D

R

T

ENa

b

c

a

ARRAA

KARDSRC

C

n

h1b

ARTICLE IN PRESSG ModelCN-338; No. of Pages 15Developmental Cognitive Neuroscience xxx (2015) xxx–xxx

Contents lists available at ScienceDirect

Developmental Cognitive Neuroscience

j o ur nal ho me pa ge: ht tp : / /www.e lsev ier .com/ locate /dcn

eview

he dual systems model: Review, reappraisal, and reaffirmation

lizabeth P. Shulmana,∗,1, Ashley R. Smithb,1, Karol Silvab, Grace Icenogleb,atasha Duellb, Jason Cheinb, Laurence Steinbergb,c

Brock University, Psychology Department, 1812 Sir Isaac Brock Way, St. Catharines, ON L2S 3A1, CanadaTemple University, Department of Psychology, 1701 N. 13th Street, Philadelphia, PA 19122, USAKing Abdulaziz University, Abdullah Sulayman, Jeddah 22254, Saudi Arabia

r t i c l e i n f o

rticle history:eceived 22 January 2015eceived in revised form 17 July 2015ccepted 19 December 2015vailable online xxx

eywords:dolescentsisk takingual systemsensation-seeking

a b s t r a c t

According to the dual systems perspective, risk taking peaks during adolescence because activation of anearly-maturing socioemotional-incentive processing system amplifies adolescents’ affinity for exciting,pleasurable, and novel activities at a time when a still immature cognitive control system is not yetstrong enough to consistently restrain potentially hazardous impulses. We review evidence from boththe psychological and neuroimaging literatures that has emerged since 2008, when this perspective wasoriginally articulated. Although there are occasional exceptions to the general trends, studies show that,as predicted, psychological and neural manifestations of reward sensitivity increase between childhoodand adolescence, peak sometime during the late teen years, and decline thereafter, whereas psychologicaland neural reflections of better cognitive control increase gradually and linearly throughout adolescenceand into the early 20s. While some forms of real-world risky behavior peak at a later age than predicted,

eward sensitivityognitive control

this likely reflects differential opportunities for risk-taking in late adolescence and young adulthood,rather than neurobiological differences that make this age group more reckless. Although it is admittedlyan oversimplification, as a heuristic device, the dual systems model provides a far more accurate accountof adolescent risk taking than prior models that have attributed adolescent recklessness to cognitive

deficiencies.

© 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-NDlicense (http://creativecommons.org/licenses/by-nc-nd/4.0/).

ontents

1. The emergence of dual systems models . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 002. The current article . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 003. Are adolescents particularly prone to risk taking? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

3.1. Risk taking in the laboratory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 004. The development of sensation seeking and reward sensitivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

4.1. Sensation seeking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 004.2. Behavioral manifestations of reward sensitivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 004.3. Neuroimaging of reward sensitivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

5. The development of self-regulation and cognitive control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.1. Self-reported impulsivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.2. Behavioral measures of self-regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3. Neuroimaging of cognitive control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .00

6. Is risk taking during adolescence related to heightened reward sensitivity and immature cognitive control? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

Please cite this article in press as: Shulman, E.P., et al., The dual sysNeurosci. (2015), http://dx.doi.org/10.1016/j.dcn.2015.12.010

7. Unresolved questions and future directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .8. Concluding comment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

∗ Corresponding author.E-mail addresses: eshulman@brocku.ca (E.P. Shulman), tuc69946@temple.edu (A.R. S

tduell@temple.edu (N. Duell), jchein@temple.edu (J. Chein), lds@temple.edu (L. Steinber1 These authors made equal contributions to the article and should be considered co-fi

ttp://dx.doi.org/10.1016/j.dcn.2015.12.010878-9293/© 2016 The Authors. Published by Elsevier Ltd. This is an open accessy-nc-nd/4.0/).

tems model: Review, reappraisal, and reaffirmation. Dev. Cogn.

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

mith), karol.silva@temple.edu (K. Silva), grace.icenogle@temple.edu (G. Icenogle),g).rst authors.

article under the CC BY-NC-ND license (http://creativecommons.org/licenses/

dx.doi.org/10.1016/j.dcn.2015.12.010dx.doi.org/10.1016/j.dcn.2015.12.010http://www.sciencedirect.com/science/journal/18789293http://www.elsevier.com/locate/dcnhttp://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/mailto:eshulman@brocku.camailto:tuc69946@temple.edumailto:karol.silva@temple.edumailto:grace.icenogle@temple.edumailto:ntduell@temple.edumailto:jchein@temple.edumailto:lds@temple.edudx.doi.org/10.1016/j.dcn.2015.12.010http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/

ING ModelD2 ogniti

hatrcsidp

lypolai

1

nbm(nopromtliS2ibtfsaa

psoupsiCiavmtsmasmto

ARTICLECN-338; No. of Pages 15 E.P. Shulman et al. / Developmental C

Social scientists and casual observers of human developmentave long noted that the transitional period between childhoodnd adulthood is a time of heightened risk-taking. Indeed, despitehe relative absence of illness and disease during this period,ates of morbidity and mortality increase substantially in adoles-ence, largely due to risk taking. The question of why adolescentseem predisposed toward recklessness is age-old; however, workn the field of developmental psychology, and more recently,evelopmental neuroscience, has provided new insights into thehenomenon.

For many years psychologists had attempted to explain ado-escent recklessness as a consequence of cognitive deficiencies inoung people’s thinking, including irrationality, poor informationrocessing, and ignorance about risk. As we have noted in previ-us publications (e.g., Steinberg, 2008), these accounts have beenargely undermined by available evidence. Generally speaking, byge 15 or so, adolescents perform as well as adults on tasks measur-ng logical reasoning, information processing, and risk perception.

. The emergence of dual systems models

About a decade ago, the budding field of developmental cog-itive neuroscience began to provide insight into how patterns ofrain development might explain aspects of adolescent decision-aking (see, e.g. Dahl, 2004). In 2008, our lab at Temple University

Steinberg, 2008; Steinberg et al., 2008) and Casey’s lab at Cor-ell (Casey et al., 2008) simultaneously proposed similar variationsf a “dual systems” account of adolescent decision-making. Thiserspective attributes adolescents’ vulnerability to risky, ofteneckless, behavior in part to the divergent developmental coursesf two brain systems: one (localized in the striatum, as well as theedial and orbital prefrontal cortices) that increases motivation

o pursue rewards and one (encompassing the lateral prefrontal,ateral parietal, and anterior cingulate cortices) that restrainsmprudent impulses (see e.g., Casey et al., 2008; Duckworth andteinberg, 2015; Evans and Stanovich, 2013; Luna and Wright,016; Metcalfe and Mischel, 1999; Steinberg, 2008). Specifically,

t proposes that risk-taking behaviors peak during adolescenceecause activation of an early-maturing incentive-processing sys-em (the “socioemotional system”) amplifies adolescents’ affinityor exciting, novel, and risky activities, while a countervailing, butlower to mature, “cognitive control” system is not yet far enoughlong in its development to consistently restrain potentially haz-rdous impulses.

Several variations on this dual systems model have been pro-osed. The version that guides our work (Steinberg, 2008) is veryimilar to that proposed by Casey et al. (2008). Both conceivef a slowly developing cognitive control system, which contin-es to mature through late adolescence. However, whereas weropose that the socioemotional system follows an inverted-Uhaped developmental course, such that responsiveness to rewardncreases in early adolescence and declines in early adulthood,asey et al. have portrayed the socioemotional system as increas-

ng in arousability until mid-adolescence, at which point it reaches plateau, remaining at this level into adulthood. Furthermore, ourersion of the dual systems model posits that the decline in socioe-otional arousability occurs independently of the development of

he control system, whereas Casey et al.’s model proposes that thetrengthening of the cognitive control system causes the socioe-otional system to become less arousable. More recently, Luna

nd Wright (2016) have proposed another variation on the dual

Please cite this article in press as: Shulman, E.P., et al., The dual sysNeurosci. (2015), http://dx.doi.org/10.1016/j.dcn.2015.12.010

ystems model (the “driven dual systems” model), which, like ourodel, hypothesizes an inverted-U shaped trajectory of socioemo-

ional arousability, but, unlike our model, hypothesizes a trajectoryf cognitive control that plateaus in mid-adolescence rather than

PRESSve Neuroscience xxx (2015) xxx–xxx

continuing to increase into the 20s, as suggested by us and by Caseyet al. In a similar vein, Luciana and Collins (2012) endorse a modelthat emphasizes the role of a hyperactive socioemotional system(“subcortical limbic-striatal systems” in their terminology) under-mining the regulatory ability of the cognitive control system (the“prefrontal executive system”) resulting in greater risk-taking dur-ing adolescence. Like Luna and Wright, Luciana and Collins arguethat the development of cognitive control is complete by mid-adolescence, as evidenced by adolescents’ adult-like performanceon non-affective measures of cognitive capacity. Fig. 1 illustratesthe similarities and differences between these versions of the dualsystems model.

