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Understanding adolescence as a period of


social-affective engagement and goal flexibility

Article in Nature Reviews Neuroscience August 2012


DOI: 10.1038/nrn3313 Source: PubMed

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Understanding adolescence
as a period of socialaffective
engagement and goal flexibility
Eveline A.Crone1* and Ronald E.Dahl2*
Abstract | Research has demonstrated that extensive structural and functional brain
development continues throughout adolescence. A popular notion emerging from this work
states that a relative immaturity in frontal cortical neural systems could explain adolescents
high rates of risk-taking, substance use and other dangerous behaviours. However,
developmental neuroimaging studies do not support a simple model of frontal cortical
immaturity. Rather, growing evidence points to the importance of changes in social and
affective processing, which begin around the onset of puberty, as crucial to understanding
these adolescent vulnerabilities. These changes in socialaffective processing also may
confer some adaptive advantages, such as greater flexibility in adjusting ones intrinsic
motivations and goal priorities amidst changing social contexts in adolescence.

Cognitive control
Adolescence, which is defined as the transition phase transition to becoming an independent and responsible
A set of neurocognitive between childhood and adulthood, is a natural time of adult is inherently intertwined with adjustments in per-
processes that are important learning and adjustment, particularly in the setting of sonal goals and motivations for example, developing
for achieving short- and long-term goals and personal aspirations (BOX1). It also is priorities related to career, identity, friends, romantic
long-term goals, particularly
a time when youths are discovering how to navigate new, partners, family, community and religious or philo-
when individuals are required
to adjust their thoughts and often compelling, social challenges and are adjusting to sophical beliefs. This developmental transition involves
actions adaptively in response myriad physical, cognitive and emotional changes within greater use of cognitive control skills, such as the use of
to changing environmental themselves1,2. The onset of adolescence is characterized top-down effortful control to modify attention, emo-
demands in order to achieve
by the start of pubertal maturation, which typically tion and behaviour in service of long-term adult goals.
their goal.
begins between 9 and 12years of age (usually 12years However, social and affective processes also have crucial
earlier in girls than in boys). The onset of puberty creates roles in these maturational changes5,6. An adolescents
a cascade of hormonal changes including dramatic success in pursuing long-term academic, athletic or
increases in the secretion of adrenal androgens, gonadal artistic goals, for example, typically requires motivation
steroids and growth hormone (BOX2). This surge in hor- to practice the relevant skills and a desire to persevere
mones has a central role within a larger set of biological through difficulties, and these motivations are shaped by
changes in the process of achieving reproductive matu- social experiences and are inherently intertwined with
1
Department of Psychology,
rity. These changes include: rapid physical growth; sexu- individual feelings about the value and relative priority
Leiden University, ally dimorphic alterations in facial structure, voice and of thegoal.
Wassenaarseweg 52, body characteristics; metabolic changes; the activation of There has been growing interest in understanding
2333AK, The Netherlands. new drives and motivations; changes in sleep and circa- the neural changes that underpin these complex devel-
2
Institute of Human
dian regulation; and a wide array of social, behavioural opmental processes. This has led to exciting scientific
Development, University
ofCalifornia, Berkeley, and emotional changes3. advances at this nexus of cognitive neuroscience, social
California 94707, USA. Although the beginning of adolescence is character- neuroscience and developmental science. Investigations
e-mails: ized by distinct and dramatic physiological changes, the into these neuromaturational changes also hold prom-
rondahl@berkeley.edu; end of adolescence has less clear biological boundaries. ise for addressing some of the high-impact negative
ECrone@FSW.leidenuniv.nl
*All authors contributed
Attaining adulthood involves changes in social roles health problems that emerge in adolescence, including
equally to this work. and responsibilities, is partly culturally defined and increased rates of accidents, alcohol and drug use, teen-
doi:10.1038/nrn3313 typically extends into the early twenties4 (BOX1). This age pregnancies, depression and suicide, and violence79.

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Box 1 | Adolescence from an anthropological perspective


and social development during adolescence has increased
tremendously. As will be reviewed, there has also been
There is a commonly cited myth that adolescence was invented by industrial society to intense interest in applying this advancing knowledge
extend occupational training beyond childhood. However, some of the to help inform broad societal issues, such as adolescent
neurobehavioural changes seen in human adolescence, such as increases in exploratory health, education and legal policies. Several influential
tendencies and changes in reward processing, have been observed in many non-human
models of adolescent brain development have proposed
species as they go through puberty (BOX4). Moreover, as documented by the
anthropologists Schlegel and Barry155 in a study of 186 pre-industrial societies, virtually
that a maturational gap between cognitive control and
every human society (including hunter-gatherers and pastoralists) recognizes an affective processes (including reward and threat process-
adolescent period as a stage that is distinct from childhood but during which ing) may explain adolescent increases in risks for engag-
individuals are not yet fully adult in status. Thus, it is not the existence of adolescence as ing in impulsive and dangerous behaviour (for example,
a developmental stage that has changed in recent history but rather the timing and see REFS2,7,8). These models tend to emphasize the
length of this developmental period. That is, historically puberty occurred at relatively relatively faster maturation of subcortical affective brain
older ages (for example, age of menarche at 1516years of age) and taking on adult areas in comparison to more slowly maturing frontal
status typically ensued within 24years. In contemporary society, puberty often occurs cortical brain areas as the reason why adolescents tend
at much earlier ages (the mean age of menarche in the United States is 12years and to make more emotional (that is, less rational) decisions,
early signs of puberty typically begin by 911years of age), whereas the process of
resulting in actions that do not sufficiently weigh consid-
achieving full adult roles is often stretched into the mid-twenties. Thus, in modern
society, adolescence has been stretched to span a much longer interval of
eration of long-term outcomes.
development. Despite the appeal of these models in explaining
In addition, the social structures of adolescents have undergone major changes in the high rates of dangerous and impulsive behaviour in
recent human history, as have key aspects of developing long-term goals. In adolescents, it also is important to evaluate the degree
contemporary society, adolescents spend most of their time in school with same-age to which the available neuroimaging data support these
peers or in other structured educational and training environments, where the primary models. A number of research groups have begun to sug-
goal is to prepare the adolescent for occupations in a distant and abstract future. In gest that there has been too much emphasis on frontal
pre-industrial societies, however, adolescence functioned primarily as a period of social cortical immaturity as the reason why adolescents engage
and reproductive development155 or apprenticing to learn directly utilitarian skills. in risky behaviour, and they have begun to point increas-
The relationships between these changes in the length, timing, nature and goals
ingly towards a more nuanced understanding of interac-
of adolescence and the brain changes associated with adolescence are not yet
understood. For example, some aspects of adolescent development (for example,
tions across cognitive, affective and social processing 12.
socialaffective changes at puberty) occur at earlier ages, whereas other There also is a growing recognition that social contexts
developmental milestones (for example, taking on adult roles and responsibilities in strongly influence how these neural systems develop and
society) occur at later ages, raising the question how this differential timing of how adolescents make decisions.
these external factors (combined with earlier activation of pubertal changes in
social and affective processing) affects the development of neural systems that are Neuroimaging adolescent development
involved in social and emotional regulation and the self-regulation necessary for Structural MRI (BOX3) and functional MRI (fMRI)
taking on fully adult roles. have been used to study how changes in brain structure
and activity, respectively, are associated with changes in
behaviour during development. In the past decade, a
In this Review, we briefly discuss some of the prevail- large number of fMRI studies have been conducted in
ing views on adolescent brain development. Next, we the domains of cognitive, emotional and social develop-
review neuroimaging studies of cognitive control, affec- ment. In these studies, the typical age range of the sub-
tive processing and social processing in adolescence. In jects is 825years, which provides a good framework
addition, we discuss the pronounced social and affective for the examination of broad changes that occur dur-
changes in adolescence, including the importance of inter- ing adolescence. However, as mentioned above, there
actions between cognitive, affective and social processing is considerable variability in the ages used, many stud-
during this period of development10,11. Last, we suggest a ies have gaps in the measurement of different phases of
reevaluation and extension of the prevailing models of adolescence (for example, comparing only early adoles-
adolescent brain development. We emphasize the lack cent 812year-olds with adults or only comparing mid-
of data supporting any simple view of frontal cortical adolescent 1317year-olds with adults) and most studies
immaturity as the explanation for adolescent vulnerabili- have only tested for linear age-related changes rather
ties, and consider the growing evidence for specific social than testing for models of adolescent-specific patterns of
affective changes that begin during pubertal development change (for example, Ushape or inverted Ushape pat-
as conferring increased vulnerabilities in some adolescent terns of development). Furthermore, age-related changes
contexts. We also highlight the need for a better under- provide a rough proxy for adolescent phases but do not
standing of the neuromaturational underpinnings to these permit examination of puberty-specific effects, and most
socialaffective changes, including the role of pubertal of these studies did not include an assessment of pubertal
development, and the potential value of investigating how development. Nonetheless, there is now an impressive set
these changes may contribute to unique opportunities for of fMRI studies through which to consider the develop-
learning and adaptation in adolescence. ing brain and its role in adolescence-specific transitions
in cognitive, affective and social processing and their
Current views of adolescent brain development interactions. Below we review and discuss these studies
Over the past decade, our understanding of the neural in the context of a meta-analysis (FIG.1a; Supplementary
mechanisms that underlie changes in cognitive, affective information S1 (table)).

