Content uploaded by Bertrand Olliac
Author content
All content in this area was uploaded by Bertrand Olliac on Jan 08, 2018
Content may be subject to copyright.
Adolescent brain development, risk-taking and vulnerability to addiction
Jacques Dayan
a,b,
⇑
, Alix Bernard
c
, Bertrand Olliac
d
, Anne-Sophie Mailhes
b
, Solenn Kermarrec
b
a
Inserm-EPHE-Université de Caen/Basse-Normandie, Unité U923, GIP Cyceron, CHU Côte de Nacre, Caen, France
b
Service Hospitalo-Universitaire de Psychiatrie de l’enfant et de l’adolescent, Université de Rennes 1 et CHGR, France
c
Equipe d’accueil 2646, PPI, Université d’Angers, France
d
Service Hospitalo-Universitaire de Psychiatrie de l’enfant et de l’adolescent, Université de Limoges, France
article info
Keywords:
Adolescent
Risk
Addiction
Prefrontal cortex
Psychoanalysis
Neuroimagery
abstract
Adolescents (12–18 years old) and young adults (18–25 years old), are more likely than older adults to
drive-or agree to be driven-recklessly or while intoxicated, to use illicit or dangerous substances and to
engage in both minor and more serious antisocial behaviour. Numerous factors during adolescence may
lead to or favour initiation of drug use, such as sensation-seeking, gregariousness and social conformity.
These aspects, however, cannot be dissociated from the increased sex drive and quest for an integrated
self. In the separation-individuation process, relationships with peers play many different roles: a field
for experimentation, emotional support, a place for ‘‘projection” and ‘‘identification”, and the possibility
of finding a partner. Unsurprisingly, therefore, drug use generally takes place in a group setting. Despite
evidence of heightened real-world risk-taking, laboratory studies have yet to yield consistent evidence
that adolescents, when on their own, are more inclined towards risky behaviour than their elders. More-
over, their comprehension and reasoning abilities in risky decision-making situations are roughly equiv-
alent to those of adults. Structural and functional neuroimaging studies have shown that neural circuitry
undergoes major reorganization during adolescence, particularly in those regions of the brain relating to
executive functions, the self and social cognition, and that the ‘‘emotional brain” may play a role in that
reorganization. Age-related decreases in gray matter volume mainly reflect a reduction in the number
of synapses and the complexity of axonal ramifications. By 18–20 years old, most of the subcortical white
matter and association pathways have reached a plateau. Risk-taking behavior and novelty-seeking may
provide, with an appropriate feed back, a mechanism to optimize brain development in adolescence.
Ó2010 Elsevier Ltd. All rights reserved.
1. Introduction
Cross sectional and, more recently, longitudinal studies have
demonstrated that the prevalence of drug use increases noticeably
during adolescence, peaking in late adolescence and early adult-
hood (Degenhardt et al., 2008; Johnston et al., 2007). For instance,
in a representative sample of 8098 subjects aged 5–54 years (US
National Comorbidity Survey), Wagner and Anthony (2002) esti-
mated peak values for initiating alcohol and marijuana use at
18 years and cocaine use at 20 years, using survival analysis tech-
niques. Individuals drink their heaviest in their late teens and early
to mid-twenties, with 44% of college students displaying binge
drinking every 2 weeks (Wechsler and Kuo, 2000). The natural his-
tory of tobacco smoking in adolescence is variable, with phases of
cessation, reduced use and relapse. In a longitudinal study, Van De
Ven et al. (2010) found that the prevalence of nicotine dependence
in young adults was 16.9% for adolescent smokers. Substance
experimentation during adolescence elevates the risk of persistent
substance use and substance use disorders in later life stages for all
types of drugs (Palmer et al., 2009; Bauman and Phongsavan, 1999;
Brook et al., 1999;Kapusta et al., 2007; Riggs et al., 2007; Winters
et al., 2008). Given that increased risk-taking during adolescence
(Furby and Beyth-Marom, 1992) has consistently been regarded
as a major risk factor for initiating drug use during this period,
we discuss how cognitive neuroscience, particularly data provided
by neuroimaging studies, can complement psychoanalytic con-
structs and thus enhance our understanding of this subject.
