Elsevier

Hormones and Behavior

Volume 64, Issue 2, July 2013, Pages 333-342
Hormones and Behavior

Review
Adolescent cognitive control and reward processing: Implications for risk taking and substance use

https://doi.org/10.1016/j.yhbeh.2013.02.008Get rights and content

Abstract

Adolescence is a unique, transitional period of human development. Once hallmark of this period is progressive improvements (relative to children) in cognitive control, core mental abilities enabling the ‘top-down’, endogenous control over behavior. However, as adolescents transition to more mature (adult) levels of functioning, limitations still exist in the ability to consistently and flexibly exert cognitive control across various contexts into the early twenties. Adolescence is also marked by peaks in sensation, novelty, and reward seeking behaviors thought to stem from normative increases in responsiveness in limbic and paralimbic brain structures, beginning around the onset of puberty. Asynchronous maturation in these systems during the adolescent period likely contributes to immature decision-making, strongly influenced by ‘bottom-up’ reward processes, and may help explain noted increases in risk taking behavior during adolescence. In this paper, structural and functional maturation in brain systems supporting reward and cognitive control processing are reviewed as a means to better understand risk taking. Particular emphasis is placed on adolescents' experimentation with drugs as a specific example of a risky behavior.

Highlights

► Brain systems supporting inhibitory control continue to mature through adolescence. ► Adolescents demonstrate peaks in reward sensitivity. ► Immature inhibitory and reward processes may underlie risky decisions.

Introduction

A quick stroll through the local shopping mall on a Friday evening may be sufficient for many to converge on a simple truth — adolescence is truly a dynamic and unique period of one's life. Adolescence is often considered to begin around the onset of puberty and culminate with the acquisition of adult social roles, although considerable inter-individual variability exists in these rough demarcations (Dahl, 2004, Spear, 2000, Spear, 2010). During this time span, which can extend a decade or longer, considerable change occurs across multiple domains (e.g., physical, cognitive, socio-emotional).

One hallmark of adolescence that has garnered considerable research attention is the progressive maturation of cognitive control. Cognitive control broadly refers to the mental abilities or processes that enable the formation and flexible use of internally generated plans to guide behavior (Fuster, 1997, Luna et al., 2001, Miller and Cohen, 2001). Key elements of cognitive control include fundamental mental operations such as inhibitory control, working memory, and attention allocation, among others (Cole and Schneider, 2007). Functional neuroimaging studies have shown that cognitive control is broadly supported by a distributed network of brain regions, including the lateral prefrontal cortex, anterior cingulate/preSMA, dorsal premotor cortex, anterior insular cortex, inferior frontal junction, and posterior parietal cortex (Cabeza and Nybert, 2000, Chein and Schneider, 2005, Cole and Schneider, 2007, Dosenbach et al., 2006). Compared to children, adolescents show improvements on behavioral tasks indexing various components of cognitive control (Luna, 2009). Compared to adults, however, adolescents are often limited in terms of not being able to consistently engage and flexibly exert cognitive control, particularly in contexts in which a salient reward is present or immediately accessible, or when they are otherwise emotionally aroused. This limitation extends into young adulthood (approximately the early twenties) and is a likely consequence of protracted microstructural and neurochemical development in the brain's cognitive control network (e.g., Casey and Jones, 2010, Casey et al., 2000, Diamond et al., 2002, Fair et al., 2008a, Hwang et al., 2010, Luna et al., 2004) (discussed more below).

Concomitant with on-going maturation in cognitive control, adolescents also demonstrate normative peaks in sensation, novelty, and reward seeking behaviors typically occurring around the onset of puberty (Chambers et al., 2003, Dahl, 2004, Spear, 2000, Steinberg, 2008). Believed to underlie these behaviors are normative increases in activation in limbic and paralimbic brain areas (e.g., orbitofrontal cortex, striatum, medial prefrontal cortex) involved in reward and emotion-related processing (Dahl, 2004). In particular, increased dopaminergic neurotransmission in mesocortical pathways has been suggested to play a prominent role in adolescents' heightened reward responses (Doremus-Fitzwater et al., 2010, Spear, 2010).

As noted elsewhere (e.g., Geier and Luna, 2009, Spear, 2010), it is important to underscore the notion that heightened sensation, novelty, and reward seeking during the adolescent period may in some sense be adaptive in that these internal drives motivate the young person to seek out and explore new environments, social situations, and experiences. In so doing, an individual may be exposed to new knowledge and skills that may be advantageous for adulthood. Supporting the notion of an adaptive role for peaks in these behaviors is evidence indicating that they are observed across societies, cultural contexts, and even species (Dahl, 2004, Spear, 2010). Yet, these heightened motivational drives, coupled with limited abilities to consistently regulate them, may also contribute to adolescents engaging in potentially dangerous or risky behaviors. Risk taking has been defined as engaging in behavior that may result in an outcome with subjectively high desirability, but that also carries with it the potential for negative, maladaptive consequences (Geier and Luna, 2009). It has been well documented that risk-taking behavior is elevated during adolescence, relative to childhood and adulthood (Dahl, 2004, Spear, 2010, Steinberg, 2004), contributing to significant increases in morbidity and mortality rates for this age group (Dahl, 2004).