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Box 2 | Sex hormones in adolescence


Pubertal development is associated with numerous changes in the brain, with evidence that hormone levels and neural
function mutually influence each other. The single most important step in the onset of puberty occurs when the
hypothalamus begins to release substantial amounts of gonadotrophin-releasing hormone (GnRH) in a pulsatile manner
during sleep. This pulsing of GnRH begins the reawakening of the hypothalamicpituitarygonadal (HPG) axis, which is
first active during prenatal and early postnatal life (sometimes referred to as the neonatal mini-puberty) and then is shut
down by inhibitory inputs to the hypothalamus, remaining quiescent throughout childhood. Pulses of GnRH stimulate the
pituitary to produce the hormones follicle-stimulating hormone (FSH) and luteinizing hormone (LH), which in turn
stimulate the ovaries and testis to produce the sex hormones oestrogen and testosterone, respectively. The mechanisms
that trigger the reawakening of pubertal GnRH pulsing are not fully understood, but they include interactions with
neural systems involved in metabolic regulation, energy storage and sleep regulation. There has been rapid progress in
understanding several aspects of the process over the past decade, including the importance of the hormone leptin (a
protein manufactured in fat cells that has a key role in regulating energy intake, energy expenditure and appetite) and
kisspeptins (a family of neuropeptides encoded by the KISS1 (KiSS 1 metastasis-suppressor) gene that have been
identified as the conduits for the effects of leptin actions on GnRH neurons in the hypothalamus).
A second neuroendocrine axis that forms a core aspect of pubertal maturation involves increases in growth hormone
(GH) secretion from the pituitary, which has a crucial role in the rapid physical growth during this period. As with the
gonadal hormones, this GH increase at puberty is also sleep-dependent. A third component of puberty involves increases
in the secretion of a testosterone-like hormone from the adrenal glands called dehydroepiandrosterone (DHEA) this
process is the least well understood in terms of the neural systems that initiate and regulate it.
The main hormones that regulate the bodily changes and emergence of secondary sexual characteristics of puberty are
testosterone, oestradiol and DHEA. The physical sex differences that emerge at puberty are in part attributable to
differences in hormone levels (for example, higher oestradiol levels in girls and greater testosterone increases in boys) but
also to differences in the distribution and types of hormone receptors in target tissues.
There is relatively limited knowledge of how these hormones influence adolescent brain development and specific
behavioural, cognitive and affective changes during adolescence. Several research groups have begun to focus on the
role of pubertal hormones on neurobehavioural changes in adolescence, with intriguing preliminary findings3,83. As
discussed in those reviews3,83, addressing these questions will require both conceptual and methodological advances.
Animal experiments that examine neural and behavioural changes associated with specific aspects of pubertal
maturation and clinical studies that examine neural changes in response to hormone treatments (for example, the
administration of oestrogen to pre-adolescent girls with Turner syndrome156) can provide additional insights.

Functional MRI studies of cognitive control Basic cognitive control functions. Many studies of basic
It is well recognized that during adolescence, there is cognitive control functions, such as working memory,
a steady increase in the ability to use cognitive control inhibition and interference, and task switching, have
over thoughts and actions13,14. Cognitive control abili- reported that regions involved in these functions in
ties start to emerge in early childhood and gradually adults (including the lateral PFC and parietal cortex)
improve over childhood and through adolescence15,16. become increasingly engaged during childhood and ado-
These abilities and are often seen as a driving force lescence (FIG.1a; Supplementary information S1 (table)).
behind cognitive development 17, and these increases in For example, in spatial and verbal working memory par-
cognitive control abilities in adolescence mark a period adigms that contrast high working memory load with
of significant advancements in learning and successful low working memory load, increases in activity in the
adaptations to a wide variety of social contexts and cul- ventral and dorsolateral PFC and parietal cortex have
tural influences. For example, the ability to exert cog- been reported when 712year-olds were compared
nitive control over thoughts and actions is of crucial with adults; when 712year-olds were compared with
importance to success in most classroom settings mid-adolescents (1317years) and adults; and for linear
not only for the direct learning of skills such as reading, comparisons from the age of 7years to adulthood2030.
maths and the capacity to reason about abstract ideas Studies using response inhibition or interference sup-
but also at the level of behavioural control that sup- pression tasks report an age-related increase in acti-
ports sitting at a desk, avoiding distractions and doing vation in the inferior and middle frontal gyrus in go
homework. versus nogo trials when children and early adolescents
Many developmental fMRI studies have been con- (712years) were compared with adults; when children
ducted in this domain, including investigations of basic and early adolescents (612years) were compared with
cognitive control functions and more complex cogni- mid-adolescents (1317years) and adults; and for linear
tive control functions in which different basic functions comparisons from the age of 7years to adulthood3136.
have to be combined. Although these functions are sep- In addition, several task switching studies have reported
arable in their contributions to complex behaviour 18, increased activation in the lateral PFC and parietal cor-
they rely on overlapping areas in the lateral prefron- tex in adults relative to children (ages 712years) and
tal cortex (PFC) and parietal cortex (also see REF.19). adults versus mid-adolescents (ages 1017years or
However, the extent to which these brain areas are acti- 1318years) in switch versus repeat trials3739. These
vated across development differs between studies and findings have been interpreted as indicating that areas
samples, as discussed below (FIG.1a). of the PFC have a slow developmental trajectory and are