2. Risk-taking during adolescence: a psychoanalytic perspective
Psychoanalytic theories of adolescence consider exploratory
behaviour to be a normal, and even necessary (philosophically
speaking), component of development during this period. Explora-
tion is motivated by several concomitant factors, such as the search
for a sexual partner, at a time of redefinition of the self and the quest
for self-affirmation. This is set against the backdrop of a weakened
sense of security, as adolescents drift away from their parents and
0928-4257/$ - see front matter Ó2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jphysparis.2010.08.007
⇑
Corresponding author. Address: Laboratoire Unité U923, CHU Côte de Nacre,
Caen, France. Tel.: +33 011 336 62 57 89 04.
E-mail address: dayan-j@chu-caen.fr (J. Dayan).
Journal of Physiology - Paris 104 (2010) 279–286
Contents lists available at ScienceDirect
Journal of Physiology - Paris
journal homepage: www.elsevier.com/locate/jphysparis
start to entertain ambivalent feelings towards them. In this com-
plex and uncomfortable context, adolescents are prone to seek an
immediate solution to their internal or external conflicts and,
accordingly, to favour immediate action. Although there are consid-
erable interindividual variations in behaviour, this tendency may
result in an increase in psychosocial and physical damage. For many
adolescents, action serves as a major testing ground for the process
of self-definition (Blos, 1967, 1980, 1989; Erikson, 1956). Adoles-
cence is the first time that an individual’s sexual identity and sense
of him- or herself as a sexual being is principally measured by what
he or she does, rather than simply wishes to do, and not just by what
his or her parents say or how they react (Ritvo, 1971). However, this
is true not only for sexual identity and behaviour, but also for a wide
range of other behaviours which help to shape social identity. Both
the quality of their emotional experiences (valence and intensity)
and the judgments of their peers contribute to the fine-tuning of
adolescents’ actions and values. This process of self-definition
through action ultimately makes an important contribution to the
relatively stable self-representations of adulthood.
The first psychoanalytic conceptualization of adolescence
(Freud, 1905) focused on the revival and transformation of infan-
tile development and infantile conflict, both preoedipal and oedi-
pal, by the biological event of sexual maturation. Freud regarded
adolescence as a transitional period, during which new solutions
to infantile internal conflicts become possible due to psychic and
sexual maturation. This theory, however, had limited efficacy in
the treatment of adolescent disorders. New theories subsequently
emerged, mainly after the Second World War, in which narcissistic
preoccupations and the construction of the self became central. In
a sense, self was seen as a psychosocial processing system as it was
to be in later neurocognitive constructs (Klaczynski, 2004). How-
ever, previous key concepts, such as the importance of sex drive (li-
bido) and (unconscious) conflict theory, were retained in the
psychoanalytic model. There were many similarities between the
observations and key theoretical points made by the most eminent
researchers of the day, such as Blos and Erikson in the United
States and Winnicott in Europe. Although the impact of sexual
maturation on behaviour, mood, thought and affect was confirmed
by treatment, other key concepts were actively investigated, in or-
der to improve the efficiency of the therapy. Thus, the search for a
coherent identity, an integrated self, in a period of metamorphosis,
correlative to new desires and new abilities, emerged as a central
construct. Erikson (1956) described what he called the adolescent
task of ‘‘weaving internal tastes, talents, and values together with
elements of one’s life history and the demands of one’s culture into
a coherent identity”. From a developmental perspective, adoles-
cence can be understood as ‘‘passing stages of tentative role try-
outs of the new pubertal self in all its potential realizations
working synergically toward a postchildhood identity” (Blos,
1962). According to Blos, this process brings in its wake a decrease
in developmental plasticity, metaphorically speaking, and a grow-
ing rigidity of the personality. New findings on brain development
tend to confirm this observation. This final phase of reduced plas-
ticity corresponds to the emergence of character.
Blos (1958, 1989) emphasized another crucial point in the
development of adolescents, namely the need for social recognition
of their ability to function as an autonomous and personal self, in
the form of ‘‘a confirmation of their gender, as manifested in social
expressions, realized in fantasy, self-gratification, or bodily affec-
tive interaction with the same or other sex”. Self-idealization is
also a typical aspect of adolescence and serves to regulate self-es-
teem (Blos, 1958, 1967). This period is usually characterized by
changing behaviours, accompanied by mood swings, increased
withdrawal, a disposition towards social isolation, but at the same
time insatiable and irrepressible gregariousness. Relationships
oscillate between being active and passive and between sharing
with others, including peers and parents, and being shared by
them. Winnicott (1965) emphasised the challenge faced by adoles-
cents when they acquire the physical abilities ‘‘for genital experi-
ence and also for actual killing” that were only fantasies in their
childhood. He referred to the necessity, in terms of the develop-
ment of the personality structure (ego), of ‘‘experiencing instinc-
tual drives and the object relationships that have the instinctual
drives as a basis”. Hence, this ‘‘experiencing”, which inevitably
leads to an increased rate of risky behaviour, is regarded as a com-
ponent of any ‘‘healthy” adolescence.
