shyness. We found that children with later‐developing shyness had the highest relative salivary cortisol response (a measure of stress reactivity; Schulkin et al., 2005) in the context of self‐presentation, the highest levels of embarrassment, and the lowest social skills according to parent‐ and teacher‐report, whereas children with early‐developing shyness displayed the highest relative resting right frontal brain asymmetry (a neural correlate of fear and avoidance) relative to the other groups (Poole & Schmidt, 2019c). In line with Buss’ (1986a,b) hypotheses, this provides partial support that early‐developing shyness may be maintained by a sensitivity toward experiencing fear, whereas later‐developing shyness may be more closely related to self‐conscious emotions.
In Study 2, we examined resting state EEG measures in children with positive shyness, nonpositive shyness, and low overall shyness. We operationalized positive shyness as the display of shy behavior (e.g., avoidance) and positive affect (e.g., smiling), whereas nonpositive shyness is the display of shy behavior without positive affect (Poole & Schmidt, 2019a, 2020a). As mentioned above, positive shyness has been regarded as an adaptive, approach‐dominant subtype of shyness (see Poole & Schmidt, 2020b, for a recent review).
Similar to Study 1, we first examined resting state frontal EEG asymmetry among children classified as positive shy, nonpositive shy, and low shy (Poole & Schmidt, 2020a). Our results revealed that children classified as nonpositive shy displayed greater relative resting right frontal EEG activity, whereas children classified as positive shy and low shy displayed greater relative resting left frontal EEG activity (a neural correlate of approach). These findings converge with studies that have examined psychosocial correlates of approach‐avoidance in these subtypes, extending this work to a neural measure. It may be the case that children who display more positive shyness exhibit an underlying biological diathesis for approach as reflected by greater relative left frontal brain activity at rest, which could facilitate approach behaviors in social situations and yield the benefits of such social interactions, including social engagement and competence.
In Study 2, we also examined frontal EEG delta‐beta correlation among these shyness subtypes (Poole & Schmidt, 2020a). Delta‐beta correlation is thought to reflect the efforts of regulatory networks to down regulate arousal in the subcortical networks (Knyazev & Slobodskaya, 2003; Schutter & Knyazev, 2012) and thus some researchers have conceptualized delta‐beta correlation as a proxy for adaptive emotion regulatory abilities. Our results revealed a relatively higher frontal delta‐beta correlation among the positive shy children compared to the nonpositive shy and low shy children (Poole & Schmidt, 2020a). As stated above, positive shyness is hypothesized to emerge from the simultaneous feelings of arousal and regulation in social situations (Colonnesi et al., 2014; Colonnesi et al., 2017; Nikolić et al., 2016; Poole & Schmidt, 2019a), and thus it is possible that the positive shy children display greater synchrony of delta and beta oscillations as reflected by stronger delta‐beta correlation due to their efforts to regulate feelings of arousal.
Frontal Brain Maturation and Adaptive Shyness
In order to further understand the adaptive function of shyness, we recently have begun to investigate whether frontal brain maturation may be related to shyness in childhood given that the frontal cortex is involved in the regulation of behavior (Fox, 1994; Passler et al., 1985) and delays in frontal maturation have been linked to a range of childhood behavioral and regulatory problems (e.g., Dawson & Fischer, 1994). One way to measure frontal brain maturation is to examine the development of EEG spectral power (Thatcher, 1991). The development of spectral power in faster frequencies (e.g., alpha) is thought to reflect increased brain maturation of the cerebral cortex, and increases in EEG power in these faster frequencies have been related to regulatory functions (Bell & Wolfe, 2007; Clarke et al., 2001). In infants and young children, there is more spectral EEG power at slower frequencies (e.g., delta) relative to faster frequencies in absolute terms and, with age, delta occupies less power, whereas alpha occupies more power in the overall power spectrum (Clarke et al., 2001; Marshall et al., 2002). Accordingly, increases in the ratio of alpha to delta power (i.e., alpha/delta ratio [ADR]) may reflect an increase in the proportion of alpha to delta power and a proxy of brain maturation.