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Box 3 | Structural brain development in adolescence


model of increased activation in the PFC is unlikely to
account for the developmental transitions in basic cogni-
Numerous structural neuroimaging studies have demonstrated that adolescent tive control that take place during adolescence53,54.
development involves widespread changes in the brain. Longitudinal research
examining changes in brain structure over time has shown that cortical white matter Complex cognitive control functions. Several recent stud-
throughout the brain increases with age throughout childhood and adolescence. By
ies have used approaches that involve more complex
contrast, cortical grey matter, which reflects neuronal density and the number of
connections between neurons, follows an invertedU shape over development, peaking
cognitive control tasks, such as performance monitoring,
at different ages depending on the region157159. Within the cortex, grey matter feedback learning and relational reasoning, which require
reduction is most protracted for the dorsolateral prefrontal cortex and the a combination of basic cognitive control functions18.
temporoparietal junction; here, cortical grey matter loss continues until the early This approach can detect strategy differences between
twenties159,160. The development of subcortical brain regions is also subject to both people in a particular task. These studies have revealed
linear and nonlinear changes, such that some subcortical regions (such as the caudate interesting developmental trajectories of PFC activation
and the putamen) linearly decrease in size throughout adolescence, whereas other (Supplementary information S1 (table)). For example,
subcortical regions (such as the amygdala and the hippocampus) show an increase in performance monitoring studies (that is, studies involving
size at the onset of puberty, after which growth stabilizes in adolescence and error and feedback processing) that included early adoles-
adulthood161. These dynamics of structural brain development have been summarized
cent (ages 812years), mid-adolescent (ages 1317years)
in several excellent reviews (for example, see REF.160).
and adult age groups did not confirm the strict frontal
cortical immaturity view5559. Instead, these studies report
not engaged to the same extent in children and adoles- that the frontal cortical network was engaged to the same
cents as in adults40. extent in participants of different age groups but under
However, many studies of the same basic cognitive different experimental conditions. Specifically, in early
control functions have found age-related decreases in adolescents, the PFC and parietal cortex were activated
frontal cortical activity in early adolescents compared following positive performance feedback, whereas in
with children and adults, mainly in the superior part of adults, the same regions were activated to the same extent
the lateral and medial PFC (FIG.1a; Supplementary infor- following negative feedback, with mid-adolescents show-
mation S1 (table)). These decreases were found for differ- ing a transition phase57,58. A similar nonlinear pattern was
ent domains of working memory (in studies comparing found in a relational reasoning task60 in early adolescents,
ages 612years, 1317years and adults)4143, for response mid-adolescents and young adults (ages 1130years).
inhibition (in studies comparing ages 612years versus When subjects were asked to combine and integrate differ-
adults)32,4448 and in task switching (in studies compar- ent spatial dimensions (that is, relational integration), only
ing ages 813years versus adults)49,50. These findings mid-adolescents (1418years) showed increased activa-
have been interpreted as indicating increased efficiency tion in the anterior PFC. The authors interpreted this as
of these networks over time. However, it is difficult to reflecting a mid-adolescence-specific cognitive strategy
confirm this interpretation because these decreases in to perform the task in an efficient way (see REFS6163 for
activation are not always accompanied by performance other examples of relational reasoning studies). Indeed,
differences. the increased activation in mid-adolescence was associ-
Thus, although the parietal cortex seems to show a ated with faster reaction times and increased accuracy.
relatively consistent pattern of increased activation in However, the exact relation between neural activation,
cognitive control tasks with increasing age (except for task performance and strategy use is not well understood
one study that showed a decrease with increasing age22), at thistime.
studies of lateral and medial PFC show both increases
and decreases in activation, depending on the task para- Flexibility for recruiting cognitive control systems? The
digm and the PFC subregion involved in the task (FIG.1a). question then arises: what is the general pattern that
Moreover, mid-adolescence-specific increases (for ages emerges from fMRI studies on cognitive control? The
1317years relative to both 612years and adults) have data discussed so far provide evidence against the view
been reported for regions in the lateral PFC in working that these brain regions simply come increasingly online
memory, inhibition and task switching tasks39,41,47,51,52 with advancing age through adolescence. Instead, the
(FIG.1a; Supplementary information S1 (table)); such an high degree of variability in the findings could reflect a
inverted Ushaped relationship between age and activa- less automatic and more flexible cognitive control sys-
tion could be due to increases in task engagement in ado- tem in adolescence. It is possible that the degree to which
lescents compared to children andadults. cognitive control processes are engaged or activated in
Taken together, it is difficult to reconcile how this adolescence are strongly influenced by the motivational
degree of variability in neuroimaging findings in the salience of the context. Factors such as the presence
development of basic cognitive control functions provides of peers, task instructions, strategies and the affective
support for the model of frontal cortical immaturity or appraisal of the value or priority of performing the task
Relational reasoning the concept of linear advances in PFC development may have relatively large influences on the extent to
An essential component of across adolescence. Indeed, if such varied findings of which cognitive control systems are recruited in ado-
fluid intelligence that requires a increases or decreases in activation can be interpreted as lescence53. As will be discussed in later sections, there is
number of verbal or spatial
dimensions to be considered
consistent with the concept of frontal cortical immaturity, growing recognition that social and affective factors are
simultaneously to reach a this would seem to render the model as virtually unfal- particularly important in influencing aspects of adoles-
correct solution. sifiable. Our meta-analysis suggests that such a simple cent engagement. The ability to quickly shift priorities,

