Neural mechanisms underlying trust to friends, unknown peers, and community members: A cross-sectional fMRI study to trust in adolescence
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Description: Adolescence is an important transition period from childhood to adulthood, in which individuals develop into contributing members of society (Crone & Dahl, 2012; Fuligni, 2019, 2020). One of the fundamental tasks during adolescence is to develop mature social relationships and societal values (Crone & Fuligni, 2020). Here, trust plays an important role. Defined as decisions favoring other individuals’ outcomes aiming at future cooperation and self-gain (Lahno, 1995), trust is one of the crucial building blocks in successfully developing social relationships (Burke et al., 2020; Crone et al., 2022; Crone & Dahl, 2012). Trust requires advanced levels of perspective taking and strategic thinking, which are processes that show continued development across adolescence (Dumontheil et al., 2010). The Trust Game is an experimental paradigm in which individuals can trust a certain number of resources (e.g., coins) to another individual (the trustee), after which those resources are increased. The trustee then has the power to either reciprocate (share the resources) or defect (keep resources for self). Prior developmental studies found age-related increases in trust between childhood and adolescence (Sutter & Kocher, 2007; van den Bos et al., 2010, 2011). However, other studies showed a general stability in trust (Fett, Shergill, et al., 2014; Güroğlu et al., 2014; Lemmers-Jansen et al., 2017; van de Groep et al., 2018). The exact developmental patterns of trust, particularly during adolescence, seem highly dependent on social contextual factors (i.e., risk for the trustor; van de Groep et al., 2018) and the behavior of the trustee in a multiple rounds Trust game or in daily life (Fett, Shergill, et al., 2014; Güroğlu et al., 2014). For example, Güroğlu et al. (2014) demonstrated that adolescents showed higher levels of trust to friends than to unknown others. However, less is known about the development of trust to societal targets, such as members of a community organization. Given that a key developmental challenge of adolescence is to develop into a contributing member of society (Fuligni, 2019), it is important to investigate adolescents’ trust to not only close (e.g., friends) but also to societal targets (e.g., community members). In a pilot study on adolescents’ trust and reciprocity (Sweijen et al., 2022), we recently discovered that adolescents trust community members less than friends but more than unknown peers. We discovered that general contributions to society and interpersonal trust beliefs were positively related to trust and reciprocity, whereas other individual differences measures (i.e., emotional support to friends and attending to other’s emotions) were not. However, the exact mechanisms which contribute to trust and reciprocity, and whether this differs for various targets, remain unknown. While previous studies give us insights into the development of target differentiation in trust choices across adolescence (Fett, Shergill, et al., 2014; Güroğlu et al., 2014; Sweijen et al., 2022), the underlying mechanisms remain unknown. Functional neuroimaging studies can shed light on the underlying processes of trust choices, and whether this is dependent on the target to which trust is shown. Given the additional socio-cognitive demands needed in the interaction between the trustee and trustor (Rilling & Sanfey, 2011), trust may be associated with flexible recruitment of brain areas underlying socio-cognitive developmental processes (Burke et al., 2020; Crone et al., 2022). This social brain network includes the anterior cingulate cortex (ACC), medial prefrontal cortex (mPFC), temporal parietal junction (TPJ), and precuneus (Blakemore, 2008; Crone & Dahl, 2012). Because trust involves responding to the needs and perspectives of others (Crone & Fuligni, 2020), mentalizing (i.e., the ability to understand the mind of one’s own and other individual’s) may be a potential mechanism associated with trust choices. Several brain regions have been associated with individual differences in mentalizing, including the mPFC and TPJ (Blakemore & Mills, 2014; Frith & Frith, 2012; Lieberman, 2007). Indeed, studies using the Trust Game showed that young adults engage these brain regions such as the mPFC during trust choices (Cutler & Campbell-Meiklejohn, 2019; van den Bos et al., 2009). However, a recent study with young adolescents found no increased activity in the mentalizing related areas TPJ and mPFC (Sjitsma et al., 2020). Moreover, previous developmental studies showed age-related increases in activity in these regions, which are argued to be related to advancing mentalizing skills across adolescence (Fett, Gromann, et al., 2014; Fett, Shergill, et al., 2014; Lemmers-Jansen et al., 2017; van den Bos et al., 2011). Together, these studies suggest that brain areas related to mentalizing may be involved in processing trust choices to other individuals, but prior studies did not consistently test this in a design in which trust choices were manipulated. While we expect that a key process is reserved for