Another perspective, Ernst’s (2014) triadic model, expands onthe dual systems concept by hypothesizing that a third brainsystem—one responsible for emotional intensity and avoidance,anchored in the amygdala—is also important for understanding thedevelopmental differences in “motivated behavior.” With respectto the type of reward-seeking risky behavior that the dual systemsmodels seek to explain, Ernst (2014) speculates that this emo-tion/avoidance system may serve to boost impulsive decisions inadolescence by amplifying the perceived cost of delay. She alsoproposes that this system may become hypoactive—dampeningavoidance impulses—in the face of a potential reward that acti-vates the socioemotional system. While this model is intuitivelyappealing, there is not much evidence to date indicating that theemotion/avoidance system and its developmental trajectory helpto explain heightened levels of risk taking in adolescence. Also, therole of the amygdala in decision-making is not yet clear (see e.g.,Somerville et al., 2014). Therefore, our review does not address thisthird hypothesized system.

2. The current article

In this article, we review evidence from both the behavioral andneuroimaging literatures that has emerged since the dual systemsmodel was originally articulated in 2008. In particular, we considerthe degree to which extant research findings support, extend, mod-ify, and challenge the theory. We focus our discussion on three mainpropositions of the model: (1) that reward sensitivity peaks in ado-lescence; (2) that cognitive control increases linearly during thisperiod; and (3) that heightened risk-taking during adolescence isthe product of heightened reward-seeking and relatively weakercognitive control.

We begin by addressing a recent criticism of the basic premisethat middle adolescence is an especially intensified period of riskybehavior. We then examine evidence regarding the trajectoryof sensation seeking across development, the reward processingcircuitry that might underlie developmental changes in sensation-seeking behavior, and the extent to which heightened sensationseeking and reward sensitivity are related to pubertal develop-ment. Next, we survey evidence on the developmental trajectoryof the ability to control impulsive behavior through self-regulatoryprocesses, and on the maturation of the brain’s cognitive controlnetwork, which is proposed to undergird this ability. Finally, weconsider evidence concerning the interaction of the two proposedsystems during risky decision making, identify several unresolvedissues, and offer some recommendations for how they might beaddressed in future research.

In examining how recent evidence informs the dual systemsmodel, we are cognizant of critiques of this viewpoint, includingcontentions that the model inadequately accounts for studies

tems model: Review, reappraisal, and reaffirmation. Dev. Cogn.

that do not find adolescents to be particularly sensitive to reward(Pfeifer and Allen, 2012; but see Strang et al., 2013 for a responseto this critique), that cognitive control does not unequivocallyimprove during adolescence (Crone and Dahl, 2012), and that

dx.doi.org/10.1016/j.dcn.2015.12.010

ARTICLE IN PRESSG ModelDCN-338; No. of Pages 15E.P. Shulman et al. / Developmental Cognitive Neuroscience xxx (2015) xxx–xxx 3

Dual Systems ModelA.(Steinberg, 2008)

Stre

ngth

Age

Stre

ngth

Age

Stre

ngth

Agesocioemo�onal system cogni�ve control system

Matura�onal Imbalance ModelB.(Casey et al., 2008)

Driven Dual Systems ModelC.(Luna & Wright, 2015)

al (re

arEt

t2bunaep2h

bmb1aiattsacrrpam

pthtrgripobr

atsse

by centuries. And yet, empirical evidence of a mid-adolescent peakin risk taking (at least in humans) is not unequivocal. As pointedout in a recent review of epidemiological data, the peak agefor risk taking varies across different behaviors, and very often

NEUROBIOLOGICAL

PSYCHOLOGICAL

Reward Sensi�vity

Sensa�on Seeking

Self-Regula�on

Cogni�ve Control

BEHAVIORAL

Decision Making

Risk Taking

Fig. 1. Alternative theoretical models of the development of the socioemotion

dolescence may not actually be a peak period of vulnerability toisk-taking (e.g., Defoe et al., 2014; Willoughby et al., 2013; but seernst, 2014 for a response to Willoughby et al.). We briefly addresshese critiques here.

We do not disagree with a fourth critique of the dual sys-ems model—that it is insufficiently nuanced (Pfeifer and Allen,012)—because this is almost certainly correct. However, weelieve that even an admittedly simplified model can serve as aseful heuristic and, more important, can help to motivate researcheeded to flesh out the details of an initially simplistic account (for

full discussion see Strang et al., 2013). Moreover, given the influ-nce this perspective continues to have on legal policy and practice,ublic health, and popular discourse about adolescence (Steinberg,014), it is important to ask whether this simplified account iselpful or misguided.

It may be useful at this juncture to clarify our terminology. Toegin, the term “adolescence” warrants discussion. Largely as aatter of convenience, scholars generally agree that adolescence

egins when pubertal development becomes evident, around age0 (somewhat later among males). The end of adolescence—thettainment of adult status—is not easily pegged to any single biolog-cal or social event, however. In research, adulthood is often defineds beginning at either age 18 or 21, the two ages most often tiedo legal majority in the developed world. However, given that 18-o 21-year-olds in industrialized societies are rarely regarded out-ide the legal system as fully mature adults, and typically have notttained many of the traditional markers of adult status (e.g., finan-ial independence, completion of formal education, stable romanticelationships, full-time employment, parenthood), we prefer toefer to this age range as “late adolescence.” For purposes of thisaper, our focus is mainly on the second decade of life, from aboutges 10 to 21, which we subdivide into early adolescence (10–13),iddle adolescence (14–17), and late adolescence (18–21).Another source of confusion in discussions of the dual systems

erspective concerns levels of analysis, since the perspective referso overt behaviors (such as risk taking), the psychological statesypothesized to motivate them (such as sensation seeking), andhe neural processes believed to undergird these states (such aseward sensitivity). In an earlier paper (Smith et al., 2013), we sug-ested that “reward sensitivity” and “cognitive control” be used toefer to the neurobiological constructs that are measured in stud-es of brain structure or function (see Fig. 2). These neurobiologicalhenomena have psychological manifestations (in our terminol-gy, “sensation seeking” and “self-regulation”) that are measuredy assessing psychological states or traits through the subjectiveeports of individuals or their evaluators.

For heuristic purposes, we use “sensation seeking” as an over-rching label for a number of interrelated constructs that refer

Please cite this article in press as: Shulman, E.P., et al., The dual sysNeurosci. (2015), http://dx.doi.org/10.1016/j.dcn.2015.12.010

o the inclination to pursue “varied, novel, complex, and intenseensations and experiences and the willingness to take physical,ocial, legal, and financial risks for the sake of such experi-nces” (Zuckerman, 1994, p. 26). Recruitment of brain regions and

ward processing) and cognitive control systems from about age 10 to age 25.

systems implicated in reward-processing (e.g., ventral striatum,orbitofrontal cortex) has been linked to measures of sensation seek-ing in humans and other animals (Abler et al., 2006; Leyton et al.,2002; Lind et al., 2005). In a similar vein, we use the label “self-regulation” to refer to a group of interrelated but distinguishableconstructs that refer to the capacity to deliberately modulate one’sthoughts, feelings, or actions in the pursuit of planned goals; amongthese constructs are impulse control, response inhibition, emotionregulation, and attentional control. Aspects of self-regulation havebeen linked to the functioning of brain regions and systems thatsubserve cognitive control (e.g., lateral prefrontal, lateral parietal,and anterior cingulate cortices) (Luna et al., 2010; Mennigen et al.,2014).

Variations in sensation seeking and self-regulation, in turn, areassociated with variations in behaviors, including risk taking, whichcan be measured through objective reports or observations. In ourmodel, risk taking is a subset of many aspects of decision makingthat share some, but not all, characteristics in common. Further-more, as Fig. 2 indicates, all decision making takes place within abroader context that encourages and enables some acts but discour-ages and prohibits others. As we discuss, the fact that adolescents’risk taking is influenced by the broader context in which it occursmakes it difficult to move seamlessly between laboratory studiesand the real world.

3. Are adolescents particularly prone to risk taking?

Allusions to adolescence as a time of rash behavior and poordecision making predate the articulation of the dual systems model

tems model: Review, reappraisal, and reaffirmation. Dev. Cogn.

Context

Fig. 2. Constructs implicated in the dual systems model of adolescent risk-takingarranged by level of analysis.

dx.doi.org/10.1016/j.dcn.2015.12.010

ING ModelD4 ogniti

ihed2

saoponcwmCcrrtrttbppm

3

shtttdbfriLBspsle

uddoroda2crrottao

ARTICLECN-338; No. of Pages 15 E.P. Shulman et al. / Developmental C

t is late adolescents, not middle adolescents, who exhibit theighest levels of recklessness (see Willoughby et al., 2013). Forxample, one of the most dangerous forms of substance use—bingerinking—is most common during the early 20s (Chassin et al.,002; Willoughby et al., 2013).

