Annual Research Review: Neural contributions to risk‐taking in adolescence – developmental changes and individual differences - Crone, Van Duijvenvoorde, Peper (2016) - Article

Many decisions in our daily lives involve an element of risk. In a risky choice, the decision outcome has a certain degree of uncertainty. The formal definition of risk taking as defined by economics is choosing the option with the highest outcome variability. This indicates that a risky choice may lead to greater benefits, but may also lead to greater negative outcomes at the expense of surety. It can be highly adaptive to take risks, for example to be able to make new relationships or to get further in a career.

What is risk taking?

Many decisions in our daily lives involve an element of risk. In a risky choice, the decision outcome has a certain degree of uncertainty. The formal definition of risk taking as defined by economics is choosing the option with the highest outcome variability. This indicates that a risky choice may lead to greater benefits, but may also lead to greater negative outcomes at the expense of surety. It can be highly adaptive to take risks, for example to be able to make new relationships or to get further in a career.

Is risk taking a normative developmental hallmark of adolescence?

Adolescence appears to be a period of increased risk taking. However, researchers have not yet been able to determine whether risk taking is observed in all adolescents and is a normative developmental hallmark of adolescence, or is present only some adolescents who have already been susceptible to problem behavior in childhood. These individual difference with regards to risk taking in adolescence remain unclear and within the scientific field there is not yet a consensus. Also because the findings with regards to risk taking are inconsistent. There is a growing need for more precise measurements of the processes that are involved in risk taking and how these change during adolescence. There are however also new insights, showing how changes in neuroanatomic and neural activity during adolescence contribute to a potential rise in risk taking.

Why are the slowly developing cognitive control abilities not responsible for risk taking during adolescence?

Risk taking has traditionally been interpreted as a purely cognitively driven process, driven by the slowly developing cognitive control abilities of adolescents. The evidence shows that the ability to use cognitive control (also referred to as executive functions) changes a lot during childhood and early adolescence and reaches adult levels around mid adolescence. There are very consistent findings, showing how different components of executive control follow different developmental trajectories. However, with regards to risk taking, mid to late adolescents perform well on executive function tasks, but show the highest levels of risk taking.

What do the recent frameworks with regards to risk taking in adolescence say?

The recent frameworks conceptualize the interaction between the cognitive and affective processes that are involved in risk taking. Adolescents are particularly susceptible to risk taking (compared to adults) when risks are unpredictable, when counterfactualy emotions (such as regret for not choosing the higher alternative) are involved, when rewards are encountered immediately, or when they are in the presence of peers.

What is the neurodevelopmental dual processing model?

Dual processing models propose that under emotionally arousing situations, adolescents may be more prone to be influenced by affective states compared to children and adults. Whereas under emotionally calm situations, they are more prone to make cognitively driven choices.

What can biology tell us about risk taking?

Biology focuses on the ventral striatum and the ventromedial prefrontal cortex. The striatum is divided into two parts:

• Dorsal part. This is related to a control network, involved in action selection, maintaining future goals and inhibiting prepotent responses.

• Ventral part. This part is related to a valuation network that is involved in decision making, learning and motivated behavior.

The ventromedial prefrontal cortex is strongly connected to the ventral striatum, which is an important structure for processing and learning. Biology is therefore interested in the developmental changes in the structure, function and connectivity of the ventromedial prefrontal cortex and the striatum to be able to understand the developmental changes and individual differences in risk taking. Research has shown that damage to the area of the ventromedial prefrontal cortex results in risk taking, especially when the contingencies are uncertain.

How does the brain respond to many different processes that are involved with risk taking?

The studies about the role of the ventromedial prefrontal cortex in risk taking were not able to separate how the brain responds to the many different processes that are involved with risk taking. Methods that examine these processes in more detail are relating risk taking to connectivity paths in the brain through white matter connections, through functional connectivity or by relating risk taking to neural activity during task performance.

What is anatomical connectivity?