Using this idea as a guiding framework, we have examined the ADR score in relation to shyness during early (Schmidt & Poole, 2018) and late (Schmidt & Poole, 2020b) childhood in three separate studies. In Study 1 (Schmidt & Poole, 2018), six‐year‐old children had resting state EEG collected across four repeated assessments separated by approximately six months. We examined how maternal‐reported shyness predicted the trajectory of ADR across the repeated assessments spanning age six to eight years. We found that low shy and high shy children exhibited a similar ADR ratio score at enrollment. However, we found that low shy exhibited the expected linear increases in ADR across visits, whereas high shy children failed to show significant increases in ADR across visits.
We sought to replicate these findings in a separate study using an independent sample of older children (age 10 to 16 years). In Study 2 (Schmidt & Poole, 2020b), we derived latent classes of observed shyness across two visits spanning approximately one year and examined if they were distinguishable on frontal ADR that was collected using EEG at enrollment. Consistent with findings in younger children (i.e., Study 1), we found that children who displayed stable‐low levels of observed shyness showed a significantly higher frontal ADR score relative to children who showed stable‐high levels of observed shyness.
In Study 3 (Schmidt & Poole, 2021), we examined the specificity of frontal ADR in relation to the positive and nonpositive shyness subtypes and a low shy group used in the Poole and Schmidt (2019b) study described above. We found preliminary evidence of a linear relation between frontal ADR score and shyness group in children, such that the positive shy group had the lowest ADR score, the low shy group the highest ADR score, and the nonpositive shy group was intermediate between the two former groups, suggesting possible differences in frontal brain maturation for some adaptive aspects of shyness.
In interpreting these findings, we have speculated two possible explanations (Schmidt & Poole, 2018, 2020b). One is a proximate explanation. That is, the pattern of less growth in the proportion of relative alpha power to delta power among shy children might reflect a neural mechanism underlying dysregulation of emotion regulatory processes in social situations, which is characteristic of some shy children. Previous work has reported that delayed frontal brain maturation may underlie some emotional and behavioral problems that are related to shyness in children (see, e.g., Dawson & Fischer, 1994; Posner & Rothbart, 2000; Schore, 1996; for reviews).
A second is an ultimate explanation. That is, delayed frontal brain maturation might reflect individual differences in the evolutionary process of neoteny. Neoteny refers to the prolongation retention of childhood characteristics and delayed maturity (Bogin, 1990; Gould, 1977, 2008). Unlike most mammals, human development is characterized by a relatively long period of childhood. This protracted period is presumed to have played a critical part of human evolution, allowing our brains to grow larger and allowing for the development of higher order cognitive processes (Bogin, 1990). Neoteny has been hypothesized as an important element to social cognitive development in humans in that one of the presumed functions of extending childhood is to allow additional time for learning to take place when the brain is highly plastic (Bjorklund, 1997, 2009; Gallese, 2017). Interestingly, there is empirical evidence for neoteny in the human brain (Somel et al., 2009), particularly the prefrontal cortex (Petanjek et al., 2011).
We have speculated that shyness may have evolved due to individual differences in frontal brain maturation, resulting from the process of neoteny (see Schmidt & Poole, 2019, for a review). The function of delayed frontal brain maturation, manifesting as an approach‐avoidance conflict in social situations, may actually allow the shy child additional time for learning of others' intentions before socially participating. Indeed, as noted earlier, expressions of positive shyness have been associated with more sophisticated Theory of Mind in two separate studies of children (Colonnesi et al., 2017; MacGowan et al., 2021). This additional time for learning others' intentions is important for negotiating familiar and unfamiliar social environments. Interestingly, perhaps the social immaturity (Rubin & Asendorpf, 1993),