Although some argue that these data pose a problem for the dualystems model, we disagree. The model does not posit that middledolescents necessarily demonstrate the highest levels of all formsf risk taking in the real world. Rather, it asserts that risk-takingropensity is highest in mid-adolescence, but that the expressionf this propensity is expected to vary depending on the context (asoted in Fig. 2). Our position is that late adolescents are less biologi-ally predisposed to risk taking than middle adolescents (consistentith the dual systems model), but that they exhibit higher levels ofany forms of real-world risk-taking due to greater opportunity.

ompared to younger individuals, people in their early 20s typi-ally experience less supervision from adults, have more financialesources, and are afforded greater legal access to many forms ofisk taking (e.g., driving, alcohol, and gambling). Thus, we contendhat maturational factors predispose middle adolescents to greaterisk taking, but that social and legal factors constrain their oppor-unities to realize this predisposition. Simply put, it is far easier forhe average 21-year-old to take risks with alcohol, cars, and gam-ling than it is for the average 15-year-old. If 15-year-olds wereermitted to drive, purchase alcohol, and enter casinos legally, ourrediction is that they would likely crash, binge drink, and gambleore than people in their early 20s.

.1. Risk taking in the laboratory

In an effort to investigate age differences in risk-taking propen-ity, unconfounded by age differences in opportunity, researchersave tested adolescent and adult participants using artificialasks—typically gambling games and driving simulations—that givehem the option to take risks in the safety of a laboratory set-ing. While such tasks are often lacking in ecological validity, theyo have the advantage of controlling for contextual differencesetween adolescents and other age groups, as well as for age dif-erences in behavior preferences. These studies yield inconsistentesults, with some finding greater risk taking in adolescence thann adulthood (e.g., Burnett et al., 2010; Mitchell et al., 2008; Vaneijenhorst et al., 2008, 2010a), others finding no age effects (e.g.,jork et al., 2007; Eshel et al., 2007; de Water et al., 2014), andtill others finding that adolescents engage in less risk taking com-ared to children (Paulsen et al., 2011). These inconsistent findingsuggest that if there is an increased risk taking propensity in ado-escence it may only manifest under certain conditions (see Defoet al., 2014 for a recent meta-analysis).

Recently, researchers have used laboratory tasks and manip-lations that better approximate certain aspects of real-life riskyecision-making. These studies have helped to delineate the con-itions under which adolescents may be more predisposed thanther age groups to take risks. For example, noting that during mosteal-world risk taking the actual chances of a positive or negativeutcome are unknown, researchers recently tested whether ageifferences in risk taking depend on whether the probabilities of

successful outcome are known or unknown (Tymula et al., 2012,013). Tymula and colleagues (2012) had adolescents and adultsomplete a risk-taking task with two different conditions: a “knownisk” condition and an “ambiguous risk” condition. In the “knownisk” condition, participants chose between a sure bet (100% chancef receiving $5) and a “risky” bet with known reward probabili-

Please cite this article in press as: Shulman, E.P., et al., The dual sysNeurosci. (2015), http://dx.doi.org/10.1016/j.dcn.2015.12.010

ies (e.g., a 50% chance of winning $50, versus $0 if they lost). Inhe “ambiguous risk” condition, participants again chose between

sure and risky option, but this time the likelihood of winningr losing on the risky option was unknown. Compared to adults,

PRESSve Neuroscience xxx (2015) xxx–xxx

adolescents made fewer risky decisions when the probabilities ofloss were known (i.e., adolescents were less risk tolerant). However,when the probabilities were unknown, adolescents made signif-icantly more risky decisions than adults. Thus, under conditionsthat are more representative of real-life risk-taking (where riskprobabilities are typically unknown), adolescents evince a greaterrisk-taking propensity than adults.

Another way in which real-life risk taking differs from risk tak-ing in the laboratory is with respect to emotional arousal. Contextsin which risk taking occurs outside the lab are often thrilling orfrightening; in the lab, both the nature of the risk taking (the stakesand considerations involved) and the surrounding environmentare typically less exciting. Scholars have argued that differencesin arousal give rise to fundamentally different ways of processinginformation (e.g., Luna and Wright, 2016; Metcalfe and Mischel,1999). The dual systems model holds that, to the extent thatdecision-making occurs under conditions that arouse the socioe-motional system (e.g., conditions that are relatively more thrilling),differences between adolescent and adult decision-making and,hence, risk taking will be more pronounced. This pattern wasobserved in one study that experimentally manipulated the degreeto which a card game risk-taking task was affectively arousing(Figner et al., 2009). Consistent with the dual systems account, ado-lescents evinced greater risk taking and poorer use of risk-relevantinformation than adults, but only in the more arousing version ofthe task.

A third difference between most laboratory risk-taking tasksand real-life risk taking is that, in the laboratory, adolescents areasked to make decisions when they are alone, whereas the major-ity of risky behaviors during adolescence occur in groups (Albertet al., 2013). To mimic this context in the lab, researchers haveemployed experimental manipulations in which adolescents com-plete risk-taking tasks in the presence of peers (real or illusory).Some studies have asked participants to bring same-aged peers tothe lab (Chein et al., 2011; Gardner and Steinberg, 2005; Kretsch andHarden, 2014), while others have deceived participants into believ-ing that they are being observed remotely by a peer (Smith et al.,2014a). Not only does the “presence” of peers increase the ecolog-ical validity of the risk-taking task (because adolescent risk takingoften occurs in groups), but it also appears to elevate emotionalarousal, which further increases the comparability to real-worldrisk-taking contexts.

Studies that have manipulated the social context have foundthat adolescents are more induced by peer presence to take risksthan are adults (Chein et al., 2011; Gardner and Steinberg, 2005;Smith et al., 2014a). These findings, which are largely consis-tent with other studies of peer effects on adolescent driving [e.g.,Segalowitz et al., 2012; see Lambert et al. (2014) for a review], sug-gest that adolescents are particularly vulnerable to the effects ofpeer presence on risk-taking behaviors. Moreover, neuroimagingdata suggest that the effect of peer presence on risk taking is dueto increased affective arousal, as evidenced by greater activationof brain regions within the socioemotional system (Chein et al.,2011). A recent extension of this line of work in our lab using arodent model found that adolescent mice, but not adult mice, con-sume more alcohol in the presence of same-aged conspecifics thanwhen alone (Logue et al., 2014).

Overall, then, there is evidence for increased risk taking inadolescence compared to adulthood, though developmental dif-ferences may only be evident under certain conditions, such asemotional arousal, ambiguous risk, and the presence of others.The tendency for adolescents to engage in more risky behaviors inhighly-arousing contexts together with increased engagement oftheir socioemotional system during peer observation point to the

tems model: Review, reappraisal, and reaffirmation. Dev. Cogn.

importance of reward processing in decision making during thisperiod of life, a topic to which we now turn.

dx.doi.org/10.1016/j.dcn.2015.12.010

ING ModelDogniti

4s

admAiriTst

comoieb2c2m1tedshoriw

4

imoelqiwss(a2onw(e(itaaYti

ARTICLECN-338; No. of Pages 15E.P. Shulman et al. / Developmental C

. The development of sensation seeking and rewardensitivity

Increased adolescent risk taking in contexts that are emotion-lly arousing is consistent with one of the central tenets of theual systems model—that activation and reactivity of the socioe-otional system reaches its peak during mid- to late adolescence.

growing literature interrogates this aspect of the model by exam-ning the psychological and neurological evidence for heightenedesponsiveness of the socioemotional system during adolescence,ncluding in situations that do not involve risky decision-making.his is important because the dual systems model proposes that theocioemotional system is more responsive generally in adolescencehan at other ages, not only in the context of risk taking.

Moreover, the model hypothesizes that the developmentalourse of the socioemotional system is, unlike the developmentf the cognitive control system, closely tied to pubertal develop-ent (for review see Smith et al., 2013). Around age 12 (for boys)

r 11 (for girls), pubertal hormones inundate the brain, trigger-ng a series of changes in neural structure and function (Eulingt al., 2008; Schulz et al., 2009), especially in dopamine-rich lim-ic regions associated with reward processing (Blakemore et al.,010; Sinclair et al., 2014). It is thought that these hormone-relatedhanges sensitize the adolescent brain to reward (Forbes and Dahl,010; Peper and Dahl, 2013), as appears to be the case in ani-al studies (Alexander et al., 1994; Clark et al., 1996; Miele et al.,

988). More specifically, the reward system is particularly sensitiveo the sudden surge of hormones at the start of puberty, height-ning sensitivity to affective stimuli. Although pubertal hormoneso not decline into adulthood, we posit that a decrease in rewardensitivity ensues during later adolescence and into young adult-ood as the reward system becomes desensitized to the effectsf these hormones (Smith et al., 2013). While admittedly limited,ecent evidence integrating measures of puberty into psycholog-cal, behavioral, and neuroscience studies supports this claim as

ell.

