al., 2015), working memory and recognition of facial expression in patients with Parkinson's disease (Alonso-Recio et al., 2014).

Augusti et al. (2014) evaluated how emotional facial expressions affected working memory in children from 9 to 12 years old. The study revealed that by using the task of operational memory with facial expressions, expressions with negative valence related to negative emotions such as sadness, anger, fear, and disgust do more harm to the working memory than emotions like joy. Morra et al. (2011) investigated the relationship between emotional comprehension, grammatical comprehension, and operational memory capacity in children between 5 and 11 years old, testing the hypothesis that working memory has a role in developing emotional comprehension. The results indicated that working memory capacity plays a decisive role in the transition of understanding emotions. Thus, the development of working memory has a considerable impact on the development of emotional understanding. Rosenqvist et al. (2014) addressed the ability to recognize emotions correlated with all other neurocognitive abilities, such as EFs in children aged 3 to 6. The results indicated that neurocognitive language skills, attention and EFs, and mind theory were significant predictors of emotion recognition ability.

For Rosenqvist et al. (2014), studies that investigate the relationship between emotion recognition and EFs, among them, language, memory, theory of mind or visuomotor functions are still very limited.

Furthermore, no published papers were found that correlate recognition of emotions and PB in the age group of this study, the relationships between these variables are still not well characterized. It is understood that evaluating the difficulties can lead to more adequate clinical evaluations and to an understanding of the recognition of emotion.

Thus, the study has the objective of analyzing the association between the recognition of emotions and the EFs, among them, working memory, inhibitory control and cognitive flexibility in preterm birth and term born (TB) schoolchildren.

This research was characterized as an exploratory and cross-sectional study to explore the descriptive/correlational the performances between the control group (TB) and the clinical group (PB). The hypotheses are that there are differences in EFs and emotion recognition between the groups and association between EFs and emotion recognition.

The call for participation was made utilizing a report in the school agenda. All members of the sample were regularly enrolled in the public-school network. The sample did not include schoolchildren whose parents did not authorize participation or who could not take the tests because of the compromised oral language, speech comprehension, visual acuity, and motor and hearing alterations. All participants presented normal or corrected vision.

In order to analyze the performance of the two groups (clinical and experimental) in the EFs, the number of categories and perseverative responses of the WCST, WISC-IV (Working Memory Index) and the percentages of inhibitory control and flexibility obtained in the FDT test (Table 1), have been utilized.

No significant differences were found among the means. The effect size was considered small or very small, demonstrating that no significant differences between the analyzed groups regarding operational memory, inhibition, and cognitive flexibility were presented.

Regarding the measures of emotion recognition, the clinical group presented a significant difference in the execution time of Phase 4 (p = .028), in which the identification of emotions occurred through excerpts of films (Table 2). PB students had a lower performance in time for the emotion recognition, in which, when compared to the other group, it took longer to finish the phase. Regardless of the absence of statistical significance between the groups in the phases, it is relevant to consider that the averages obtained indicated that the clinical group had a lower performance because they got fewer items right, made more mistakes, and took longer to complete the phases.

Table 1
Comparison of Groups in the Executive Functions indexes

Note p = significance; SD = standard deviation; d = Cohen's D

Table 2
Averages, standard deviation, minimum/maximum, and number of responses in the phases of BACRE-I

Note p = significance; SD = standard deviation

In the analysis of eye tracking during the emotion recognition, the comparison between the groups showed a significant difference in defocusing (p = .002). The clinical group, that is, PB schoolchildren, performed more deviations in eye movement away from the stimulus face while performing emotion recognition.

About the emotion recognition, in the clinical group, the cognitive flexibility had correlation with the execution time in Phase 1 (p = .030, r = .384), Phase 2 (p = .026, r = .0392), Phase 5 (p = .016, r = .422) and with the total time (p = .023, r = .0401). The inhibitory control correlated with Phase 5 in time (p = .027, r = .391), hits (p = .043, r = .360) and total errors (p = .043, r = .360). The operating memory was correlated with the total errors of Phase 2 (p = .037, r = .0370). In the control group the perseverations were related to time (p = .17, r = -.340) and hits (p = .17, r = .340) of Phase 1 (Table 3).

Based on the objectives proposed in this research, the results showed correlations between emotion recognition, operational memory, cognitive flexibility, and inhibitory control in the analyzed groups. However, the correlations are weak, and the more significant correlation found was between cognitive flexibility and Phase 5 (r = .422). Besides that, it is necessary to consider that the sample size is small.

Table 3
Correlation between the groups in the phases of BACRE-I and executive functions

Note p = significance; r = correlation coefficient; SD = standard deviation; WMI = Working Memory Index; IC = Inhibitory control; CF = Cognitive flexibility; NC = Number of categories; P = Perseverations

The main objective of this study was to analyze the association between emotions recognition and EFs, specifically the operational memory, cognitive flexibility, and inhibitory control in PB and TB students.