Anatomical connectivity is established through white matter bundles that consist of myelinated axons. Anatomical connectivity has been used to study striatal and prefrontal cortex communication in relation to risk taking. This technique can be especially helpful for investigating the dual processing hypothesis, because it suggests that there is an imbalance between both brain systems (suggesting an abnormal communication through white matter pathways).

What role does testosterone play in risk taking during adolescence?

Hormonal changes, such as an increase of testosterone, may trigger some of the changes in risk taking behavior during adolescence. Higher levels of testosterone are related to more economic and non-economic risk taking. Given the massive changes in hormone levels during adolescent development, it is possible that these changes have an important shaping role in brain organization and prefrontal cortex-striatum connectivity. This may implicate risk taking behavior.

How can changes in risk taking behavior during adolescence be attributed to changes in brain morphology?

Gray and white matter undergo big changes from childhood to adulthood. There is an overall reduction of gray matter volume and cortical thickness, an increase in white matter volume, and changes in the organization of white matter connections. These changes in the brain structure are thought to reflect fine-tuning and specialization of neuronal networks and underlie refinement of motor functioning, higher order cognition and cognitive control. Research has shown that the striatum-prefrontal cortex white matter tracts are related to impulsivity control, and that relatively fast development of the medial orbitofrontal cortex decreases risk taking behavior in girls, but increases risk taking in boys.

Can risk taking behavior be considered adaptive behavior?

Risk taking can be a form of adaptive exploratory behavior. Adolescence is associated with quickly changing environmental demands that require adaptive skills and high flexibility. Risk taking can be associated with obtaining personal autonomy and identity based on experience, and adolescents can have the opportunity to learn from the negative consequences of their behavior.

How is reward anticipation related to risk taking behavior during adolescence?

The ventral striatum is active when anticipating and when receiving rewards, relative to no rewards or losses. Research indicated that adolescents may be more driven by rewards. However, the heightened response in the striatum of adolescents was not found when the delivery of reward remained uncertain or depended on performance.

What neural activity is involved when taking voluntary risks?

A risky decision is when a person needs to decide between a certain chance of getting a small reward, and an uncertain chance of getting a high reward. Safe choices seem to be associated with activation in the dorsolaterale prefrontal cortex, whereas risky choices seem to be associated with activation in the ventromedial prefrontal cortex. There was one part of the brain, lying at the intersection of the ventromedial prefrontal cortex and the ventrial striatum, that seemed to be more active for adolescents when they were making a risky decision, indicating a unique affective coding of rewards in adolescence.

To what extent does the connectivity between the striatum and the prefrontal cortex change during choice or outcome?

There seems to be an age-related increase in functional connectivity between the ventral striatum and the medial prefrontal cortex when receiving positive feedback relative to negative feedback (and gains compared to losses). The ventral striatum and the medial prefrontal cortex seem to have a regulatory role, since the strength in connectivity between them attenuated risk taking.

What is resting-state connectivity analysis?

Resting-state connectivity analysis is a new way to examine the relation between risk taking and striatum-prefrontal cortex connectivity by examining functional activity during rest. Task-free connectivity patterns (or resting-state connectivity) assess synchronous activity between brain regions when individuals are awake but resting, and focuses on spontaneous low frequency fluctuations in the blood oxygen level dependent signal. It allows to investigate age-related chances in intrinsic functional connectivity in children of all ages, because of their minimal attentional demands. Important findings that have been discovered through this method:

• A decline in positive coupling between the striatum and the ventromedial prefrontal cortex indicates a functional specialization of value-based processes that may be partially driven by testosterone. It is possible that the functional roles of the subgenual anterior cingulate cortex versus the striatum becomes more differentiated with age.

• In late childhood functional coupling between the striatum and the ventromedial prefrontal cortex may result in increased reward valuation. With development increasing, functional specialization leads to a decoupling of these regions that supports reward-based learning and controlled behavior.

• There was no relation between the ventromedial prefrontal cortex and the striatum connectivity and alcohol use, but the connectivity between the ventromedial prefrontal cortex and the amygdala was a strong predictor of alcohol use.