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adjusting the degree of cortical activation in a given task of developing tighter integration of some regions into
or situation according to the social and motivational con- long-range networks over time, while segregating the
text could contribute to greater variability in cognitive short-range connections between other sets of regions
control. However, this flexibility in making quick adjust- into separate networks. Because the long-range connec-
ments in the degree of engagement across changing con- tivity patterns are still undergoing maturational strength-
texts may be crucial to the ability of youths to learn about ening, it is likely that some aspects of integrative cognitive
and adapt to rapidly changing adolescent social contexts. control may be less automatic and more flexible during
For example, adolescents are often the fast-adopters of adolescence. As a result of weaker connectivity across
social change such as learning new trends in language, these long-range integrating circuits, adolescents may
technology, music and fashion or when adapting to new be more vulnerable to variability in performance under
cultures after immigration64. high demands on attentional and decision-making net-
Interestingly, two longitudinal studies that followed works in some situations (because the ability to integrate
adolescents (ages 823years and 1518years) over a control is less automatic); however, these same qualities
period of 3years reported no age-related changes in acti- (less automatic responses) may also enable adolescents to
vation in the frontoparietal network in a feedback-learn- respond in creative and adaptive ways. Most importantly,
ing and working memory paradigm. Instead, changes in however, these findings suggest that adolescence is a cru-
task performance in the same person measured at dif- cial time of development during which specific learning
ferent ages correlated with changes in activation in the (or training) experiences may actively sculpt final con-
lateral PFC65,66. Furthermore, in a working memory train- nectivity patterns in some of these long-range cognitive
ing study, young adolescents (ages 1113years) showed control networks (see REF.70 for a training study on func-
increased activation in the lateral PFC after 6weeks tional connectivity in adults supporting the view of adap-
of practice, whereas before training these adolescents tive change in the frontal cortical circuitry).
showed less activation in the lateral PFC compared to Taken together, findings from the few existing longi-
adults before training 67. These findings support the idea tudinal and training studies (which are more powerful in
that frontal cortical brain regions in adolescence are sen- detecting the trajectories of brain change than the more
sitive to context and that their activity can be enhanced usual cross-sectional studies comparing individuals of
by training. The training study 67 indicates that this flex- different ages) highlight the complexities of disentangling
ibility of the frontal cortical network may be greater in specific developmental changes during adolescence. An
adolescence than in adulthood, although further studies important goal for future research will be to parse the
are needed to confirm these findings. developmental changes in brain activation that reflect
This proposed flexibility in frontal cortical networks four relatively different processes that could influence
in adolescence is further supported by studies on func- cognitive performance in adolescents: maturational
tional connectivity in the absence of a behavioural task changes in the fundamental capacity to perform a task;
(that is, resting state analyses). These studies have dem- other task-relevant factors, such as degree of engage-
onstrated that the main circuitry for cognitive control ment, motivation and sensitivity to social and affective
is already in place at the start of adolescence68, but the context; changes that reflect the direct effects of training;
strength of connectivity within this circuitry continues and developmental changes in the capacity for learning and
to undergo maturational changes across adolescence. For training. As reviewed below, it appears that task per-
example, there is a tendency for short-range connections formance (and perhaps some developmental learning
to become weaker with age, whereas long-range connec- effects) in adolescents may be particularly sensitive to
tions, which are important for integration across circuits, social and affective influences.
become stronger with age69. The authors of this study
interpreted their findings as consistent with a model Functional MRI studies of affective processing
Neural systems that underpin affective processing can
be conceptualized not only as systems involved in emo-
Box 4 | Animal research on puberty-specific changes in reward processing
tions and motivation but also, more broadly, as a net-
There is compelling evidence from animal models showing that changes in gonadal work of valuing systems that are involved in learning
hormone levels in puberty induce a (second) organizational period to guide the about rewards and threats and in regulating approach
remodelling of the adolescent brain in sex-specific ways162,163. Rodent studies have also and avoidance behaviours accordingly. During adoles-
shown a remodelling of the dopaminergic systems involved in reward and incentive cent development, the most salient types of rewards and
processing in the peri-adolescent period. This remodelling involves an initial rise in
threats typically reside in the social domain (for exam-
dopamine receptor density, starting in pre-adolescence, and a subsequent reduction
of dopamine receptor density in the striatum and prefrontal cortex163 a pattern that
ple, being admired, accepted or rejected by peers and
is more pronounced in males than females163. As a result, dopaminergic activity early romantic and sexual experiences). Accordingly, it
increases substantially in early adolescence and is higher during this period than earlier is important to recognize the inherent overlap between
or later in development163. The developmental changes in reward processing in animals affective and social processing in adolescence. However,
in these studies are similar to those emerging from the human functional MRI literature. to date, most studies in this area have focused on mon-
Given the important role of dopamine in reward processing, the developmental etary rewards to examine how the ventral striatum,
changes in dopamine receptor levels may be linked to the increase in novelty seeking, which is a subcortical brain region that is active when a
exploratory behaviour and reward-seeking behaviour at puberty164,165. Thus, person receives or expects a reward71, responds to risks
translational research focusing on the mechanisms that underpin pubertal changes in and rewards in adolescents compared to adults (FIG.1b;
reward responses may provide important insights into human adolescent behaviour.
Supplementary information S1 (table)).

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a Working memory, inhibition and task switching b Risk-taking and rewards


80 80

60 60

40 40

20 20

0 0

20 20

40 40

20 20
40 60 40 20 0 20 40 60 80 100 120 40 60 40 20 0 20 40 60 80 100 120

c Emotional faces d Social reasoning


80 80

60 60

40 40

20 20

0 0

20 20

40 40

20 20
40 60 40 20 0 20 40 60 80 100 120 40 60 40 20 0 20 40 60 80 100 120

Increasing across adolescence Decreasing across adolescence Adolescent transition

Figure 1 | Meta-analysis of functional MRI studies in adolescents. Results from a meta-analysis of a representative
set of functional MRI studies, which were conducted between 2001 and 2011, of cognitive, Nature affectiveReviews | Neuroscience
and social
processingin adolescents compared to other age groups. a | Frontoparietal and anterior cingulate cortex activation in
working memory2030,4143,52,65,167, inhibition3136,4448,168 and interference suppression and task switching studies35,3739,49,50,78.
b|Striatum activation in reward processing studies7282,169. c | Amygdala and striatum activation for face processing
studies8994,96,100,170. d | Anterior medial prefrontal cortex and temporoparietal junction activation in socialcognitive
reasoning studies107113,115,116,127,128,130,171,172. For illustrative purposes and for reasons of comparability, a slice of the mid-brain
is shown ((x = 0), Montreal Neurological Institute coordinates) but the activations are displayed as circles when activation
was in ventral and dorsolateral prefrontal cortex (x > +/ 20) or in superior frontal sulcusfrontal eye fields and parietal
cortex (x > +/ 20), and as squares when activation was in the medial prefrontal cortex (x < +/ 20). The findings of the
reviewed studies are summarized as increasing across adolescence (light blue squares and circles), which indicates that
the specific region is more engaged with increasing age; decreasing across adolescence (red squares and circles), which
indicates that the specific region is less engaged with increasing age; and adolescent transition (purple squares and
circles), which indicates that mid-adolescents process information differently from both children and adults. It should be
noted that: first, the increases and decreases were dependent on the contrast used and therefore should be interpreted in
this context (see REF.173) and, second, not all studies used more than two age groups a design that does not allow for
an examination of transitions. Supplementary information S1 (table) provides an overview of all studies that were included
in the meta-analysis, including the age range and sample size for each age group.

When receiving rewards, adolescents (ages finding that underactivation (or no change) in ventral
1217years) consistently show increased striatal acti- striatum activity is found during reward anticipation
vation relative to children (ages 712 years) and in adolescents may help to explain why some studies
adults7280. By contrast, adolescents tend to show less show no differences between adolescents and adults in
activation in the striatum than adults during reward risk-taking behaviour, despite pronounced neural dif-
expectation or anticipation (that is, when participants ferences during reward processing 73,8486.
observe a cue that indicates a potential reward)76,81,82. One way in which reward processing may influ-
The differential response to cues (reward anticipation) ence decision-making is through the prediction error.
and actual receipt of rewards in adolescents may help to Reward prediction error signals reflect the difference
explain some of the inconsistencies with regard to ven- between the expected value of an action and the actual
tral striatum activity in adolescents83. For example, the outcome of the action, and are encoded by phasic