the mentalizing brain network during trust, reward processing and cognitive control are also expected to play an important role during trust choices. That is, the reward network, which includes the orbitofrontal cortex (OFC) and ventral striatum (i.e., caudate, putamen, and nucleus accumbens; Delgado et al., 2005; Fett, Gromann, et al., 2014; Lemmers-Jansen et al., 2017; van den Bos et al., 2009), is involved in an individual’s motivation to cooperate with others (Declerck et al., 2011; King-Casas et al., 2005). For example, Fett et al. (2014) found increased activity in social reward-related areas during trust choices. The authors reported that age was positively associated with the posterior cingulate/precuneus and negatively associated with the OFC, left and right caudate nucleus, and bilateral PFC, possibly reflecting an increased sensitivity towards social signals. These findings are in line with those from another study showing increased activity during trust choices in the right caudate (Lemmers-Jansen et al., 2019). In addition, cognitive control also plays an important role in the motivation to cooperate (Declerck et al., 2011), such that individuals rely on the cognitive control network while regulating self-oriented impulses involved in trust choices. Cognitive control has been associated with age-related increases in the ACC and dorsolateral PFC (dlPFC) related to trust (Fett, Gromann, et al., 2014; Lemmers-Jansen et al., 2017; van den Bos et al., 2009). However, the question remains whether the neural correlates of trust choices differ for various targets. It is suggested that brain areas involved in mentalizing (i.e., mPFC, TPJ, precuneus) are modulated by the relationship with the other individual, because previous studies found that prosocial choices involving liked compared to neutral or disliked others were associated with increased activity in these brain areas (Güroğlu et al., 2008; Schreuders et al., 2018). Moreover, Telzer et al. (2011) demonstrated increased activity in regions involved in mentalizing during prosocial decisions about specific others who are viewed as similar or close to oneself, such as family members. Similarly, prior studies using giving paradigms have shown that the neural correlates of differentiating between close and societal targets are distinct. These developmental studies demonstrated increased activity in adolescents in the anterior intraparietal lobe (IPL), TPJ, putamen, and right lateral PFC (lPFC) during giving to friends compared to unfamiliar peers, as well as age-related increases in activity in the lPFC when giving to others (Schreuders et al., 2018, 2019; van de Groep et al., 2020, 2022). The authors suggest that this increased neural activity to friends relative to unknown peers possibly reflects increased perspective-taking, often referred to as cognitive empathy (van den Bos et al., 2010). Whereas these studies using giving paradigms show partly separable neural mechanisms underlying decisions for self and others, trust is a more complex behavior that relies on additional social consideration processes, such as reputation effects (Rilling & Sanfey, 2011). As such, the question remains whether target differentiation for this more complex behavior relies on the same neural substrates. Previous studies, in which participants played Trust Games with trustworthy and untrustworthy counterparts, demonstrated age-related decreases in activity in the OFC and caudate (Fett, Gromann, et al., 2014) and in the anterior mPFC (van den Bos et al., 2011) during interactions with trustworthy individuals. Furthermore, age-related increases in TPJ activity when interacting with untrustworthy individuals were found to be associated with age-related decreases in trust choices (Fett, Gromann, et al., 2014; Lemmers-Jansen et al., 2017). Based on prior studies using giving paradigms and Trust Games, preliminary evidence exists on the distinct neural correlates of prosocial decisions to close and societal targets. However, these studies mainly focused on these decisions for close others, such as friends and strangers, and trustworthy and untrustworthy individuals. Because adolescents also develop relations with targets outside their friends and family networks (Fuligni, 2019), it is important to investigate these neural mechanisms underlying trust choices to societal versus close and unknown others. However, it remains unknown whether distinct neural mechanisms underly trust and reciprocity towards community members, with whom individuals have no interpersonal relationship. Using a modified version of the Trust Game (Berg et al., 1995; Güroğlu et al., 2014; Sweijen et al., 2022), the main aim of the current study is to examine the neural correlates underlying trust choices to close, unknown, and societal others during adolescence. That is, we aim to examine the neural activity of the social brain networks (specifically, (a)mPFC, TPJ, precuneus, OFC, ventral striatum, dlPFC, IPL, and ACC) in relation to trust directed at close (i.e., friends), unknown (i.e., unknown peers), and societal (i.e., community members) others in adolescence. In addition, we aim to investigate both linear and nonlinear developmental trajectories in trust choices (van den Bos et al., 2010).