In the field of EFs, no significant differences were found between the groups, corroborating a study by Loe et al. (2012) and Tavares (2019), in which the performance in EFs was the same both in PB and in the TB. For instance, Jaekel et al., (2016), Aviles et al., (2018), and Basso (2014) found differences in EFs between the groups, in which PB negatively affected inhibitory control skills. In addition, they found that the lower the gestational age of the child, the lower inhibitory control, due to interruption of gestational development. It is believed that the fact that the clinical group sample consisted mostly of moderate to late preterm was related to the fact that the performance of the two groups was similar, with no statistically significant differences, differing two results from other studies. Moreover, to Everts et al. (2019), in PB, the development of EFs occurs in a prolonged way throughout childhood until adolescence, when they reach at least the same level of performance and may improve beyond TB in inhibition and cognitive flexibility.

The performance of the groups in the recognition of emotions obtained in this research corroborated the research by Williamson and Jakobson (2014), pointing out that preterm children had more difficulty identifying emotions correctly. However, Ríos-Flórez and Flóres Barco (2017) found no relation between recognition of basic emotions and PB. However, assessments mainly use two-dimensional facial stimuli, but Wang et al. (2017) indicate that the use of three-dimensional stimuli favors recognition more efficiently and quickly. Bernstein and Yovel (2015) claimed that research should expand to study dynamic stimuli, considering that facial motion rather than static images convey most real-life social interactions. Dynamic displays improve decoding accuracy, have greater ecological validity, and are more suitable for research (Slepian & Carr, 2019).

In eye tracking, preterm students had less focus on recognizing emotions. Loe et al. (2012) obtained the same results in research on EFs, in which the PB showed an impaired capacity to retain fixation during the evaluation. Research by Yaari et al. (2018) indicated that premature newborns looked away to better process emotional information and regulate arousal levels. This same pattern of look deviation in the identification of emotions was evidenced in Fuentes et al. (2018), who sustained that it impacts emotion recognition, considering that the understanding of emotions in the social context provides clues about the present conditions, indicating the directions that the behavior must follow to be socially adequate and have adaptive value. In this way, they convey the emotional state, and the ability to produce and recognize it is an important component of interpersonal communication.

The mentioned data on the correlation between inhibitory control and recognition of facial expressions of emotions agreed with the study by van Rijn et al. (2011). This study correlated the assignment of emotions with inhibitory control, where the difficulty in identifying emotions was related to inhibitory control problems, which influenced the performance of the selection of appropriate social significance, being a possible marker of vulnerability for psychosis. According to Diamond (2013), inhibitory control allows selective participation, focusing on what the individual chooses, and suppressing attention to other stimuli, involving control over behavior and emotions. The lack of inhibitory control leaves the individual at the mercy of impulses, habits of thought or action, and/or stimuli in the environment. Thus, the development of inhibitory control skills is vital for children living in the social environment.

Early identification of inhibitory control difficulties and emotion recognition can be beneficial in targeting children at risk of maladaptive development, and there are many opportunities for intervention during early childhood (Rhoades et al., 2009). Therefore, it is important to identify interventions (Hüning et al., 2017).

The emotion recognition requires operational memory, and these requirements are greater as the number of options to choose from increases. Difficulties in working memory are likely to cause specific problems in tasks of labeling facial expressions of emotion, where participants are asked to make a decision (Phillips et al., 2008). People with greater operational memory capacity are more adept at controlling emotions than others (Schmeichel et al., 2008). Thus, in general, the relevance of EFs is understood, which enables the individual to adapt quickly and flexibly to changed circumstances, maintain focus and face new unforeseen challenges (Diamond, 2013).

The study tried to identify if there was an association between EFs and emotions recognition in the preterm and full-term groups. However, when EFs were associated with emotion recognition, correlations were found, with the highest correlation between cognitive flexibility and Phase 5. The results identified in the study by Erfanian et al. (2018) indicated the relationship between components of EFs and emotion recognition. In other words, working memory is enhanced by improving emotion control, initiating, planning, organizing, and monitoring the amount of emotional recognition. Thus, difficulties in EFs negatively influence the emotion recognition.

The data obtained in the research are important for the planning of interventions and prognosis, considering that it is essential to understand the pattern of preterm child development, considering the results throughout the development so that the use of data with different gestational ages are vital to building this understanding (Silveira & Procianoy, 2019). Understanding the consequences of prematurity and ways to minimize the effects is urgent to promote each individual's quality of life and the repercussions it causes (von Doellinger et al., 2017).

Although the objectives of this study were met, there are some limitations, such as the sample size and the weak correlations found. However, even with the limitations inherent to this research, it is believed that it made it possible to understand the association between EFs and emotion recognition in schoolchildren TB and PB. In future studies, larger and more representative samples are recommended to minimize or even eliminate these limitations.

Citar este artículo como: Dos Santos Telaska, T.; Jaworski de Sá Riechi, T. I.; Mota de Oliveira, T.; Silva, L. & Pereira Bellon, O. R. (2023). Emotion recognition and executive functions in school children born term and preterm. Revista Argentina de Ciencias del Comportamiento, 15(2), 15-25.

https://revistas.unc.edu.ar/index.php/racc/article/view/32788/42477 (pdf)