High-risk behaviours may also be displayed by adolescents suf-
fering from mental disorders, such as antisocial personality or
affective disorders. As the causes of these types of behaviours
are, to a certain extent, the same for all adolescents, they can shed
light on the risky behaviours of healthy individuals. Narcissistic
rage and violent behaviours, or withdrawal of cathexis, may
emerge in response to disillusionment with parents, common to
both healthy and vulnerable adolescents. In view of this, adoles-
cence may be best understood through the prism of the develop-
mental phase of early childhood.
For adolescents, an excess of activity is no more ‘‘risky” than an
excess of passivity. During adolescence, the psychic conflict be-
tween the activity and passivity of the ego is reflected in an exter-
nalized conflict over action: the ego’s task is to restrain and contain
impulses, as well as to release and gratify them. It should be noted
here that the term ‘‘ego” is sometimes used in the literature to re-
place ‘‘self” and refers to a construct that is indeed vaguely similar
to self and not so very far removed from the cognitive concept of
‘‘central executive” (Bornstein, 2005). Similarly, there are a number
of discrepancies between the terms used to characterise adolescent
behaviours. For example, it is commonly said that ‘‘adolescents are
characterised as impulsive” and prone to ‘‘risk-taking”, with these
constructs sometimes being used synonymously. However,
although adolescents may be impulsive in some situations, they
may also be passive and inhibited, while adults routinely react
promptly and even impulsively. Rates of accidental deaths or inju-
ries in the United States and Europe, for instance, are higher among
young adults (18–25 years) than among adolescents. Peaks for
drug use and dependence, although they vary according to the
country being studied, often occur around or after 18 years.
When adolescents find themselves in a situation with no
acceptable solution for the preservation of their self-esteem or
self-identity, they may choose a risky solution. This relatively fre-
quent attitude may be described as impulsive, but also underlines
the adolescent’s need to preserve his or her future, as ethical
choices predominate at this stage of development. Another behav-
iour which may be called impulsive is ‘‘acting out”, an unconscious
ego defence mechanism which is brought into play when individ-
uals engage in some kind of behaviour that serves to ease the emo-
tional pain and anxiety associated with an unconscious conflict
between their drive and their conscience.
2.1. Risk-taking alone is not a sufficient condition for addiction
Freud (1927) wrote that human beings cannot avoid using ‘‘sed-
atives”, of which there are at least three kinds: those that decrease
our suffering, those that give us substitute satisfactions and those
that make us insensitive to our misery. According to this state-
ment, every civilization uses drugs and a large number of human
beings experience drugs during adulthood. In some cases, drug
use is associated with mental disorders, such as antisocial behav-
iour disorder, posttraumatic stress disorder, depression and narcis-
sistic personality disorder. Addiction differs from simple use or
even misuse because it is a compulsive, self-maintained phenome-
non. Drug use, particularly if repeated, allows individuals to ascribe
less importance to relationships and decreases torments and wor-
280 J. Dayan et al. / Journal of Physiology - Paris 104 (2010) 279–286
ries about their social life. According to Freud, in a letter to Fliess
dated 22 December 1897, (Freud, 1985) the prototype of addiction
(‘‘the great habit”) is masturbation, a narcissistic and mechanically
driven source of satisfaction, associated with a repetitive and
impoverished fantasy life, and ‘‘alcohol, morphine, tobacco are only
substitutes”. When drugs gradually invade people’s lives, represen-
tations associated with the use of the toxic substance increasingly
take the form of ‘‘memories in the body” (Gaddini, 1992) or ‘‘sym-
bolic equations” (Segal, 1957), and generally obey the rules of the
primary process (Freud, 1900). Freud (1912) also propounded the
notion of competition between normal sexuality and the compul-
sion for a particular substance in the case of addiction. He later
wrote that intoxication is a means of escape from pain, substituting
the pleasure principle for the reality principle (Freud, 1927)
According to Glover (1932b), drugs appear to obliterate instinctual
tension or frustration, by ‘‘cutting off” the outside world. This ac-
counts for the extreme sense of compulsion associated with addic-
tion. However, as the latter is a process associated with a specific
brain dysfunction that seems to be similar for adolescents and
adults, it will not be studied here.
