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), and delayed onset of some developmental milestones in shy children (Caspi et al., 1988) reflect the process of neoteny. We speculate that the delaying of brain maturity, particularly in the frontal brain regions, may be a neotenous feature present in some shy individuals, which serves as a putative mechanism linking shyness and adaptive behavior.
Although it is difficult to empirically test ultimate and evolutionary explanations of behavior, as reviewed in the series of EEG studies above, we have begun to explore the proximate explanation using EEG measures to index brain maturation and emotion regulatory processes underlying adaptive shyness. We have also recently begun to explore more proximate hypotheses of the adaptive nature of shyness by examining adaptive processes in the shy brain using perceptual tasks. Here we adapt shy individuals to affective faces varying in emotional expressions and examine their corresponding afterimages to that particular emotion. For example, after adapting to a positive facial expression (e.g., happy faces), the typical visual afterimage that follows is to perceive a negative facial expression (e.g., angry face), while after adapting to a negative facial expression (e.g., angry face), the typical visual afterimage that follows is to perceive a positive facial expression (e.g., happy face). However, there appear to be individual differences in the experience of these afterimages. We found that young adults who had high levels of both shyness and sociability were more likely to perceive a negative face emotion afterimage after adapting to happy faces and a positive face emotion afterimage after adapting to angry faces than young adults classified by other combinations of high and low shyness and sociability (Poole et al., 2020). These findings suggest that the experiences of these afterimages appear to be linked to personality and may be a window into understanding individual differences in how well the brain adapts to social stimuli, with some shy subtypes possibly showing an advantage in adapting to these social stimuli.
Future research could test the proposed shyness‐neoteny hypothesis in several ways (see Schmidt & Poole, 2019). First, if there are indeed maturational delays associated with some types of shyness, then perhaps these delays would be evidenced on epigenetic markers of aging, which could be examined. Second, to the extent that neoteny may have allowed for prolonged learning to take place, then there may be differences in learning and memory among some types of shyness in different social contexts that could be examined. Lastly, the shyness‐neoteny hypothesis could be tested between the sexes for preferences across a range of stimuli, for example, people expressing neotenous features (e.g., coyness, youthful smiles) and characteristics of some
