Stress and working memory in children and adolescents: Insights from a multisystem approach
Introduction
Working memory (WM) is a cognitive system that supports active integration, computation, and manipulation of information for brief periods of time (e.g., Miyake & Shah, 1999). Given its multifaceted nature, it is unsurprising that WM underlies performance across a range of cognitive tasks, including reading abilities (e.g., Swanson, 1994), reasoning (e.g., Kyllonen & Christal, 1990), mathematics (e.g., Bull, Espy, & Wiebe, 2008), and other processes critical to complex cognitive activities. Indeed, WM is widely considered to be a core indicator of learning capacity, and considerable research has been devoted to identifying predictors of WM, particularly across childhood when learning capacity is key to a range of academic and professional outcomes.
One potential predictor of WM that has been widely studied in adults is stress levels during a WM task. Studies have manipulated stress pharmaceutically or via exposure to psychological stressors such as the Trier Social Stress Test (TSST; Kirschbaum, Pirke, & Hellhammer, 1993), a well-validated laboratory stress induction task that involves giving a speech and performing mental arithmetic in front of neutral evaluators. During such studies, measures of behavioral and physiological arousal are often collected; saliva samples, for instance, are assayed for cortisol to index activation of the hypothalamic–pituitary–adrenal (HPA) axis and for salivary alpha-amylase (sAA) to index activation of the sympathetic nervous system (SNS). Results suggest that stress impairs WM (see Shields, Sazma, & Yonelias, 2016, for a review), with the magnitude of the stress response being proportional to the severity of WM impairment (e.g., Duncko, Johnson, Merikangas, & Grillon, 2009). Mechanistically, the effect may be due to stress-consuming resources in neural regions involved in WM that would otherwise be available to engage in the WM task (attentional control theory; Eysenck, Derakshan, Santos, & Calvo, 2007).
Some research on stress and WM in children also exists. Most such research, however, has focused on the relations between chronic stress (e.g., prolonged adversity), rather than acute stress (e.g., Berry, Blair, Willoughby, & Granger, 2012), and WM. Among the few studies that have investigated acute stress and WM in children (de Veld et al., 2014, Quesada et al., 2012), results diverge from those observed in adults. Quesada et al. (2012), for example, had 8- to 10-year-olds complete a developmental version of the TSST (TSST for Children [TSST-C]; Buske-Kirschbaum et al., 1997) or control activity followed by a WM test. Compared with children exposed to the control activity, children exposed to the TSST-C displayed higher arousal (increased salivary cortisol and sAA) but did not differ in WM performance. de Veld et al. (2014) similarly reported no significant differences in 9- to 11-year-olds’ WM on a task completed after exposure to the TSST-C or a control activity. Nor did any significant associations emerge between the magnitude of children’s cortisol and sAA responses to the TSST-C and their WM performance.
Despite these two studies suggesting that acute stress is unrelated to WM in children, several key questions remain. The first concerns the age differences of the participants. Children in both studies were between 9 and 11 years of age. This narrow span might not adequately capture developmental changes, including notable neurocognitive processes and stress-related reactivity that have implications for how youths respond to stressors and how those responses relate to WM (Somerville, Jones, & Casey, 2010). Children are, for example, less sensitive to social evaluation than adolescents and adults and so might not respond as vigorously to procedures such as the TSST-C (Blakemore, 2008). Including a wider age range would allow for clearer insight into whether the negative effects of stress on WM with adults are mirrored in youths of different ages.
Second, only de Veld et al. (2014) assessed the direct and interactive associations between HPA- and SNS-induced arousal and WM. Joint activation of both systems predicted performance on a memory retrieval task but was unrelated to WM performance. Given the regulatory function of HPA axis activation following SNS activation, concurrent activation of the two systems during the WM task should lead to the most consistent and noticeable negative associations between stress and performance, as found in adults. Further tests of potential interactive links, therefore, are warranted.
Third, measurement sensitivity may be important. The backward span task included in Quesada et al., 2012, de Veld et al., 2014 primarily assesses WM storage capacity. However, WM includes simultaneous storage and regulation of information (i.e., integration, computation, and manipulation). Other WM tasks that capture both processes may have greater construct validity and measurement sensitivity than those that capture only storage (Jaeggi, Buschkuehl, Perrig, & Meier, 2010). The n-back is one such measure. An accuracy score captures overall WM function by assessing storage and inhibitory control, whereas a false alarm (FA) score captures the inhibitory control facet of WM by quantifying the tendency of incorrectly identifying nontargets as targets (Jaeggi et al., 2020). The link between stress and inhibitory control is underexamined, and there is no consensus regarding whether acute stress impairs inhibitory control in adults (Shields et al., 2016). To our knowledge, no study has examined associations between acute stress and inhibitory control in youths. Such an investigation, however, would be extremely valuable in providing a more nuanced understanding of potentially varying effects of stress on different facets of WM processes.
The purpose of the current study was to address these very issues and provide additional insight regarding how acute stress relates to WM processes across development. To induce arousal, 8- to 15-year-olds completed the TSST–Modified (TSST-M; Yim, Granger, & Quas, 2010), during which repeated saliva samples were collected and later assayed to index HPA axis (cortisol)- and SNS (sAA)-driven arousal. Immediately afterward, youths completed the n-back task. Accuracy and FA scores were calculated. We hypothesized that (1) negative associations would emerge between arousal and n-back accuracy, with this association being more pronounced with age, and (2) joint activation (i.e., concurrent arousal of the HPA axis and SNS) would be more negatively related to n-back accuracy than activation of one system. Finally, we made no a priori predictions about arousal and n-back FA scores, although we explored these relations directly and in conjunction with age.
Section snippets
Participants
A total of 104 8- to 15-year-olds (M = 11.63 years; 48.1% female) from a large suburban area served as participants. Ethnicities included Caucasian (80%), Asian (13%), and multiethnic (7%) youths. Annual household incomes ranged from $30,000 to more than $200,000. Data from 9 youths were dropped because they did not finish the TSST-M, because the saliva assays were problematic, or because of WM administrative error. Our final sample included 95 youths.
Materials and procedure
Parents were recruited via a database of
Results
Preliminary analyses revealed no gender differences in age, reactivity, or WM performance (ts < |1.23|, ps > .05), and income (scale responses) was not related to reactivity or WM. Gender and income are not considered further. Descriptive statistics and correlations among study variables are presented in Table 1. All variables were normally distributed except accuracy (negatively skewed and leptokurtotic). Although squaring the scores normalized the distribution, substituting transformed scores
Discussion
The purpose of the study was to investigate acute stress and WM associations in youths across development. We tested whether these relations varied as a function of age or concurrent versus independent activation of the HPA axis and SNS. Lastly, we explored whether associations between stress and WM differed when only the inhibitory control facet of WM processes was considered. Findings partially supported expectations but also revealed nuanced patterns, suggesting that the links between acute
Acknowledgments
This study was supported by funding from the National Institute of Child Health and Human Development (HD087685) and the National Science Foundation (LSS1921187) to J.A.Q.
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