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activity in the mesolimbic dopamine system (includ- Functional MRI studies of social development
ing the ventral striatum). These prediction error sig- The fundamental maturational task of adolescence is
nals appear to have a crucial role in the process of achieving adult social competence that is, developing
learning and adjusting behaviour to adapt to chang- the knowledge and skills to be capable of functioning
ing contexts or conditions. The first developmental independently from parents or other responsible adults.
study 56 of prediction error signals in children, adoles- Adolescents appear to be naturally motivated to want
cents and adults found that prediction error signals greater independence from their parents and to establish
in the striatum were highest in adolescents, whereas their individuality 102. Adolescents are drawn to build and
decision-value signals in the medial PFC did not show explore new social networks (that is, peer groups) and to
a consistent developmental pattern. Results of a sec- increase prioritization around peer issues of belonging,
ond developmental study of reinforcement learning did acceptance and interests in romantic and sexual partners.
not implicate the prediction error signal directly but Achieving success in these domains requires new social
pointed to the connectivity between the ventral stria- skills, social knowledge, affect regulation, adaptive cop-
tum and medial PFC as the source of developmental ing skills and, in general, improved social competence103.
differences in how learning signals guide adolescent There has been recent progress in understanding neu-
behaviour 87. Interestingly, recent evidence has demon- ral systems relevant to two dimensions of social develop-
strated that value-based decision processes are based ment in adolescence: socialcognitive development, which
on neural computations that use the subjective value concerns the knowledge and capacity to understand
of the expected reward88, again implicating interactions social situations, and socialaffective development, which
between reward prediction at the level of the ventral concerns the motivational and emotional aspects of
striatum and higher-level, cortical processing of valu- socialskills.
ing, which is likely to incorporate more subjective
aspects of valuing, such as the social or affective con- Socialcognitive development. There has been consider-
text. Taken together, these findings point to a promis- able progress in understanding the development of neu-
ing line of investigation into the mechanisms by which ral systems that underlie socialcognitive skills such as
subcortical value-based inputs may interact with corti- mentalizing104. Basic social detection and theory-of-mind
cal value-based inputs to signal motivational salience. develop in early childhood, whereas more complex
In addition to these studies of reward processing, a socialcognitive skills, such as mentalizing and meta-
number of investigations have examined developmental cognition, mainly develop in adolescence. The devel-
changes in the response to threat stimuli. For example, opment of complex socialcognitive skills is probably
increased activity in subcortical brain regions has been driven partly by environmental demands and experi-
observed in adolescents in response to emotional faces ences, such as the greater need to adapt to the peer group
(FIG.1c). Several studies have reported enhanced activity and newly emerging romantic interests. Such socialcog-
in the amygdala, a region of the brain that is important nitive skills become increasingly important as adolescents
for the processing of negative affect, in mid-adolescents learn to adapt to rapidly changing social environments,
(ages 1218years) compared with adults when look- in which the opinions and evaluations of peers become
ing at pictures of fearful faces8994 (see REFS9599 for increasingly salient.
studies that focused on other brain regions or younger Recently, researchers have identified a social brain
children). Pictures displaying positive emotional (for network a network of brain regions, including the
Socialcognitive example, happy) faces induced more activation in ado- medial PFC and temporoparietal junction (TPJ) that is
development
Changes in cognitive skills and
lescents relative to adults in the ventral striatum the important for mentalizing and perspective-taking 105 and
knowledge that facilitate area that is also more active in response to receiving that undergoes structural and functional changes dur-
understanding social situations, rewards in mid-adolescents relative to adults94,100. Thus, ing development 106. Studies using mentalizing and social
such as mentalizing and it appears that mid-adolescence is associated with a interaction paradigms have shown that specific regions in
perspective-taking abilities.
more general intensification of affective processing, not the social brain network contribute to the development of
Socialaffective only in the approach or positive affect domains intention understanding in social reasoning in children
development (such as rewards and happy faces) but also for stimuli and adolescents (see REF.106 for a review). As highlighted
Changes in motivational and that may signal threat and avoidance (that is, fearful in our meta-analysis (FIG.1d), studies using social reason-
emotional aspects of social faces). ing paradigms107114 and self-knowledge paradigms115,116
processing (such as empathy,
increases in the salience of
Together, these findings suggest that the neu- have shown that the medial PFC is often more activated
obtaining status, admiration rodevelopmental changes in affective processing in in adolescents (ages 918years) compared to adults106,
and affiliation from peers) and approach and avoidance follow nonlinear developmen- whereas the TPJ is often less activated in adolescents
the development of affective tal patterns, with a peak in subcortical brain activation (ages 1017years) compared to adults106.
skills that support social
in mid-adolescence. This pattern may underlie part One of the main changes in the nature of social inter-
competence.
of the intensification of emotional and motivational actions in adolescence is the shift from self-oriented
Mentalizing experiences in mid-adolescence, and this intensifica- behaviour towards other-oriented (that is, pro-social)
The ability to infer mental tion of affect may create new challenges to emotional behaviour 117. These changes enable the formation of
states of others, such as ones regulation and self-control101. Moreover, the increased more complex social relationships and are particularly
intentions, beliefs and desires
a key dimension of social
activity in valuing systems in adolescence may reflect important for functioning in peer groups adolescents
cognitive development in a sensitive period for learning about sources of reward have a stronger motivation for peer acceptance compared
adolescence. and threat, particularly in social domains. with children and adults118. Social interaction paradigms

