such that displays of positive affect may allow for modulation of arousal while children remain oriented toward novel social stimuli (Colonnesi et al., 2014; Poole & Schmidt, 2019a; Sroufe & Waters, 1976). In support of this notion, Asendorpf (1990) noted that within a coy smile, gaze aversion tends to occur during the most communicative part of the smile, suggesting that the smile may act as a regulatory mechanism by modulating one’s internal milieu. Moving forward, it would be helpful to determine whether positive and nonpositive shyness are in fact differentially related to level of self‐regulation, and whether individual differences in temperamental self‐regulation influence the development and maintenance of positive and nonpositive expressions of shyness.
Taken one step further, it would be interesting to determine whether different aspects of self‐regulation (e.g., inhibitory control, attentional shifting) work to moderate the association between positive and nonpositive shyness and social behavior or clinical outcomes similarly to when shyness is treated as a homogenous construct. Finally, using evolutionary frameworks such as differential susceptibility to guide future studies and analyses may provide us with valuable information about the multiple contexts that may support adaptive functioning in both positive and nonpositive expressions of shyness (Belsky & Pluess, 2009; see also Schmidt & Miskovic, 2013).
How Are These Self‐Regulatory Mechanisms Instantiated in the Brain in Adaptive Shyness?
Although the origins of shyness are multifaceted, interest in the neurobiological foundations of shyness has received considerable attention over the past several decades (see, e.g., Fox et al., 2001, 2005; Kagan et al., 1987, 1988; Schmidt & Schulkin, 1999, Schmidt & Miskovic, 2013, 2014, for reviews). This has been fostered by the availability of theoretical frameworks for understanding nonhuman animal and human brain‐behavior relations as well as advancements in technologies that have allowed for the relatively noninvasive collection of electrical brain activity such as electroencephalography (EEG). This combination has positioned researchers well to study the neural substrates underlying shyness, and how these neural processes may mediate adaptive and nonadaptive behaviors associated with shyness.
Frontal Brain Asymmetry and Shyness
One of the most widely studied neural correlates of shyness and related phenomena is frontal brain EEG alpha asymmetry. This work is rooted in motivational models of frontal brain activation, which have described resting state frontal brain alpha asymmetry as a trait‐like measure (i.e., a biological diathesis) that is stable across time and context (see Coan & Allen, 2004; Davidson, 2000; Fox, 1991, 1994; Reznik & Allen, 2018, for reviews). According to this framework, greater relative activity in the left frontal brain region is presumed to facilitate approach‐related motivations and emotions such as sociability and happiness, whereas greater relative activity in the right frontal region has been implicated in avoidance‐related motivations and emotions such as shyness and fear (Reznik & Allen, 2018).
Researchers have used EEG‐based data to derive asymmetries of frontal brain activity and the frontal activation motivational model as a theoretical platform to test hypotheses related to individual differences in temperament (including shyness and related constructs) and affective style across development (see Schmidt & Miskovic, 2014, for a review). Typically, these studies examined frontal asymmetry as the difference in EEG alpha power in the right frontal hemisphere minus EEG alpha power in the left frontal hemisphere. Because EEG alpha power is inversely related to cortical activity, negative scores reflect greater relative right frontal brain activity (Tomarken et al., 1992).
During different developmental periods, researchers have provided support for the relation between right frontal asymmetry and social avoidance‐related tendencies. For example, in infants and children, resting right frontal asymmetry has been associated with behavioral inhibition and emotional reactivity (Calkins et al., 1996; Davidson & Fox, 1989; Fox & Davidson, 1987; McManis et al., 2002), which are the temperamental antecedents of shyness. In preschool children, those described as socially inhibited and withdrawn during interactions with peers show right frontal asymmetry at rest (Fox et al., 1996), as do temperamentally shy children (Poole et al., 2018, 2019; Theall‐Honey & Schmidt, 2006). In adults, higher levels of behavioral inhibition, shyness, and social anxiety also have been linked to right frontal asymmetry at rest (Moscovitch et al., 2011; Schmidt, 1999; Sutton & Davidson, 1997) and increases in right frontal brain activity in responses to social stress in adults (Davidson, et al., 2000) and children (Schmidt et al., 1999).
Adaptive Subtypes of Shyness in the Brain
An additional line of our research has been to examine the neural substrates of different subtypes of shyness in children that are presumed to have different adaptive functions. As mentioned earlier in the first section, we have been particularly interested in different subtypes of shyness that share conceptual overlap, such as fearful/nonpositive shyness and self‐conscious/positive shyness, as they appear to have different adaptive functions. We have recently explored each of these two different conceptualizations of shyness in two separate studies to determine whether we could distinguish them on resting brain‐based measures.
In Study 1, we classified children with early‐developing (fearful) shyness and a later‐developing (self‐conscious) 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).