2.2. The path to addiction can be understood as resulting from an
inability to tolerate affect
Although drug use is frequently initiated during adolescence, it
has yet to be established whether single or even repeated use is en-
ough for an individual to become addicted. As previously reported,
the peak for drug initiation is after 17 years, depending on the sub-
stance (with the exception of tobacco), and the peak for depen-
dence after 18 years. It could therefore be argued that addiction
is primarily a phenomenon of early adulthood.
Drugs relieve psychological suffering. According to Khantzian
(1997) opiates attenuate feelings of rage or violence, alcohol re-
lieves feelings of isolation, emptiness and anxiety, and stimulants
can increase hypomania, relieve depression and counteract hyper-
activity and attention deficit. Although prolonged self-medication
may lead to addiction, it does not appear to be the main cause.
Addiction, which presupposes craving and dependence, has been
linked to early developmental failures (Johnson, 1999) leading to
an inability to tolerate affects and thence to regulate self-esteem
or relationships (Krystal, 1982; Zinberg, 1975). To conclude, the
psychoanalytical approach distinguishes between simple drug
use and addiction, although their causation and maintenance
may overlap. In adolescence, the former results mainly from the
tendency to explore the environment with one’s peers, although
a reduction in one’s active fantasy life and high levels of anxiety
are often involved in addiction. Unsurprisingly, therefore, drug
use generally takes place in a group setting and involves a degree
of social ritualism-two elements which play a major role in com-
bating anxiety and distress (Glover, 1932a; Johnson, 1999; Johnson
et al., 2000; Khantzian, 1997; Hopper, 1981). Moreover, in the case
of addiction, uncertainty in social, sexual and affective relation-
ships tends to disappear, to be replaced by highly conventional
and ritualized behaviours, leading to compulsory satisfaction.
Hence, faced with the pressure of a burgeoning sex drive and the
need to engage in relationships, vulnerable personalities unable
to withstand deceit, distress, shame, anger and anxiety may find
in addiction a substitute for real life. Self-coherence is, at least
for a while, maintained with the support of the drug.
3. Risk-taking during adolescence: neuropsychological aspects
The advent of neuroimaging has profoundly modified our
knowledge of adolescent brain development acquired from animal
or post mortem studies.
Structural and functional neuroimaging studies have revealed
that neural circuitry undergoes a major reorganization in adoles-
cence, particularly in those regions of the brain involved in execu-
tive functions, the self and social cognition. Functional
neuroimaging has shown that these regions also play a key role
in the regulation of behaviour and emotion, and in the perception
and evaluation of risk and reward. Accordingly, ‘‘impulsivity, risk-
taking behavior, and novelty-seeking may provide a mechanism to
expand the range of possibilities that will then provide the appro-
priate feedback for optimal sculpting of the brain” (Luna et al.,
2001).
3.1. Structural neuroimaging
Most studies of structural brain development take the form of
either magnetic resonance imaging (MRI) measurements of grey
matter (GM) and white matter (WM) volumes or, more recently,
diffusion tensor imaging (DTI) investigations of the macro- and
microstructure of WM. Results are consistent, whether they are
yielded by cross-sectional studies, some with large cohorts of chil-
dren (N> 200), or by the somewhat sparser longitudinal studies,
generally involving smaller samples (Gogtay et al., 2004;N= 13)
though with some notable exceptions (Shaw et al., 2006;N= 307).
3.1.1. Grey matter maturation
Put succinctly, GM volume undergoes a prepubertal increase,
followed by a postpubertal loss. Considerable developmental
changes occur in GM volume, density and cortical thickness be-
tween childhood and adulthood. Age-related decreases in apparent
GM volume mainly reflect a reduction in the number of synapses
and the complexity of axonal ramifications, due to accelerated
elimination or ‘‘synaptic pruning”, with an attendant increase in
the degree of myelination of intracortical axons. Cortical complex-
ity decreases during adolescence in both the left and right hemi-
spheres (White et al., 2010). Overall, GM volumes display
heterogeneous developmental trajectories across the major lobes,
peaking in the frontal lobes at around 11 years, but continuing to
increase in the temporal lobes until 14 years. Longitudinal studies
of GM development at functionally subregional levels also point to
heterochronic maturational trajectories. Typically, the primary
sensorimotor cortices and the frontal and occipital poles mature
first, with maturation proceeding rostrally, from the parietal areas
to the frontal ones, and caudally and laterally over the parietal,
occipital and, late after adolescence, temporal cortices.