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can be used to investigate neural activity associated understanding; however, some of these changes may
with self-oriented thoughts and other-oriented thoughts involve implicit learning processes and rely on the devel-
and actions. Inspired by classic social utility models of opment of socialaffective skills. Indeed, considerations
decision-making, social psychologists have developed of self and others outcomes appear to be influenced by
experimental games in which two-person interactions the social environment of adolescents. For example,
are investigated in a laboratory setting. According to there is evidence that popular adolescents (that is, those
social utility models, social behaviour is generally moti- frequently liked and seldom disliked by peers) generally
vated by self-gain and by concern for others105. The lat- help, share and cooperate with peers and score highly on
ter is essential for other-oriented behaviour and requires measures of empathy and perspective-taking 129.
the ability to consider other peoples feelings, thoughts,
intentions and actions, therefore drawing heavily on Socialaffective development. There is growing under-
theory-ofmind (that is, perspective-taking) abilities. standing of the neural systems that underlie aspects of
Comparison of self-gain and other-gain is involved in socialaffective development in adolescence. For exam-
social judgements of fairness and reciprocity, which ple, studies on empathy 130 and social acceptance and
in turn have important roles in the display of other- rejection131134 have reported differences in brain activity
oriented behaviour. Therefore, these games provide a between children, adolescents and adults in brain areas
valid experimental context for studying these important involved in processing affect and social pain, including
aspects in the development of self- and other-oriented the temporal pole and the insula (Supplementary infor-
processes105. mation S1 (table)).
Two of the most commonly used games to study One study 131 that examined, in different age groups
social decision-making in adults are the Ultimatum (ages 810years, 1214years, 1617years and adults),
Game119 (FIG.2) and the Trust Game120. These games have neural activation in response to social acceptance and
proven to be highly useful for studying developmental rejection from peers found increased activation in the
differences in self- versus other-oriented thoughts105. ventral anterior cingulate cortex (ACC) and striatum in
Studies using these games have found that self- each age group when a participant received feedback that
oriented thoughts decrease and other-oriented thoughts a peer liked them compared to feedback indicating that a
increase with age, with a transition phase around peer did not like them. This is consistent with the idea
mid-adolescence (ages 1216 years) during which that social acceptance is salient across these age groups
other-oriented thoughts become more dominant than self- and continues to be salient in adulthood. Social rejection
oriented thoughts. In addition, these studies showed that was associated with activation of the insula and dorsal
children and early adolescents (ages 912years) have less ACC in all age groups, but only adults showed additional
understanding of other peoples intentions when making recruitment of the dorsolateral PFC, which may indicate
or judging decisions and, with age, increasingly take the a better capacity to regulate rejection, although this was
perspective of others into account 121123. A meta-analysis not tested using behavioural measures. In a study using
demonstrated that these games activate brain regions the Cyberball game to elicit feelings of rejection, early
that are implicated in the different value computations adolescents (ages 1012years) showed more activation
of social interaction, such as the valuing of self-gain ver- in the subgenual ACC during rejection than adults135.
sus gains for others124. That is, the brain regions that are Activity in this region was associated with greater rejec-
involved in social cognition (anterior medial PFC, TPJ tion-related distress in youths in a different Cyberball
and insula) are involved in judging fairness and in recip- study 136. Activity in the insula (which was also associated
rocating trust, and activity in these regions depends on with greater rejection-related distress)136 was reduced in
perspective-taking demands125,126. individuals who have many friends in daily life (in the
Age comparisons using these games have demon- 2years before the fMRI scan)137, suggesting that young
strated that with increasing age, adolescents are increas- adolescents who had developed strong friendship net-
ingly responsive to the perspective of another player. works were less sensitive to social rejection. Finally, this
Self-oriented thoughts
Concern for outcomes that Concurrent with this behavioural change, there was a same research group also showed that increased sub-
benefit ones own gains, such gradual increase in activation in the TPJ (and the dor- genual ACC and medial PFC activity to social exclusion
as in economic exchange when solateral PFC) and a gradual decrease in activation in in the 1213year-olds predicted increased depressive
benefits for self and benefits the anterior medial PFC across adolescence123,127,128. The symptoms in the year following the Cyberball study 138.
for others are often conflicting.
increase in TPJ activation correlated with the perspec- Taken together, these findings show promising
Other-oriented thoughts tive-taking behaviour, independently of age, confirming approaches to investigating the development of social
Concern for outcomes that the role of this area in perspective-taking 128. The overac- affective processing in adolescence; however, they also
benefit others, even when this tivation in the anterior medial PFC and underactivation raise a number of questions. One particularly thorny
is at the expense of gains for
in the TPJ in adolescents relative to adults mentioned set of issues focuses on questions about the direction of
self, such as when evaluating
what is fair for two parties. above could be interpreted as underlying the decrease in effects. For example, some changes in neural activation
self-oriented thoughts and actions and the increase in other- in response to social and affective stimuli may depend on
Trust Game oriented thoughts and actions, respectively, that occur new patterns of social learning and experience in adoles-
Two-person interaction game across adolescent development. cence (such as greater reaction to social rejection second-
that requires
perspective-taking and relies
It is important to recognize that some of these devel- ary to affective learning that is simply more likely to occur
on feelings of fairness and opmental changes in fairness and reciprocity appear during this period of development). By contrast, changes
concern for others. to reflect changes in explicit social knowledge and in the neural systems that underpin the motivational

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REVIEWS

salience of peer rejection may undergo maturational contribute to the increase in motivational salience of
changes that render the systems biologically more reac- social learning relevant to depression. For example, there
tive. It also seems likely that bidirectional effects could is evidence that the increased risk for depression in ado-
occur (maturational changes that fundamentally alter lescence is linked to the increase in gonadal hormone lev-
the motivational salience or reactivity that also interact els139. Given the finding that neural activity during social
with learning experiences that are more likely to occur in rejection at ages 1213years predicted later depression,
adolescence). Such bidirectional interactions could con- this suggests that pubertal hormones may influence
tribute to spiralling effects over time, such as sensitivity to socialaffective development, perhaps by increasing the
rejection and a pattern of negative experiences leading affective salience (and vulnerability to long-term conse-
to the development of depression in adolescence. Studies quences) of social rejection.
of high-risk and clinical samples followed over time will
be needed to test these hypotheses. Puberty and socialaffective changes
There is also a need to focus on the specific role of There is growing evidence that some of the social and
puberty as a neurodevelopmental mechanism that may affective changes that occur in adolescence are linked

a Proposer b Rejection of unfair oer


10-year-olds
13-year-olds
15-year-olds
20-year-olds
Unfair Fair 100%
oer oer
Responder Responder

Rejection rate
50%
Accept Reject Accept Reject

Proposer Proposer Proposer Proposer


receives 8 receives 0 receives 5 receives 0
Responder Responder Responder Responder 0%
receives 2 receives 0 receives 5 receives 0 No Fair Hyperfair
alternative alternative alternative

c Activation for no-alternative-reject condition


6 TPJ
4
Contrast value

4
5 10 15 20 25
Age (years)

Figure 2 | Interactive decision-making paradigms to examine social reasoning. a | AnNature example of the |Ultimatum
Reviews Neuroscience
Game (UG) a two-person interaction game that requires perspective-taking and relies on feelings of fairness. The game
involves a proposer and a responder. The proposer can divide a fixed amount of money between the two players, and the
responder decides whether to accept or reject the offer. When the offer is accepted, both players receive the stake
according to the offer. When the responder rejects the offer, both players receive nothing. b | To vary perspective-taking
demands on the responder, studies have made use of the miniUG, in which the proposer is given two money-dividing
options by the computer. One option is always an unfair division (8 for proposer, 2 for responder), and depending on the
experimental condition, the second option can be unfair as well (no alternative for proposer condition), a fair split (fair
alternative condition) or a split that gives the advantage to the responder (hyperfair alternative condition). Results from
behavioural tests show that in the miniUG, responders take into consideration the options that the proposer had121,127.
That is, unfair offers are mostly rejected when the alternative was fair or hyperfair but are more often accepted when the
alternative was also unfair (in other words, the proposer could not help it but was restricted by the offers from the
computer). Developmental studies have shown that in the noalternative condition, which relies most on
perspective-taking skills of the responder, there was an age-related decrease in rejection, indicating that the ability to
understand the perspective of the first player increases with age. c|This increase was accompanied by increased
activation in the temporoparietal junction (TPJ)127.