.1. Sensation seeking

One psychological manifestation of socioemotional reactivitys sensation seeking. As anticipated by the dual systems model,

easures of sensation seeking are often found to be predictivef self-reported risk taking (e.g., Kong et al., 2013; MacPhersont al., 2010). True sensation-seeking behavior is difficult to elicit inaboratory environments (at least, among human subjects); conse-uently, the vast majority of studies examining age-related changes

n sensation seeking rely on self-report. As would be expectedithin the dual systems account, longitudinal and cross-sectional

tudies generally find evidence of a peak in self-reported sensationeeking around mid-adolescence and a decrease into adulthoodHarden and Tucker-Drob, 2011; Peach and Gaultney, 2013; Quinnnd Harden, 2013; Romer and Hennessy, 2007; Shulman et al.,014a,b; Steinberg and Chein, 2015; Steinberg et al., 2008). Thisverall pattern is further corroborated by a number of longitudi-al studies following individuals from childhood into adolescence,hich find that sensation seeking increases across this time period

Collado et al., 2014; Lynne-Landsman et al., 2011; MacPhersont al., 2010). For example, using the Brief Sensation-seeking ScaleHoyle et al., 2002), Collado and colleagues (2014) found a linearncrease in sensation seeking in individuals aged 9–13. Fewer longi-udinal studies of sensation seeking have followed individuals fromdolescence into adulthood. However, two recent studies using

Please cite this article in press as: Shulman, E.P., et al., The dual sysNeurosci. (2015), http://dx.doi.org/10.1016/j.dcn.2015.12.010

large, longitudinal data set (the National Longitudinal Study ofouth 1979 Child and Young Adult Survey) have helped to addresshis gap and clarify the developmental pattern of sensation seek-ng across adolescence. Harden and Tucker-Drob (2011) found that

PRESSve Neuroscience xxx (2015) xxx–xxx 5

self-reported sensation seeking increased from age 10 to mid-adolescence, and then decreased thereafter into early adulthood.Analyzing the same data set, Shulman and colleagues (2014a,b)found that females demonstrated an earlier peak in sensation seek-ing (age 16–17) than males (age 18–19), and a steeper declinethereafter. Overall, these studies suggest that, as the dual systemsmodel would predict, sensation seeking follows an inverted-U pat-tern over time, consistent with the proposed pattern of change inthe socioemotional system.

The hypothesis that pubertal development drives developmen-tal change in the socioemotional system in adolescence is derivedin part from older studies linking higher levels of sensation seek-ing to more advanced pubertal status (Martin et al., 2002; Resnicket al., 1993). Newer studies have replicated this result (Castellanos-Ryan et al., 2013; Gunn and Smith, 2010; Quevedo et al., 2009;Urošević et al., 2014) and have found evidence that the correla-tion between self-reported pubertal development and sensationseeking may be stronger for boys than for girls (Castellanos-Ryanet al., 2013; Steinberg et al., 2008). Also, as would be expected basedon the link between puberty and sensation seeking, recent studieshave found that more advanced pubertal status in adolescents isassociated with greater involvement in behaviors that are closelyrelated to sensation seeking, such as substance use (Castellanos-Ryan et al., 2013; de Water et al., 2013; Gunn and Smith, 2010),law-breaking (Collado et al., 2014; Kretschmer et al., 2014), andrisk taking in laboratory contexts (Collado et al., 2014; Kretsch andHarden, 2014; Steinberg et al., 2008; but see van Duijvenvoordeet al., 2014 who did not find a correlation between pubertal statusand performance on a gambling task).

4.2. Behavioral manifestations of reward sensitivity

Compared to self-report studies of sensation seeking, there aremarkedly fewer behavioral studies examining the development ofreward sensitivity, and these have heterogeneous methodologiesand findings, which makes it difficult to draw firm conclusionsabout age differences. One large-scale study utilized the IowaGambling Task (IGT; Cauffman et al., 2010) to explore age-relatedchanges in reward sensitivity. In the standard version of the IGT,participants are presented with four decks of cards, two that willwin them money over repeated play (advantageous decks) and twothat will lose them money over repeated play (disadvantageousdecks); participants are permitted to choose freely from the fourdecks (e.g., Smith et al., 2011b). However, Cauffman et al. (2010)modified the task such that the computer pseudorandomly selecteda deck on each trial and the participant was asked to decide whetherto play or pass. This modification allowed the researchers to disen-tangle affinity for the advantageous decks—a measure of rewardsensitivity—from avoidance of disadvantageous decks. The resultsindicated that mid-adolescents aged 14–17 and older adolescentsaged 18–21 learned to play from advantageous decks faster thaneither younger adolescents (ages 10–13) or adults (ages 22–25),a finding that was recently replicated in an international sampleof more than 5000 individuals (Steinberg and Chein, 2015). Thisoutcome suggests that ages 14–21 are a period of heightened sen-sitivity to reward. Using the same data set, Steinberg (2010) alsofound that self-reported sensation seeking, but not impulsivity, wasassociated with overall rate of plays from rewarding decks at theend of the task.

Another way researchers have examined developmental differ-ences in reward sensitivity is by substituting neutral stimuli (e.g.,letters) with rewarding ones (e.g., happy faces) in traditional behav-

tems model: Review, reappraisal, and reaffirmation. Dev. Cogn.

ioral tasks (e.g., measures of impulse control), and then observingthe extent to which the presence of rewarding stimuli impactsperformance. Two such studies have examined age differences(comparing children, adolescents, and adults) in performance on

dx.doi.org/10.1016/j.dcn.2015.12.010

ING ModelD6 ogniti

aaui(aet[l2

(Tdwrataf(taitefovnmtta

4

attuaawamtcsbal

fssrdseaiat

ARTICLECN-338; No. of Pages 15 E.P. Shulman et al. / Developmental C

n “Emotional Go/No-Go” task. In all Go/No-Go tasks, participantsre presented with a rapid sequence of target and non-target stim-li, both of which are typically emotionally neutral. Participants are

nstructed to press a button when a target stimulus is presenteda “go” trial) and to withhold the button press (do nothing) when

non-target stimulus is presented (a “no-go” trial). Non-targetvents occur relatively infrequently, making it challenging for par-icipants to restrain the impulse to press the button on no-go trials.As with most measures of self-regulation, performance improvesinearly with age on traditional Go/No-Go tasks (see Casey et al.,002 for a review).]

In the Emotional Go/No-Go task employed by Somerville et al.2011), the stimuli were photographs of either happy or calm faces.hey found that for adolescents (ages 13–17) more than for chil-ren (ages 6–12) or adults (ages 18–29), withholding a button pressas more difficult when the no-go stimulus was a happy face—a

ewarding stimulus—than when it was a calm face. In fact, onlydolescents showed impaired impulse control in the happy, rela-ive to the calm, no-go condition. The researchers proposed thatdolescents’ greater emotional response to the (rewarding) happyace made it harder for them to restrain the impulse to “approach” iti.e., press the “go” button). If so, these results support the proposi-ion that adolescents are particularly sensitive to reward. However,nother study (Tottenham et al., 2011) using a similar, but notdentical, Emotional Go/No-Go task did not find this pattern (i.e.,hey found no emotion by condition by age group interaction forrroneous button presses). Though there were methodological dif-erences between these two studies, the failure to find the effect inne of the two underscores the need for further research in thisein. It also highlights the benefits of being able to incorporateeuroimaging methods. Engagement of the socioemotional systemay not always be robust enough (especially in laboratory settings)

o consistently bias behavior. Neuroimaging enables researcherso detect age differences in the engagement of this system, evenbsent behavioral consequences.

.3. Neuroimaging of reward sensitivity

In recent years, many neuroimaging studies have asked whetherdolescents are particularly sensitive to reward. Beyond iden-ifying differences between adolescents and other age groups,hese studies help address questions about the neural mechanismsnderlying adolescents’ heightened reward-seeking. For example,mong those who agree that adolescents are more inclined thandults to seek out rewards, there has been disagreement overhether this results from the fact that rewards are experienced

s exceedingly pleasurable during adolescence (and are thereforeore enticing) or because they are experienced as less so (and are

herefore less satisfying). Indeed, one early notion, now largely dis-redited, posited that adolescents suffer from a “reward deficiencyyndrome” which impels them to seek out exciting experiencesecause mundane ones are not sufficiently rewarding, much likeddicts who seek out drugs because quotidian experiences noonger excite them (for a discussion, see Spear, 2002).

To date, most of the developmental neuroscience literature hasocused on developmental differences in the striatum, and morepecifically in the ventral portion of the striatum, which is con-idered one of the main regions involved in the calculation ofeward (Knutson et al., 2001; Luciana and Collins, 2012). In ourual systems account, increases in risk taking and other reward-eeking behaviors are thought to be a consequence of increasedngagement of the striatum during decision-making, thus biasing

Please cite this article in press as: Shulman, E.P., et al., The dual sysNeurosci. (2015), http://dx.doi.org/10.1016/j.dcn.2015.12.010

dolescents toward more rewarding choices. Heightened sensitiv-ty to rewarding outcomes of prior decisions may contribute todolescent risk-taking as well. There is evidence, for example, thathe volume of the nucleus accumbens (part of the ventral striatum

PRESSve Neuroscience xxx (2015) xxx–xxx

and presumed to be the central structure in the reward system)increases during the first part of adolescence and then shrinksthereafter (Luciana and Collins, 2012).

