The aim of this study was to examine the neural correlates of facial affect processing across this sensitive period of adolescent socioemotional development by using a highly ecologically valid stimulus set and paradigm (assessing implicit regulation of dynamic adolescent expressions) in a healthy sample of 10–23 year-old females. Consistent with prior studies that employed various emotion regulation paradigms (Lieberman et al., 2007; McRae et al., 2012; Ochsner et al., 2009; Pitskel et al., 2011; Silvers et al., 2015), our novel peer dynamic stimulus set reliably and robustly recruited key neural regions involved in the network of emotion reactivity (MOFC/vMPFC, bilateral amygdala) and regulation (bilateral dorsal and ventral LPFC). These data suggest that viewing peer faces (compared to labeling) was associated with heightened MOFC/vMPFC activity, while labeling peer faces (compared to viewing) was associated with heightened activity in bilateral ventral LPFC and bilateral dorsal LPFC as well as left amygdala. However, in our cross-sectional study spanning most of adolescence, none of our a priori regions of interest (MOFC/vMPFC, amygdala, dLPFC, and vLPFC) demonstrated the age-related trends in activity to dynamic peer faces that could be expected by extending imbalance models to the affective domain. These findings suggest that the field’s characterization of sensitive periods in socio-affective neurodevelopment may be highly influenced by the particular stimuli and paradigms used. In particular, when using stimuli and paradigms that may be more socially salient (peer faces) and ecologically valid (dynamic expressions and implicit regulation), the neurodevelopmental trends in emotional reactivity and regulation may vary from commonly assumed patterns derived from applying dual systems or imbalance models to the affective domain.
Current neurodevelopmental models posit that changes in amygdala and prefrontal function – or in their connectivity (Casey, 2015) – underlie changes in affective responding in childhood and adolescence (Casey et al., 2008; Ernst et al., 2006). Such models are bolstered by a rich body of animal work demonstrating developmental changes in prefrontal-amygdala dynamics (Bouwmeester et al., 2002a,b; McCallum et al., 2010; Pattwell et al., 2012), as well as extensive adult neuroimaging research linking the amygdala and prefrontal stearoyl-coa desaturase to a host of emotional processes (Buhle et al., 2014; Costafreda et al., 2008; Kober et al., 2008). However, there is also emerging evidence that the amygdala does not exclusively respond to aversive, or even affective stimuli (Cunningham and Brosch, 2012). As such, it is possible that developmental changes in amygdala and prefrontal function are related not only to emotional development, but also to a broader set of developmental processes (e.g., salience processing, social appraisals) (Pfeifer and Blakemore, 2012; van den Bulk et al., 2013). The present study sought to examine two non-competing possibilities for how amygdala and prefrontal function relate to general and affect-specific changes in development.
The first possibility was that age would predict general changes in the way individuals respond to both negative affective and neutral stimuli. Specifically, it was hypothesized that age would be associated with diminished engagement of subcortical systems like the amygdala which has been broadly implicated in responding to motivationally salient (Cunningham and Brosch, 2012), intense (Anderson et al., 2003), and emotion-eliciting – both positive and negative (Breiter et al., 1996) – stimuli (Costafreda et al., 2008). A sizeable body of neuroimaging work suggests that amygdala responses to aversive stimuli including fearful faces and emotionally evocative scenes are elevated in childhood (Gee et al., 2013; Silvers et al., 2015) and adolescence (Guyer et al., 2008; Hare et al., 2008; Monk et al., 2003; Passarotti et al., 2009) and decrease in adulthood. However, the evidence that age-related changes in amygdala responses are emotion-specific is more mixed (Helfinstein and Casey, 2014). Indeed, neuroimaging studies have revealed age-related decreases in amygdala responding for neutral (Forbes et al., 2011; Thomas et al., 2001), positive (Vasa et al., 2011), or a combination of different types of stimuli (Hare et al., 2008; Swartz et al., 2014; Vink et al., 2014). This suggest that perhaps children interpret a broader variety of affective and neutral stimuli as being salient or personally relevant than do adults and thus show elevated amygdala responses for both aversive and non-aversive stimuli. Among studies that have specifically examined age-related effects in the amygdala for aversive stimuli, most have focused on contrasts between aversive stimuli and fixation (Gee et al., 2013), or, in the case of our own work, on the effects of different regulatory conditions on responses to aversive stimuli (Silvers et al., in press; Silvers et al., 2015). While such approaches are useful for characterizing changes in amygdala function in affective contexts, they do not address whether or not such age-related changes are unique to affective contexts. As such, this prior research leaves open the possibility that the amygdala shows general, rather than negative affect-specific, age-related decreases in responding.