Discussion
Previous experiments investigating adolescent decision making under risk have demonstrated adult-like risk-attitudes in laboratory settings on one hand (Steinberg, 2004, 2008; Boyer, 2006; Reyna and Farley, 2006; van Leijenhorst et al., 2008) and risk-seeking attitudes in the presence of peers on the other (Gardner and Steinberg, 2005). We hypothesized that these seemingly opposing results are suggestive of a generalized sensitivity to the demands of social context that can explain commonly observed increases in conformity during adolescence (e.g. Berns et al., 2010). This hypothesis suggests that arousing advice provided by peers and real-life settings can lead to enhanced risk-taking, while risk-averse advice commonly provided by adults can lead to decreased risk-taking. We therefore investigated developmental effects of a specific risk-averse social context, provided by advice from an expert economist, on risky decision making across three age groups.
Behavioral results indicate, in agreement with our hypothesis, that advice had the greatest impact on risk-taking of EAs and LAs compared to ADs. Neuroimaging results demonstrate that the effect of advice was mediated by modulating activity in DLPFC. The effect of advice within this brain region was such that it underlined the salience of safe choice options in adolescents by specifically enhancing the correlation strength between brain activity and valuation parameters reflective of safe choice options. Taken together with prior research implicating DLPFC in behavioral control and suppression of emotional impulses (Knoch et al., 2006; Delgado et al., 2008a; Hare et al., 2009), these results are suggestive of advice modulating relevant cognitive and affective processes involved in decision making by influencing activity in lateral prefrontal cortex, a region that is known to undergo significant structural and functional developmental changes during adolescence. Our results, together with previous reports on adolescent decision making (e.g. Gardner and Steinberg, 2005; Berns et al., 2010), therefore suggest that risk attitude during adolescence is influenced by demands made by a particular social context.
Employing a behavioral model grounded in CPT, we observed that advice had a significant impact on risk-taking across all age groups, such that its presence produced more risk-averse behavior. Advice significantly decreased risk-taking for high-probability gambles in both adolescent groups compared to ADs, such that adolescents showed a significant change in the curvature of w(p), changing from an S-shaped curve previously observed in adolescents (Harbaugh et al., 2002), to an inverted S-shape commonly observed in adults (e.g. Tversky and Kahneman, 1992; Gonzalez and Wu, 1999), which produced risk-averse CEs. These results demonstrate that expert advice significantly reduced risk-taking in both adolescent groups relative to ADs. Indeed, in the presence of advice, more adult-like risk attitudes were observed in adolescents, suggesting that risk-averse advice can significantly affect adolescent behavior, when it comes from an adult.
Functional magnetic resonance imaging results support our main hypothesis that advice can have a significantly greater modulatory impact on adolescent, compared to adult brain systems relevant for integrating the advice in the decision process. Developmental differences in the recruitment of neural valuation mechanisms were obtained mainly in the presence of advice in regions implicated in cognitive control, behavioral inhibition and emotion regulation, such as dorsolateral and ventrolateral PFC (Delgado et al., 2008b; Koechlin et al., 2003), reward-processing, such as vmPFC and medial OFC (e.g., Grabenhorst and Rolls, 2011), as well as social cognition, such as posterior TPJ (e.g., Saxe and Kanwisher, 2003). Importantly, the effect of advice was specific in adolescents, such that it led to an increase in correlation strength of BOLD with risk-averse valuation parameters. Given the risk-reducing effect of the advice on behavior in adolescents, combined with a specific modulatory impact on neural correlates of valuation, we conjecture that expert advice operates by enhancing inhibitory processes in adolescents, leading to a more deliberative decision strategy.
A number of previous observations support this conjecture. Previous research has demonstrated delayed development within prefrontal systems implicated in cognitive control and behavioral inhibition relative to neural systems involved in affective processing (Casey et al., 2005; Blakemore, 2008; Galvan, 2010). Functionally, such delayed development is commonly reflected by an increased engagement of cognitive control regions, such as DLPFC, with age in a variatey of cognitive and social choice tasks (e.g. Crone et al., 2006; Guroglu et al., 2011; van den Bos et al., 2011). Interestingly, a similar developmental pattern has been observed in TPJ, such that increased recruitment is observed with age in the context of social tasks (e.g. Guroglu et al., 2011; van den Bos et al., 2011; see also Blakemore, 2008). This developmental pattern has been interpreted to reflect a growing ability to engage cognitive and inhibitory control (Bunge and Wright, 2007; Crone, 2009), as well as social cognition (Blakemore, 2008; but see Poldrack, 2010). Our results support and extend this notion by demonstrating that social context generated by an adult advisor can lead to the expression of adult-like behavior in adolescents via enhancing activation patterns within cognitive control regions in the context of a task that requires both mentalizing and suppression of prepotent behavior (Engelmann et al., 2009a). Finally, a number of recent fMRI studies investigated the influence of advice on neural correlates related to valuation and learning (Behrens et al., 2008; Biele et al., 2011; Klucharev et al., 2008). Biele et al., (2011) examined the effect of advice on outcome-related signals in the context of a reward-based decision-making task. Results demonstrated modulations of BOLD activity after following advice in a network of regions including the septal area, caudate nucleus and vmPFC. Here we show that advice can also modulate value-related signals in vmPFC and DLPFC during the choice period, but that the extent of such modulation depends on developmental stage. A neuroimaging study by Klucharev et al. (2008) investigated expert influences on memory of and attitude toward products. Their results demonstrated that a single pairing of a picture depicting a product with a photograph depicting a celebrity perceived as an expert for a given product category enhances: (i) subsequent recall and (ii) positive attitude toward products (Klucharev et al., 2008). Interestingly, the attitude enhancing effect of celebrities judged to be experts in a given product category was mediated by elevated activity in caudate nucleus. Results from the current investigation confirm and extend these findings by demonstrating developmental differences in brain signals reflective of subjective value during choice in bilateral caudate nucleus (see Supplementary Figure S6).
A few limitations should be mentioned. We employed an adult expert as our treatment across all age groups, which may confound age status with expertise in the current investigation. This was done because an actual person was chosen to function as advisor to create a naturalistic experimental setting and, additionally, his long list of accomplishments in the fields of economics and finance was presented to participants in detailed instructions to provide trustworthy advice in the treatment condition (see Engelmann et al., 2009a for further details). Since such accomplishments could not have been accumulated by an adolescent advisor, an adult expert was used across all age groups. Finally, age groups were not matched by gender in the current investigation.
Taken together, the current pattern of results provides evidence demonstrating that, across development, different brain systems mediate the risk-reducing effect of advice during decision making under risk. Specifically, advice modulated activity in vmPFC in adults, while in adolescents, advice modulated brain responses related to valuation in DLPFC. Based on these results we propose that the risk-reducing effect of the social context on behavior in adolescents operates via valuation-specific enhancements of inhibitory and cognitive control processes that lead to a more deliberate decision strategy. To our knowledge, this is the first neurobiological study of the mechanisms whereby advice from an authority figure affects risky choices differentially across development. Despite previous reports questioning the efficacy of interventions for reducing dangerous behaviors among adolescents (Steinberg, 2008), our results indicate that advice from an authority figure or more specifically risk-averse advice, can effectively reduce risk-seeking choices in adolescents. However, because during key moments in adolescent life, advice is likely provided by peers, an important goal of future investigations is to examine whether such intervention methods would maintain their efficacy within social contexts that favor risk-seeking behavior, such as the presence of peers.