As discussed by Steinberg (2008), the neuroscience literatureincludes both studies that support and challenge the dual systemsaccount of heightened striatal engagement during adolescence(e.g., Bjork et al., 2004; Galvan et al., 2006). Since that 2008 publi-cation, several reviews have discussed methodological differencesacross these studies that may have contributed to the inconsistentfindings (see Galvan, 2010; Richards et al., 2013). Indeed, the devel-opmental neuroimaging literature on reward processing has grownsubstantially over the last several years, and we believe there arepatterns to be noted, and conclusions to be drawn, that help explainwhat appear to be contradictory findings.

In its current state, the literature provides considerable evi-dence that when developmental differences in striatal activationare present during reward processing (both during the anticipa-tion and the receipt of reward) adolescents engage the striatum toa greater extent than both children and adults (Barkley-Levensonand Galvan, 2014; Christakou et al., 2011; Galvan and McGlennen,2013; Galvan et al., 2006; Geier et al., 2010; Hoogendam et al., 2013;Jarcho et al., 2012; Padmanabhan et al., 2011; Silverman et al., 2015;Van Leijenhorst et al., 2010b). For example, a recent longitudinalstudy found that, across mid-adolescence (roughly ages 15–18),ventral striatal activation in response to “risk taking” on the bal-loon analogue task (which also reflects reward-seeking) declinesintra-individually over time, and that striatal activation during thetask is correlated with self-reported risk taking outside the lab-oratory (Qu et al., 2015). However, a handful of studies find theopposite pattern—dampened striatal response during adolescencerelative to adulthood (Bjork et al., 2004, 2010; Hoogendam et al.,2013; Lamm et al., 2014)—and others fail to demonstrate any agedifferences (Krain et al., 2006; Teslovich et al., 2014; Van Leijenhorstet al., 2006).

In trying to explain this inconsistency, it is important to notethat disparate findings emerge only for contrasts that focus on theanticipation of a reward. Studies focusing on striatal engagementduring the receipt of a reward consistently find that adolescentsengage the striatum to a greater extent than adults (Galvan andMcGlennen, 2013; Hoogendam et al., 2013; Van Leijenhorst et al.,2010b), suggesting that adolescents are—as the dual systems modelclaims—more sensitive to rewarding outcomes.

The fact that striatal engagement is relatively higher among ado-lescents than among children or adults during receipt of rewardsbut not necessarily during reward anticipation potentially chal-lenges our conception of adolescent risk taking as being drivenby the prospect of a reward. However, nuances in task design,modeling of the anticipatory event in imaging analyses, and therelationship between striatal engagement and behavioral rewardsensitivity may account for these seemingly inconsistent results,for several reasons. First, the time points at which events are mod-eled, and the specific trial periods that are included within themodel, can dramatically affect the observed neural response (e.g.,Geier et al., 2010). One factor that seems to differentiate studiesthat do and don’t report increased adolescent engagement of thestriatum during reward anticipation is the degree to which antic-ipatory cues reliably predict the delivery of the reward. Studiesusing a task design in which the reward cue signals not only theopportunity for reward, but also an increased likelihood of earningthat reward, tend to find increased adolescent activity in the stria-tum during anticipation (e.g., Barkley-Levenson and Galvan, 2014;Van Leijenhorst et al., 2010b). Meanwhile, studies using tasks for

tems model: Review, reappraisal, and reaffirmation. Dev. Cogn.

which the anticipatory cue signals the possibility to earn a reward,but is equivocal with respect to the likelihood of succeeding inobtaining the reward (as in typical implementations of the Mon-etary Incentive Delay task), do not yield a consistent pattern of

dx.doi.org/10.1016/j.dcn.2015.12.010

ING ModelDogniti

d2

iirrWidoeeiacdsfi

etpIlvMctFgricwso(

tcSi(Fdpimapeti

wbiite2L(

n

ARTICLECN-338; No. of Pages 15E.P. Shulman et al. / Developmental C

evelopmental differences (e.g., Bjork et al., 2007; Teslovich et al.,014).

Second, developmental findings regarding striatal outputs dur-ng reward anticipation are more consistent in studies where theres also concomitant behavioral evidence that the adolescents areelatively more sensitive to the rewards being presented (e.g., fastereaction times on rewarded trials, more reward-related errors, etc.).

hile most reward processing tasks used in neuroimaging stud-es do not include a behavioral measure or control for behavioralifferences in reward sensitivity across development, the handfulf studies that do (Barkley-Levenson and Galvan, 2014; Christakout al., 2011; Geier et al., 2010; Padmanabhan et al., 2011; Somervillet al., 2011) all report both greater recruitment of the striatum dur-ng anticipation of reward and higher reward sensitivity amongdolescents compared to adults, reflected in the behavioral out-omes. Unfortunately, the majority of reward tasks used in theevelopmental literature lack a useful behavioral index of rewardensitivity—an issue that may also account for variability in striatalndings across development.

Our lab recently explored how socioemotional arousal influ-nces adolescents’ neural responses to reward by testing whetherhe presence of peers increased striatal activation during a reward-rocessing task in which no risk was involved (Smith et al., 2015).

n this study, we examined the effects of peer observation on ado-escents’ and adults’ neural response to reward using a modifiedersion of the High/Low Card Guessing Task (Delgado et al., 2003;ay et al., 2004). During the receipt of reward, adolescents who

ompleted the task in the presence of their peers recruited the stria-um to a greater degree than when they completed the task alone.urthermore, only when peers were present did adolescents evincereater striatal activation than adults. These findings provide cor-oborating evidence that, during adolescence, social context is anmportant modulator of reward processing, even when this pro-essing is uncoupled from risk taking. Consistent with this claim,e have shown that, in the presence of peers, adolescents evince a

tronger preference for immediate (as opposed to delayed) rewardsn a Delay Discounting task that does not involve risk takingO’Brien et al., 2011; Weigard et al., 2014).

Recent neuroimaging studies also support the idea that, in addi-ion to having profound effects on brain structure [a topic notovered in the present article; see Blakemore et al. (2010) andmith et al. (2013) for reviews], pubertal development plays a rolen developmental change in the sensitivity of the striatum to rewardBraams et al., 2015; Forbes et al., 2010; Op de Macks et al., 2011).or example, a landmark, longitudinal neuroimaging study of chil-ren, adolescents and young adults (N = 299, ages 8–27) found, asrevious studies have, that activation of the nucleus accumbens

n response to monetary reward (relative to loss) was higher inid-adolescence than at other ages (Braams et al., 2015). Moreover,

ctivation of this region was related both to greater self-reportedubertal stage and higher levels of salivary testosterone (Braamst al., 2015). This finding provides strong support for the claim thathe heightened responsiveness of the socioemotional system dur-ng adolescence is, at least in part, a result of pubertal development.

Thus far, we have discussed reward sensitivity specificallyith respect to striatal activation. However, there also have

een advances in how we understand developmental changesn the functioning of other regions hypothesized to participaten reward processing, including the dorsal portion of the stria-um (Benningfield et al., 2014; Hoogendam et al., 2013; Lammt al., 2014), mPFC (Christakou et al., 2011), OFC (Galvan et al.,006; Galvan and McGlennen, 2013; Hoogendam et al., 2013; Van

Please cite this article in press as: Shulman, E.P., et al., The dual sysNeurosci. (2015), http://dx.doi.org/10.1016/j.dcn.2015.12.010

eijenhorst et al., 2010b), and the anterior insular cortex (AIC)Galvan and McGlennen, 2013; Van Leijenhorst et al., 2010b).

In a recent paper, we posited that continuing maturation of con-ectivity between the striatum and the AIC, which appears to act

PRESSve Neuroscience xxx (2015) xxx–xxx 7

as connective hub that influences the engagement of both the con-trol and reward processing networks, may account for inconsistentrecruitment of the striatum in adolescent reward processing (Smithet al., 2014b). Because reward processing entails the coordinatedaction of a network of regions, developmental studies examiningthe reward system as a whole, rather than focusing on activa-tion of specific regions considered in isolation, will likely yieldgreater insight into changes in reward processing during adoles-cence, including the reasons for the inconsistent recruitment of thestriatum in adolescent reward processing (Smith et al., 2014b).

One study has already demonstrated the potential value ofsuch a network-based approach. Using resting state data, Cho andcolleagues (2012) examined functional connectivity between thestriatum, thalamus, and AIC as adolescents and adults completeda reward processing task. They found that during anticipation ofreward (i.e., during cue presentation) adolescents and adults didnot differ in the functional connectivity between these regions. Fur-ther, they observed that activity in the AIC and thalamus precededVS activation in both adolescents and adults. These results sug-gest that the bottom-up processing of rewards (as demonstrated bycommunication between these three regions) is adequately devel-oped by adolescence. Therefore, it may be that developmentaldifferences between adolescents and adults in reward sensitivityare not due to immature connectivity, but rather to differencesin top-down influences on the subjective valuation of reward.More studies considering the socioemotional system as a coordi-nated network are needed to inform our understanding of how thedevelopment of this system relates to age-differences in rewardprocessing.