Risk taking is a complex behavioral construct manifested in various ways (e.g., participation in extreme sports, driving excessively fast, engaging in unprotected sex). One primary example of a risky behavior that is common during the adolescent years is experimentation with various illicit and licit substances, most frequently alcohol, nicotine, and marijuana (e.g., Jacobus et al., 2012). Substance use during the adolescence years represents a critical public health issue as it can result in serious proximal and distal consequences (e.g., car accidents following binge drinking, secondary health problems like cancer due to chronic smoking). Of course, many adolescents who experiment with substances only do so during adolescence and experience little to no long-term effects. Nonetheless, a significant minority does experience problems and their initial experimentation with substances can escalate to extremely adverse outcomes including addiction. As such, increased knowledge of the underlying neurobiological factors contributing to risky decisions, like choosing to experiment with drugs, and factors that may expose vulnerability to dependence, represents a major goal of developmental cognitive neuroscience and is a focus of this review.

One prominent theoretical framework used to explain adolescents' proclivity for risk taking is the “dual-process” model (e.g., Somerville et al., 2010, Steinberg, 2008). This model posits that risk taking stems largely from a developmental ‘asynchrony’ between heightened activity in reward systems (which generally occurs around the onset of puberty (Dahl, 2004)) and relatively less mature (inconsistent) cognitive control systems (which do not reach adult-like levels of function until the early to mid-twenties) (e.g., Casey and Jones, 2010, Ernst et al., 2006, Geier and Luna, 2009, Somerville et al., 2010). In essence, this model suggests that the perceived benefits or rewards associated with engaging in a particular behavior are relatively over-valued by adolescents (compared to adults or children) spurred by their heightened reward responsiveness, while persistent limitations in “top-down” cognitive control (compared to adults) results in a reduced or inconsistent ability to regulate these often strong, ‘bottom-up” reward-related drives.

Within the general framework of the dual-process model, it has been proposed that risk taking behaviors may be usefully conceptualized as stemming from one or more decisions made in the context of a potential reward (Geier and Luna, 2009).1 Decision making, in turn, consists of more basic components, principal among them being reward processing and cognitive control processes, particularly inhibitory control (Balleine et al., 2011, Hooper et al., 2004, Pierrot-Deseilligny et al., 2003). As a concrete example of the role these component processes may play in risky decision making, consider a scenario in which an adolescent is offered a marijuana joint at a party. There are various options available to the adolescent, each associated with particular costs and benefits (involving the reward system). For example, the anticipated pleasurable feelings associated with taking the drug (in addition to potential social approval, an important consideration for adolescents) might be weighed against its potential costs (losing control of one's actions, getting sick, etc.). Similarly, the costs and benefits of abstaining (e.g., loss of social approval vs. maintaining control over one's body) might also be weighed. The decision to engage in the behavior or not involves evaluating the relative strengths of the competing contingencies, then inhibiting action associated with the ‘lower’ option and engaging motor systems that underlie approaching (choosing) the other (both of which rest on cognitive control). It has been proposed that examination of the neurobiological bases of these more basic processes (e.g., inhibitory control and reward processing), and their interaction, will further our understanding of more complex risk-taking during adolescence by identifying the specific nature of immature function in key component brain areas (Geier and Luna, 2009, Geier et al., 2010).

Toward this end, the main objective of this article is to review and evaluate the current state of knowledge on the development of cognitive control (particularly inhibitory control) as well as its relation to reward processing, component systems thought to underlie more complex decision-making processes and risk taking. Throughout, links are drawn between still-maturing brain processes and vulnerability to risky decision-making made in the context of rewards. Special consideration is given to initiating substance use as a specific type of risky behavior given its prevalence, the potential serious adverse consequences, and because many drugs of abuse (e.g., nicotine) act on many of the same brain systems that are undergoing significant maturation during adolescence, potentially altering their function and leading to further risky decisions.

To begin, a brief primer on adolescent brain structural development is provided, including an overview on gray and white matter microstructural changes. While an in-depth treatment of brain development is beyond the scope of this article, an understanding of fundamental concepts of structural brain maturation through adolescence is important in this context as it lays the foundation for interpreting changes in cognitive function, discussed later.

Section snippets

Brain development through adolescence

By the time most individuals enter adolescence, the overall size, cortical folding, and weight of the brain are comparable to adults (Armstrong et al., 1995, Caviness et al., 1996, Giedd et al., 1996). Despite gross similarities with adults, however, significant changes in brain morphology still occur during the adolescent period (Giedd and Rapoport, 2010). Principal among these include changes (decreases) in cortical gray matter, increased white matter, and alterations in neurotransmitter

Maturation of cognitive control

Cognitive control comprises a range of mental operations and processes that enable one's behavior to be guided by internally generated plans and goals rather than simply responding to external stimuli. It has been well documented that the ability to internally guide behavior is available early in development (Amso and Johnson, 2005, Bell and Fox, 1992, Diamond and Goldman-Rakic, 1989). During adolescence, progressive refinement occurs in these pre-existing abilities, specifically the ability to

Summary and conclusions

Adolescent risk taking behaviors, of which initiating substance use behaviors represent a significant type, may be viewed as stemming from immature decisions made in the context of rewards. Central to decision making are more basic cognitive abilities including inhibitory control and reward processing. Converging evidence from the studies reviewed in this manuscript indicate immature function in these component processes. Normatively heightened reward reactivity, supported in part by increased

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