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to the onset of puberty 13,83,140. Studies have focused on Second, the prevailing models are based on cogni-
the role of the onset of puberty in the social re-orien- tive neuroscience studies that have relied primarily on
tation towards peers10, in changes in neural process- cross-sectional comparisons between samples of ado-
ing of reward141 and as shifting the balance of affective lescents and children and/or adults, and these groups
processing (with relatively more reward versus threat have typically been defined by widely varying age ranges
processing) interacting with cognitive control2,101 in ado- across different studies and laboratories. As a result, the
lescents. Despite considerable evidence that puberty is current understanding of the maturational processes
linked to the increases in sensation-seeking and some that underlie adolescent development is limited. One
aspects of risk-taking that occur in adolescence3,9,83, important example is the need to better understand the
there is little understanding of the specific hormonal role of pubertal maturation on specific neurodevelop-
changes that influence the development of those neural mental processes. We believe that this challenge will
systems involved in motivational or emotional tenden- entail addressing not only methodological issues (for
cies towards sensation-seeking behaviour. More gener- example, conducting studies designed to disentangle
ally, relatively few studies have investigated the role of age and pubertal effects) but also conceptual issues (for
puberty versus the role of age perse or the role of specific example, refining models to address the role of specific
hormones in these behavioural changes. hormones on specific aspects of social and affective
We believe there are several reasons why it is impor- development).
tant to investigate the role of hormonal changes in Below, we offer suggestions on how these challenges
puberty at the interface between social and affective can be tackled and present a model of adolescent brain
processing. For example, there is growing evidence that development that includes a focus on the role of puberty
increases in risk-taking in adolescence emerge after the (FIG.3). Our model proposes that the combination of flex-
increase in sensation-seeking associated with puberty ibility in PFC recruitment and changes in socialaffec-
and occur primarily in affective salient social contexts. tive processing can create vulnerabilities to engaging in
That is, adolescents show greater risk-taking than adults negative behaviours in some incentive situations but is
or children primarily when they are with peers (or believe generally adaptive and developmentally appropriate to
they are being observed by peers), and such peer effects the tasks and learning demands of adolescence. There
are evident in both real-life and laboratory studies of risk- are two key aspects to this model. The first focuses on
taking 77,142. Greater risk-taking in adolescence has also socialaffective engagement and goal flexibility; and
been reported in emotionally charged (or hot) situa- the second focuses on the role of pubertal hormones in
tions, but no adolescent increases in risk-taking occur socialaffective engagement.
in low-affect (or cool) contexts in the same experimen-
tal task143. On the basis of these and other findings (as Socialaffective engagement and goal flexibility. As
discussed below), we propose that changes in gonadal described above, there is growing evidence that ado-
hormone levels at puberty contribute to adolescent risk- lescence is a developmental period during which the
taking through two interacting effects, namely by increas- degree of cognitive engagement is relatively flexible,
ing the motivational salience of acquiring social status and depending on the social and motivational salience of a
by increasing the tendency to seek novel and high-inten- goal. This flexibility (and sensitivity to social and affec-
sity affective experiences particularly in social contexts tive influences) may confer greater vulnerabilities for
that create opportunities to gain peer admiration. adolescents to act in ways that appear impulsive and
immature, such as placing greater motivational value
Moving forward: new heuristic models on gaining peer admiration for a daring action than
On the basis of the findings reviewed above, we high- considering the risks and long-term health conse-
light what we regard as two important challenges facing quences of that behaviour. However, this capacity to
the field regarding the prevailing models of adolescent quickly shift goal priorities may also enable adolescents
brain development. First, the prevailing models are typi- to effectively engage cognitive systems in situations in
cally used to address broad issues of clinical relevance which they are highly motivated to do so and in ways
and social policy in ways that emphasize frontal cortical that facilitate learning, problem-solving and the use
immaturity (or a maturational gap in cognitive control) of divergent creative abilities144. Indeed, emerging evi-
to explain the emergence of risky, impulsive and dan- dence from animal studies supports the idea that juve-
gerous behaviours in adolescents. As described above, niles can outperform adults in some complex cognitive
neuroimaging studies in adolescents do not support tasks (BOX5).
these aspects of the prevailing models. Rather, the data Our model also is consistent with the idea that ado-
point to an adolescent flexibility in cognitive engage- lescence is an important period for developing cognitive
ment, depending on the social and motivational context. control skills through training and experience. When
The exciting challenge is to better understand how these adolescents are motivated, their capacity to engage can
incentives exert such strong influences on adolescents result in quick mastery of complex tasks. Consider, for
engagement, decisions and behaviour not only in ways example, a tedious and precision-demanding task such
that create vulnerabilities towards unhealthy incentives as using cell phone text messaging to communicate with
but also in ways that create unique opportunities for peers individuals who have learned these skills in ado-
learning, adaptation and positive motivations relevant to lescence typically reach a higher level of mastery than
health, education and social development in adolescence. those who have learned asadults.

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Gradual development of the cognitive control system (DLPFC, dorsal ACC and parietal cortex)
Gradual development of social brain network (mPFC, TPJ, subgenual ACC and insula)

Flexible frontal cortical Positive growth


engagement, depending on trajectories
motivational salience of context (e.g. adaptive exploration,
mature long-term goals
Motivational and goal exibility and social competence)
(shifting priorities)

Increased socialaective Negative growth


inuences on goals and behaviour trajectories:
Diminished goals
(e.g. depression and
social withdrawal)
Pubertal changes in the limbic system (ventral striatum and amygdala): increases in sensation-seeking, novelty-seeking Excessive motivation
and motivational salience of peer contexts towards negative goals
(e.g. substance use and
excessive risk-taking)
Puberty onset Transition to adulthood
Time
Figure 3 | A model of adolescent brain development. This figure illustrates a proposed model of adolescent brain
Nature Reviews | Neuroscience
development that begins with changes in social and affective processing (yellow boxes) associated with the onset of puberty.
Specifically, rapid increases in hormone levels at the onset of puberty influence the development of limbic circuits, probably by
inducing changes in the ventral striatum and amygdala (these regions have a pre-eminent role within the broader
corticostriatal circuitry, which enables affect-laden stimuli to influence goals and behaviour). These pubertal changes
contribute to increases in novelty-seeking, sensation-seeking and a tendency to process status-relevant social stimuli (for
example, receiving attention and admiration from peers) as having increased motivational salience. Although these social and
affective changes begin early (near the onset of puberty), they appear to peak in mid-adolescence and continue to influence
behaviour, decisions and learning throughout several years of adolescent experiences (indicated by the colour gradient in the
bottom yellow box). These social and affective influences interact with a broader set of changes in cognitive control and social
cognitive development (blue boxes), which includes the acquisition of social and cognitive control skills that develop gradually
across adolescence. These interactions between socialaffective processing systems and cognitive control systems contribute
to flexibility in the engagement of frontal cortical systems in adolescents, depending on the motivational salience of the
context. In many contexts, these changes lead to increased social motivation and tendencies to explore, take risks and try new
things particularly when such bold behaviours may bring admiration from peers. An important feature of this model is the
prediction that this increase in socialaffective engagement not only influences incentives and behaviour in the moment (for
example, choosing a specific bold but risky action to impress peers) but also influences motivational learning and patterns of
behaviour over longer intervals (depicted by spirals). Specifically, over time, these tendencies to quickly shift priorities
according to social incentives can contribute to healthy exploration and risk-taking behaviours, which promote social and
emotional learning and the development of skills and knowledge that underpin adult social competence. However, these same
tendencies can also lead to negative spirals, such as when risk-taking and motivational learning processes respond to
unhealthy incentives, such as drug and alcohol abuse or dangerous thrill-seeking. Another version of a negative spiral as a
consequence of increased flexibility in adjusting goals and heightened sensitivity to social evaluation may be perceived failure
in receiving admiration from peers, leading to disengagement from social goals, as seen in adolescent depression. The model
proposes that changes in socialaffective processing in combination with flexible prefrontal cortex (PFC) recruitment is
generally adaptive and developmentally appropriate to the tasks and learning demands of adolescence, but in some situations
perhaps through interactions between individual risk factors and risk environments can contribute to negative
consequences. ACC, anterior cingulate cortex; DLPFC, dorsolateral PFC; mPFC, medial PFC; TPJ, temporoparietal junction.