In summary, despite occasional inconsistencies in the literature,self-reported sensation seeking, behavioral measures of rewardsensitivity, and neuroimaging studies of reward processing sup-port the contention that reward sensitivity reaches its apex duringadolescence (e.g., Barkley-Levenson and Galvan, 2014; Christakouet al., 2011; Collado et al., 2014; Galvan and McGlennen, 2013;MacPherson et al., 2010; Shulman et al., 2014a,b; Somerville et al.,2011; Van Leijenhorst et al., 2010b). The bulk of developmen-tal research on this topic provides evidence for a mid-adolescentpeak in reward sensitivity, and although the neuroimaging litera-ture does not allow for a precise estimation of age of peak striatalresponse, the weight of the evidence indicates that adolescentsengage the striatum (and other components of the reward net-work) to a greater extent than adults, particularly during receiptof reward and when differences in reward sensitivity are reflectedin decision-making behavior. Also consistent with the dual systemsaccount, studies that have incorporated measures of puberty typi-cally find that sensation seeking and reward sensitivity are higheramong those (particularly boys) who are more pubertally advanced.

5. The development of self-regulation and cognitive control

5.1. Self-reported impulsivity

A second major claim of the dual systems model is that cognitivecontrol increases linearly across adolescence and does not reachfull maturity until several years after the peak period of rewardsensitivity. In the developmental literature, impulse control (or itsinverse, impulsivity) is the psychological variable most often usedto assess self-regulation (or its absence). Impulsiveness—actingin an unplanned and reactive, or less thought out, fashion—isoften considered a quintessential adolescent characteristic that

tems model: Review, reappraisal, and reaffirmation. Dev. Cogn.

predisposes adolescents to engage in reckless behaviors (Romer,2010). To date, studies examining age differences in self-reportedimpulsivity—both cross-sectional (Leshem and Glicksohn, 2007;Steinberg et al., 2008) and longitudinal (Harden and Tucker-Drob,

dx.doi.org/10.1016/j.dcn.2015.12.010

ING ModelD8 ogniti

2d

bovsflQssf

5

rio2(crastct122

dhsccasti(itritrmngantbii2

rdrpa2

ARTICLECN-338; No. of Pages 15 E.P. Shulman et al. / Developmental C

011)—find that impulsivity decreases with age across the secondecade of life.

Importantly, the protracted maturation of impulse control iselieved to continue into young adulthood, where even 18–19 yearlds report higher impulsivity (i.e., less impulse control) than indi-iduals in their early twenties (Vaidya et al., 2010). Although adultsometimes engage in impulsive acts, by the early-to-mid 20s therequency of impulsive behavior appears to stabilize at levels muchower than those exhibited by adolescents (Steinberg et al., 2008;uinn and Harden, 2013). For example, using a three-item impul-

ivity scale, Quinn and Harden (2013) found a linear decrease inelf-reported impulsivity between the ages of 15 and 21, but nourther age differences among individuals between 21 and 25.

.2. Behavioral measures of self-regulation

Self-regulation is commonly assessed in behavioral tasks thatequire response inhibition, a form of cognitive control thatnvolves overcoming automatic or inappropriate responses in favorf goal-relevant information processing and actions (Casey et al.,002). The most widely used measures of response inhibitione.g., Go/NoGo, antisaccade, and Stroop paradigms) are typicallyonfigured to assess “reactive inhibition,” which refers to the out-ight restraint of motor and perceptual impulses in response ton external stimulus (e.g., canceling a prepotent response uponeeing a signal, or maintaining attention in the presence of dis-ractions). A wealth of behavioral evidence on reactive inhibitoryontrol demonstrates that self-regulation improves from childhoodo adulthood (Bezdjian et al., 2014; Bunge et al., 2002; Casey et al.,997, 2002; Durston et al., 2002; Marsh et al., 2006; Paulsen et al.,015; Rubia et al., 2006, 2013; Smith et al., 2011a; Tamm et al.,002; Velanova et al., 2009; Veroude et al., 2013).

Within this literature, adolescents and adults consistentlyemonstrate better inhibitory control compared to children;owever, differences between adolescents and adults are not con-istently found unless the behavioral paradigm is particularlyhallenging. For example, studies that use the traditional Stroopolor-word task find no differences in cognitive control betweendolescents and adults (e.g., Andrews-Hanna et al., 2011), whereastudies that use an emotional version of the Stroop to assesshe effect of emotional interference in cognitive control reportmprovements in self-regulation from adolescence to adulthoode.g., Veroude et al., 2013). Thus, while adolescents’ ability to inhibitmpulses appears to be comparable to adults’ in relatively simpleasks, the sort of self-regulatory skills necessary to appropriatelyespond to more cognitively demanding situations continue tomprove from adolescence to adulthood. This developmental pat-ern is also observed in measures of proactive (as opposed toeactive) inhibitory control, which involves advance planning andonitoring in anticipation of the need to stop a response or to

ot engage in a future action (e.g., slowing down responses too-stimuli in anticipation of a no-go signal approaching, thereforellowing more time to appropriately cancel a response when theo-go signal appears; Vink et al., 2014). These findings suggesthat while basic response inhibition mechanisms may be maturey adolescence, self-regulatory mechanisms underlying challeng-

ng reactive response inhibition tasks and proactive responsenhibition (e.g., planning) may still be developing into the early0s.

The proposition that the prolonged development of self-egulation is more evident under challenging conditions has beenemonstrated using the Tower of London task. In this task, which

Please cite this article in press as: Shulman, E.P., et al., The dual sysNeurosci. (2015), http://dx.doi.org/10.1016/j.dcn.2015.12.010

equires strategic planning, participants must rearrange objects onegs (either real or depicted on a computer monitor) to produce

specific pattern in the fewest possible moves (De Luca et al.,003; Steinberg et al., 2008). Researchers manipulate the difficulty

PRESSve Neuroscience xxx (2015) xxx–xxx

of trials by increasing the number of moves required to completethe rearrangement successfully. The amount of time a participantspends deliberating before making his or her first move (latencyto first move) is used as a measure of impulse control (becausemaking an initial move too rashly can extend the number of movesneeded to solve the problem). A study from our lab found no dif-ferences between children, adolescents, and adults in latency tofirst move or in the number of moves taken to complete the trialon easy trials (i.e., those that can be solved in 3 moves) (Albertand Steinberg, 2011). However, on difficult trials (i.e., those thatrequired 5 or more moves to be solved), performance improvedwith age from childhood to adulthood, and this trend coincidedwith greater deliberation time prior to the initial move. These find-ings suggest that when difficult tasks are used, such as those thatrequire strategic planning, improvement in self-regulation contin-ues throughout adolescence and into the early 20s, consistent withthe dual systems model.

Importantly, the ongoing development of self-regulation intoearly adulthood is also in line with the idea that the develop-ment of self-regulation is independent of pubertal development(Smith et al., 2013). In the most comprehensive test of the rela-tionship between self-regulation, and pubertal status Steinbergand colleagues (2008) found that self-reported and behavioral self-regulation was correlated with age but not pubertal status. Instead,pubertal status was more closely tied to sensation seeking. Whilethis is the only study we know of that simultaneously examinesthe relationship between age, pubertal status, self-regulation, andsensation seeking, thus far the findings support the notion that thedevelopment of the socioemotional system is dependent on puber-tal status while self-regulation seems to develop independently.

Other findings suggest that adolescents’ ability to exert adult-like self-control also may vary depending on whether rewards areoffered for better performance (Luna et al., 2001). In several stud-ies that have rewarded participants for better performance on anantisaccade task, researchers have found that incentives boost ado-lescents’ performance to adult levels (Geier et al., 2010; Jazbec et al.,2006; Padmanabhan et al., 2011). For example, using an antisac-cade task where some trials were rewarded and some were not,Geier and colleagues (2010) found that adolescents performed bet-ter on rewarded trials, compared to non-rewarded trials, thoughtheir overall task performance did not differ from that of adults.At first blush, it may appear that these results are incompatiblewith the dual systems model, since its basic claim is that height-ened awareness of the availability of rewards should underminecognitive control in adolescents, not strengthen it. It is importantto note, though, that this proposition of the dual systems modelis posited specifically with respect to situations in which reward-seeking impulses conflict with self-regulatory efforts, as do mostinstances of risk taking. In contexts where increased sensitivityto the opportunity for reward serves to motivate faster and moreattentive responding, without disturbing relevant cognitive pro-cesses, adolescents’ relatively heightened sensitivity to reward maybe helpful rather than harmful. For that matter, even in certain risk-taking scenarios—in particular, those in which increased risk takingresults in more optimal performance, such as in certain gamblingtasks for which risky choices have a higher expected value—greaterreward sensitivity can offer an advantage.

Overall, the self-report and behavioral literatures on self-regulation suggest that this capacity improves with age acrosschildhood, adolescence, and into adulthood. Furthermore, it maybe that adolescents’ ability to self-regulate is more dependent thanadults’ on contextual factors, such as task difficulty, the prospect

tems model: Review, reappraisal, and reaffirmation. Dev. Cogn.

of a reward for better self-control, and the manner in whichrewards are presented. Although adolescents may exhibit adult-like self-regulation under ideal circumstances by around age 15,this capacity is still tenuous, and maturation of self-regulation may

dx.doi.org/10.1016/j.dcn.2015.12.010

ING ModelDogniti

bs

tviiaaltf(

5

diitwmcecws

isw2oamw2Tnatbf2R

aarcBefnaihfh“ofcau

ARTICLECN-338; No. of Pages 15E.P. Shulman et al. / Developmental C

e best indexed by the consistency with which individuals demon-trate self-control across different contextual circumstances.

As we have noted previously (Strang et al., 2013), it is imprudento conclude that heightened reward sensitivity is inherently disad-antageous, or that impulsivity is always problematic. In situationsn which greater attentiveness to reward or more impetuous behav-or is desirable, adolescents may enjoy a distinct advantage overdults. Indeed, one of the tenets of the dual systems model is thatdolescence evolved as a period during which individuals are moreikely to engage in sensation seeking and less likely to restrain urgeso pursue immediate rewards because this combination may con-er a reproductive advantage during a period of heightened fertilitySteinberg, 2014).

.3. Neuroimaging of cognitive control

In recent years, developmental neuroimaging has helped eluci-ate the neural mechanisms underlying age-related improvements

n cognitive control. Continuing maturation of response inhibitions often examined in terms of development of the prefrontal cor-ex, and particularly the lateral prefrontal cortex (lPFC). In lineith the dual systems framework, we postulate that develop-ental improvements in cognitive control are supported by the

oncurrent maturation of these underlying neural regions and bynhancements in top-down connectivity between frontal cognitiveontrol regions and other cortical and subcortical areas associatedith motor processing, affective processing, and the execution of

elected actions.Irrespective of age, individuals who perform better on response

nhibition tasks (i.e., Go/No-Go, Flanker, Stroop, Stop Signal, anti-accade) exhibit greater activation of the lPFC compared to thoseho perform poorly (Durston et al., 2006; Rubia et al., 2006,

013; Velanova et al., 2009). Across adolescence, performancen response inhibition tasks improves with age—a pattern thatppears to be explained by continuing maturation of the lPFC, withost studies finding either a linear increase in lPFC recruitmentith age (Adleman et al., 2002; Bunge et al., 2002; Durston et al.,

006; Marsh et al., 2006; Paulsen et al., 2015; Spielberg et al., 2015;amm et al., 2002; Velanova et al., 2009; Vink et al., 2014) or sig-ificantly increased engagement of the lPFC from adolescence todulthood (Rubia et al., 2000, 2006, 2013; Veroude et al., 2013). Fur-hermore, several studies have demonstrated a direct relationshipetween age-related increases in lPFC engagement and success-ul cognitive control (Adleman et al., 2002; Andrews-Hanna et al.,011; Bunge et al., 2002; Casey et al., 1997; Durston et al., 2006;ubia et al., 2006, 2007, 2013; Velanova et al., 2009).

Whereas the behavioral and neuroimaging literatures gener-lly indicate a relationship between increases in cognitive controlnd engagement of the lPFC from adolescence into adulthood, theelationship between age, behavior, and neural engagement fromhildhood to adolescence is not as consistent (Alahyane et al., 2014;ooth et al., 2003; Braet et al., 2009; Casey et al., 1997; Durstont al., 2002). In fact, some studies find that children utilize morerontal regions than adults—in terms of overall volume and/or mag-itude of activity—in order to successfully withhold a prepotentction. These findings have led researchers to posit that increasesn self-regulation from childhood to adolescence and into adult-ood may be due to a developmental progression from diffuse to

ocal activation (Durston et al., 2002). In this account, during child-ood and early adolescence, the brain is inefficient and needs towork harder,” recruiting neurons across a larger frontal area inrder to successfully inhibit a response (though see Poldrack, 2014

Please cite this article in press as: Shulman, E.P., et al., The dual sysNeurosci. (2015), http://dx.doi.org/10.1016/j.dcn.2015.12.010

or a critique of the explanatory value of the term “efficiency” in thisontext). As the brain undergoes continued reorganization acrossdolescence, necessary neural connections are strengthened andnnecessary ones are pruned, creating a more efficient brain and

PRESSve Neuroscience xxx (2015) xxx–xxx 9

leading to more focal recruitment of regions within the lPFC duringsuccessful inhibition.

Cognitive control encompasses the integration of several (oftensimultaneous) processes that support planning behavior in accordwith one’s intentions (Miller, 2000). The effective integration ofthese processes relies not only on the functional recruitment ofimplicated brain regions, but also on the strength of connectiv-ity among them (Hwang et al., 2010; van Belle et al., 2014). Forexample, a study by Hwang and colleagues (2010) examined devel-opmental changes in connectivity underlying inhibitory controland found that connectivity between the prefrontal cortex andother cortical areas increased from childhood into adolescence,with some connections continuing to strengthen from adoles-cence to adulthood. The increases they observed in the numberand strength of frontal connections to both cortical and subcorti-cal regions during the transition from adolescence into adulthoodsuggest that developmental improvements in cognitive controlmay be supported by age related enhancements in the top-downregulation of task-engaged regions. Results such as these under-score the potential benefit to the field of fMRI studies movingbeyond simplistic models of regional activation toward more elab-orate models that consider connectivity among regions throughoutdevelopment, as well as the strength and efficiency of thoseconnections, which likely support age-related increases in theacquisition and execution of complex cognitive control skills (see,e.g., Satterthwaite et al., 2013). This is particularly true because, asnoted earlier, there is reason to believe that continuing changes inconnectivity account for the observation that some aspects of cog-nitive control continue to strengthen into early adulthood, insteadof plateauing in adolescence.

6. Is risk taking during adolescence related to heightenedreward sensitivity and immature cognitive control?

As reviewed above, research largely supports the dual systemsmodel’s characterization of adolescence as a time of heightenedsocioemotional reactivity (relative to earlier and later periods) andstill maturing cognitive control. Moreover, there is considerableevidence consistent with the proposition that the developmen-tal trajectories of reward sensitivity and cognitive control (and,by extension, sensation seeking and self-regulation) differ, withthe former following an inverted U-shaped pattern and the latterevincing protracted, linear improvement that extends into the thirddecade of life.

How well does the literature support the claim that devel-opmental change in these two systems explains heightened risktaking during adolescence? The model posits that it is the con-fluence of the developmental patterns of the socioemotionaland cognitive control systems—relatively high responsiveness toreward combined with relatively weak self-regulation—that ren-ders adolescents particularly vulnerable to risk taking. If the twosystems contribute to risk taking in an additive manner, we shouldfind independent correlations between the functional state of eachsystem and risk-taking propensity. Indeed, there is evidence for thispattern in the literature.

In order to serve as a test of the dual systems model in predict-ing risk taking, a behavioral study must include measures of bothsocioemotional reactivity and cognitive control. Unfortunately,constructs reflecting the functional status of the socioemotionaland cognitive control systems, like sensation seeking and impulsiv-ity, tend to be highly correlated (e.g., Shulman and Cauffman, 2014;

tems model: Review, reappraisal, and reaffirmation. Dev. Cogn.

Steinberg et al., 2008), despite being theoretically and empiricallyseparable (Duckworth and Kern, 2011; Duckworth and Steinberg,2015). Thus, for studies that examine the relationship betweenonly one of these constructs and risk taking, the correlation will

dx.doi.org/10.1016/j.dcn.2015.12.010

ING ModelD1 ogniti

bSmseeaotgrmiscthlwe

rstov(Fsu2dohadsu2a2teoeapolra

srcdfecCDftc(f

ARTICLECN-338; No. of Pages 150 E.P. Shulman et al. / Developmental C

e contaminated by the contribution of the unmeasured construct.ome of this overlap between sensation seeking and self-regulationay be artifactual—a result of the difficulty of developing mea-

ures that cleanly assess one construct and not the other. (Forxample, items like “I often get myself into trouble” could reflectither sensation seeking or impulsivity.) But some of the observedssociation between these constructs may be attributable to anngoing dynamic interplay between the socioemotional and cogni-ive control systems; for example, when the socioemotional systemenerates an impulse to pursue an intrinsically rewarding expe-ience and the cognitive control system counters with a signaleant to restrain the impulse. Although a large number of stud-

es have examined risky behavior in relation to measures of eitherensation seeking or impulse control, very few have examined theoncurrent contributions to risk taking of psychological manifesta-ions of socioemotional activation and cognitive control. Even fewerave examined this question in a sample spanning childhood, ado-

escence, and adulthood, which would be necessary to fully testhether variation in the functional status of these two systems

xplains age-related patterns in risk taking.In the few studies that have simultaneously assessed constructs