This flexibility of cognitive control may also confer socialcognitive and socialaffective skills. As described
adaptive advantages for learning to navigate the often earlier, the fundamental task of adolescence is to achieve
unpredictable social challenges of adolescence. The mature levels of social competence. The requisite skills
increased tendencies towards novelty-seeking and greater require a great deal of practice, learning and refine-
socialaffective engagement might naturally nudge moti- ment particularly in the realms of self-control and
vational tendencies towards the exploration of peer and affect regulation in socially charged situations. Natural
romantic contexts. This may promote behavioural explo- tendencies to approach, explore and experiment with
ration in ways that create risks and vulnerabilities but also these often frightening, but sometimes thrilling, peer
in ways that contribute to learning and developing new and romantic social situations and to quickly engage

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Box 5 | An example of motivational flexibility in adolescent mice


calcarine sulcus and right lingual gyrus, which are all
regions known to be high in androgen receptors. Of note,
A study examined learning and decision-making in adolescent (or juvenile) however, the fMRI findings show similar testosterone
(2627day-old) and adult (6070day-old) mice in a twochoice and fourchoice effects on male and female reward processing, whereas
odour-based foraging task166. The mice learned to discriminate different odours and the structural findings showed sex differences, with tes-
learned which one was associated with a reward. Subsequently, the reward was paired
tosterone being associated with grey matter thinning in
with a different odour, and the reversal phase of the task assessed how fast the juvenile
and adult mice learned this new association. The adolescent mice learned the
girls but with grey matter thickening in boys154.
fourchoice discrimination and reversal faster than adult mice, with shorter choice There is a need for a better understanding of the
latencies and more focused search strategies, suggestive of increased behavioural effects of testosterone (and other hormones) on behav-
flexibility. The authors interpreted these findings as suggesting that adolescent mice iour and brain function during human adolescent devel-
are optimized to make flexible decisions in uncertain and unstable environments, opment. The evidence for the role of testosterone in
which are likely to be encountered during adolescence. social motivation (in animal studies and studies in adult
humans) raises compelling questions about the role of
testosterone in socialaffective changes during adoles-
frontal cortical systems in flexible ways may promote cence. For example, if the pubertal surge in testoster-
key aspects of learning and socialaffective development one levels amplifies the motivational salience of social
in adolescence. status (in both boys and girls), adolescents may show a
general increase in the motivation to be admired. The
The role of hormones on socialaffective development. specific types of behaviour (and reward learning) that
There has been growing interest in the cognitive, affective result from this increased motivation could vary widely
and social effects of puberty-related changes in the levels across cultural contexts. Thus, in a culture that admires
of several hormones, including oestradiol (which affects bold, assertive behaviour in boys but not in girls, different
prefrontal functioning 145), oxytocin (which influences adolescent experiences in boys versus girls may sculpt
social bonding and social motivation146), and adrenal motivational learning in fundamentally different ways
androgens (dehydroepiandrosterone or dehydroepian- through patterns of adolescent experience. Similarly, in
drosterone sulphate) and testosterone (which influence a Tibetan Buddhist monastery, where adolescent boys
the motivation to attain and maintain social status147149). may be competing for social status by demonstrating
Among these, we believe that the social effects of testos- the greatest kindness and compassion, the testosterone-
terone are particularly relevant to understanding some amplified desire to be admired might promote a very dif-
key changes in adolescence. Animal and human studies ferent pattern of motivational learning in boys than in
have shown that testosterone influences neural systems other societies. These examples highlight the importance
that regulate reward and social motivation. For exam- of interactions between biology and social context in the
ple, in juvenile animals, testosterone has a crucial role refinement of neural circuitry in adolescence.
in rough-and-tumble play, which serves as an important
preparatory precursor to competition for dominance, ter- Conclusions and future directions
ritory maintenance and access to mates. Specifically, tes- As highlighted in this Review, some of the most com-
tosterone acts to direct attention and enhance approach pelling questions about the adolescent window of matu-
to threatening social situations150. Data from human stud- ration focus on the affective dimension of motivations
ies including behavioural studies in which testosterone and goals. This includes mechanistic questions about
was administered to adults, experimental economic stud- hormone-specific effects in early adolescence that con-
ies and functional neuroimaging studies have provided tribute to the intensification of feelings related to social
compelling evidence for the role of testosterone as a social valuation. Progress in understanding these mechanistic
hormone147149. Together, these findings indicate that tes- questions may provide insights into the unique oppor-
tosterone promotes the search for and maintenance of tunities for motivational learning in adolescence. For
social status, and that testosterone alters the appraisal of example, how do social and affective learning in ado-
threats and rewards particularly when these are rele- lescence contribute to the development of individual
vant to social status147,148. A recent fMRI study in adults151 differences in motivational priorities, such as enduring
showed that testosterone appears to cause a functional heartfelt goals? It seems clear that these learning pro-
decoupling of amygdala and ventral PFC activity. The cesses involve implicit and affective aspects of devel-
studies conducted in adults may be relevant to models of oping ones values and attitudes as well as the explicit
adolescent brain development because there is growing cognitive processes of setting priorities. For example,
evidence for pubertal changes in ventral PFC, including individual differences in the tendencies to be kind, hon-
the emergence of sex-differences at puberty 11. est and loyal in a romantic relationship may have as
To date, few studies have directly investigated much to do with ones feelings about these values as with
how testosterone influences adolescent development. consciously weighed decisions about the consequences
Preliminary findings from fMRI studies suggest that of such behaviours. Another example concerns acquired
testosterone levels correlate with maturational changes intrinsic motivations in adolescence. Progress in identi-
in reward processing in adolescent boys and girls152,153. fying the neurodevelopmental underpinnings of these
Structural MRI studies have shown associations between acquired motivations are relevant to understanding the
circulating testosterone levels and cortical thickness in development of healthy versions of inspired passions as
the left inferior parietal lobule, middle temporal gyrus, well as vulnerabilities for developing unhealthy versions

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REVIEWS

of acquired motivations, such as drug and alcohol use style (more flexible, exploratory and sensitive to social
and reckless versions of thrill-seeking. affective influences) compared with adults. This notion
It seems likely that during several phases of develop- argues against the idea that the adult brain is the optimal
ment across the lifespan, neural systems in the PFC may or normal functional system and that differences during
have some experience-expectant qualities that is, adolescent development represent deficits.
they may have windows of development during which As we have described in this Review, there is a com-
the brain expects or is biologically prepared for learn- pelling need for studies that advance, refine and test key
ing. These qualities enable adaptive adjustments that features of this heuristic model at the level of the underly-
are relevant to the challenges and opportunities that ing neural changes, in large part because these questions
tended to occur at that phase of development during our have such relevance to early intervention and prevention
evolutionary history. Accordingly, the social challenges for a wide range of adolescent-onset health problems, as
and changes facing adolescents (throughout human his- well as broad implications for health, education, juvenile
tory 155) may have favoured a slightly different cognitive justice and social policies aimed atyouths.

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