eflective of the socioemotional and cognitive control systems (e.g.,ensation seeking and impulse control) along with measures of riskaking, the anticipated correlations are found. Both higher levelsf sensation seeking and lower levels of impulse control explainariation in risk taking, over and above the effects of one anotherCyders et al., 2009; Donohew et al., 2000; Quinn and Harden, 2013).or example, one study of college students found that sensationeeking uniquely predicted increases in the frequency of alcoholse, over and above several measures of impulsivity (Cyders et al.,009). Another found that both sensation seeking and “impulsiveecision making” were independently associated with greater oddsf ninth-graders engaging in sex, non-coital sexual behavior, alco-ol use, and marijuana use (Donohew et al., 2000). Moreover, thesessociations were comparable in magnitude, except that impulsiveecision-making was more strongly associated with having sex andensation seeking was more strongly associated with marijuanase. Similarly, unpublished data from our lab—based on a sample of83 10–30-year olds and using a scale that surveyed involvement in

wide range of risk-taking behaviors (see Shulman and Cauffman,014)—suggests that impulse control and sensation seeking con-ribute equally (betas = −.21 and .21, respectively) to self-reportedngagement in risky behaviors (controlling for age, sex, and eachther). An obvious shortcoming of these studies is that they relyxclusively on self-report. However, if common method variancelone were driving the findings, one would not expect to see inde-endent relations between risk taking and either sensation seekingr impulsivity once the other predictor was controlled. Anotherimitation of these studies is that it is not yet clear how well self-eport measures reflect the functional status of the socioemotionalnd cognitive control systems.

Neuroimaging studies have the advantage over behavioraltudies of being able to measure activation within distinguishableegions thought to correspond to the socioemotional and cognitiveontrol systems (although heightened activity in these regionsuring a laboratory task does not constitute a direct measure of theunctional status of these systems). A few studies have examinedngagement of regions associated with the socioemotional and/orognitive control systems during adolescent decision making (e.g.,ascio et al., 2015; Kahn et al., 2015; Paulsen et al., 2011; vanuijvenvoorde et al., 2015b). However, only Chein et al. (2011)

ound increased engagement of structures within the socioemo-

Please cite this article in press as: Shulman, E.P., et al., The dual sysNeurosci. (2015), http://dx.doi.org/10.1016/j.dcn.2015.12.010

ional system and decreased activation of structures within theognitive control system simultaneously within a risk-taking taska driving simulation). One additional study (Paulsen et al., 2011)ound age effects in both the PFC and striatum during risk taking.

PRESSve Neuroscience xxx (2015) xxx–xxx

During risky (i.e., varying expected values) compared to sure(i.e., guaranteed reward) decisions, several PFC regions showedincreased activation with age, consistent with Chein et al. (2011).On the other hand, striatal activation was inconsistent, makingthese results difficult to interpret.

Another recent study examined the extent to which age differ-ences in impatience during a temporal discounting task—in whichparticipants choose between a smaller immediate reward and alarger delayed reward—are explained by variations in self-reported“present hedonism” (i.e., reward sensitivity) and “future orien-tation” (i.e., impulse control) and engagement of neural regionsand networks during decision making (van den Bos et al., 2015).Though the decision making task did not involve risk, the studyis nonetheless relevant to the dual systems model because it wasdesigned to probe the degree to which adolescents’ tendency todiscount the future is due to greater reward sensitivity or weakerself control. The results indicated that choices to delay gratifica-tion in the decision task were associated with greater self-reportedfuture orientation and increased engagement of frontoparietal con-trol circuitry, but not with variation in self reported hedonism.Also, improvements in frontostriatal connectivity mediated thelink between age and willingness to wait for a larger reward. Theauthors interpreted these results as showing that weak cognitivecontrol, rather than heightened reward sensitivity, explains ado-lescents’ tendency to discount the future. However, limitations ofthe methodology (e.g., limited range on the present hedonism scale,lumping immediate rewards together with rewards to be receivedin two weeks for analysis of the discounting data, and the unemo-tional context of the laboratory) may have biased the study againstfinding linkages between reward sensitivity and impatience (seeSteinberg and Chein, 2015).

Whereas other studies have not demonstrated simultaneouslyheightened socioemotional activation and dampened cognitivecontrol within the same task, a few recent ones have observedheightened striatal activation when adolescents receive a rewardfollowing a decision (Braams et al., 2014, 2015). In one furtherrelevant study (Cascio et al., 2015), researchers recruited recentlylicensed drivers (∼age 16) to complete a response inhibition taskand, one week later, a driving simulation in the presence of a peerconfederate. The peer either encouraged risky driving or safe driv-ing. In the latter condition (encouragement of safe driving), greaterengagement of cognitive control circuitry (i.e., IFG and BG) duringthe response inhibition task (indicative of better cognitive control)predicted safer driving behavior in the simulated driving task. Par-ticipants who exhibited higher cognitive control also showed noincrease in risky driving in the condition in which the peer encour-aged risk taking, suggesting that individuals who evince greaterengagement of cognitive control circuitry may be more resistantsocioemotional arousal. These findings indicate that poor cogni-tive control, as expected, also plays a role in risk-taking behavior.However, because the study did not compare age groups, it cannotaddress whether maturation of cognitive control helps to accountfor developmental patterns in risk taking.

In another recent study, van Duijvenvoorde and colleagues(2015b) had children, adolescents, and adults complete a risk-taking task (Columbia Card Task). While overall risk-takingtendency did not differ by age, adolescents showed greater acti-vation of control circuitry (including the dmPFC) as the riskinessof the decision increased. This effect was not seen in children oradults. The authors suggest that heightened recruitment of controlcircuitry was necessary due to the heightened emotional responseto risk during this age. Although there is good reason to believe

tems model: Review, reappraisal, and reaffirmation. Dev. Cogn.

that the functional status of both the socioemotional and cognitivecontrol systems during adolescence contribute to heightened risktaking during this stage of development, the dual systems modelstill awaits a comprehensive study that confirms (or disconfirms)

dx.doi.org/10.1016/j.dcn.2015.12.010

ING ModelDogniti

ttb

7

fFbtrUriitimtvncrpt

taeoemcceswerhensoNedocaan2r(tflmm

ao

ARTICLECN-338; No. of Pages 15E.P. Shulman et al. / Developmental C

he purported joint effects of the developmental trajectories ofhe socioemotional and cognitive control systems on risk-takingehavior.

. Unresolved questions and future directions

There are many unresolved issues in the literature that awaiturther research attention. Here we highlight just a few of them.irst, because of differences in opportunity to engage in riskyehavior outside the laboratory environment, the effects of matura-ion of the socioemotional system and cognitive control system oneal-world risk taking are likely to be modest and difficult to detect.ndoubtedly, contextual constraints on the behavior of adolescents

elative to adults overwhelm any putative effect on actual risk tak-ng. To take an obvious example, even if 15-year-olds are highern sensation seeking and lower in self-regulation than people inheir 20s, these differences will not be reflected in age differencesn reckless driving in a country where 15-year-olds are not per-

itted to drive. Thus, tests of the dual systems model will requirehe continued development of laboratory tasks that are ecologicallyalid but that afford individuals of different ages equal opportu-ity to take risks. Future efforts to test the dual systems model’slaims also would benefit from collaboration between behavioralesearchers and neuroscientists to develop measures that morerecisely reflect the functioning of the neural systems underlyinghe socioemotional and cognitive control systems.

Second, still unresolved is the question of why the socioemo-ional system declines in responsiveness between adolescence anddulthood. Luciana and Collins (2012) have speculated that experi-nce with rewards and learning lead to lower background levelsf dopamine, a proposition that has not yet been tested. Caseyt al.’s (2008) model implies that decreases in risk taking after theaturation of the socioemotional system, which in their view is

omplete by mid-adolescence, are ultimately attributable to theontinued strengthening of the cognitive control system. Given thevidence of reduced reward responsiveness in the key node of theocioemotional system in adulthood (relative to adolescence), itould seem that their version of the model suggests that strength-

ning of the cognitive control system prospectively dampens theeactivity of the socioemotional system. One study from our labas tested this hypothesis: Shulman et al. (2014b) examined theffects of self-reported impulse control (a reflection of the cog-itive control system) and sensation seeking (a reflection of theocioemotional system) on one another over time in a large samplef youth, ages 10–25, who were assessed biennially as part of theLSY79 Children and Young Adults Study. The analysis failed to findvidence that increases in impulse control prospectively predictecreases in sensation seeking; in general, these two traits devel-ped independently. Recently, a neuroimaging study using intrinsiconnectivity found that increases in dlPFC-subcortical (thalamusnd striatum when not controlling for age2) connectivity acrossdolescence were associated with increases in cognitive control butot with decreases in reward sensitivity (van Duijvenvoorde et al.,015a). Instead, decreases in reward sensitivity were related to age-elated decreases in connectivity within the socioemotional systemvmPFC, OFC, and striatum). Together these findings lend supporto the notion that these traits develop independently. However,urther investigation of this question is warranted; in particular,

Please cite this article in p