The dorsolateral prefrontal cortex (DLPFC) and the superior
temporal cortex, which contain association areas that integrate
high-level information in several sensory modalities, are the last
to mature, after 16–17 years (Gogtay et al., 2004), suggesting that
the higher-order association areas only mature after the lower-or-
der sensorimotor regions, whose functions they integrate, have
matured. The DLPFC serves as the highest-order cortical area,
responsible for executive functions such as motor planning, organi-
zation and regulation. It is also involved in working memory. The
superior temporal gyrus (STG) has also been identified as a critical
structure in social cognition. The reduction in size of the DLPFC at
the end of adolescence suggests that pruning/myelination may oc-
cur in parallel (Giorgio et al., 2010; Gogtay et al., 2004). Three re-
cent studies examined changes in regional cortical thickness in
relation to various cognitive functions, namely IQ for Shaw et al.
(2006), memory for Sowell et al. (2001a,b) and executive functions
(inhibition, shifting and updating) for Tamnes et al. (2010). Chil-
dren with the best scores demonstrated a particularly plastic cor-
tex, with an initial accelerated and prolonged phase of cortical
increase followed by a particularly vigorous phase of cortical thin-
ning. Frontal lobe GM thinning was also more strongly predictive
of memory capacity (Sowell et al., 2001a,b). GM reduction in the
J. Dayan et al. / Journal of Physiology - Paris 104 (2010) 279–286 281
frontal cortex observed between adolescence (12–16 years) and
early adulthood (23–30 years) is also associated with changes in
the striatum, putamen and globus pallidus-structures implicated
in risk-taking. The maturation of these frontostriatal regions may
be subserved by enhancing long-distance connectivity in different
WM tracts, and then increasing the ‘‘fine-tuning” of neuronal con-
nectivity. In adults, complex tasks may be accomplished more
automatically, with the recruitment of phylogenetically ancient
parts of the brain such as the striatum and cerebellum.
3.1.2. White matter maturation
Contrary to GM, WM volumes increase roughly linearly
throughout the first four decades of life, with a peak around the
mid-forties, when speed for certain fine motor skills is also opti-
mal. Lebel et al. (2008)’s extremely interesting study conducted
on a large sample (N= 202, aged 5–30 years) showed that the brain
undergoes major microstructural changes during adolescence and
indeed beyond, until 25 years. By 18–20 years, most of the subcor-
tical WM and association pathways have reached a plateau. How-
ever, significant maturation has been observed between 20 and
25 years, notably of the corticospinal tract, lenticular and caudate
nuclei, and thalamus. The cingulum and the uncinate fasciculus
continue their maturation beyond 25 years. This study is one of
several reporting nonlinear development, with frontal tracts
maturing later than the more posterior ones (Lenroot et al.,
2007). The exponential development of WM during adolescence
may be regarded as a continuation of the exponential patterns of
development observed during infancy and early childhood (during
the first 5 years of life, fractional anisotropy (FA) values increase by
up to 200%).
Some studies have associated DTI indices with cognitive mea-
sures, such as intellectual abilities (Schmithorst et al., 2005) and,
more recently, verbal skills. In a group of 168 participants aged
8–30 years, Tamnes et al. (2010) found that high verbal abilities
were associated with accelerated WM development in late adoles-
cence/early adulthood before reaching a plateau, unlike average
verbal abilities, which were correlated with more protracted devel-
opment that continued into early adulthood. Liston et al. (2006) re-
ported a relationship between frontostriatal radial diffusivities and
inhibition abilities. Once more, these studies highlight the impor-
tance of the frontostriatal network in the development of executive
functions.
A handful of studies have combined volume- and tract-based
analyses. In 2010, Giorgio et al. reported the first longitudinal
study to have focused on the adolescent period (13–18 years). Data
showed that GM volumes decreased in many cortical areas, includ-
ing higher-order association areas, such as the DLPFC, as well as in
primary sensorimotor and sensory cortices. Conversely, WM vol-
umes increased in several regions, notably the frontal lobe, corpus
callosum and arcuate fasciculus.
In conclusion, neuroimaging studies have shown that an exten-
sive reorganization of neural circuitry takes place during adoles-
cence, particularly in those regions of the brain involved in
executive functions, the self and social cognition. This reorganiza-
tion primarily constitutes a simplification of neural circuitry and
could be interpreted as the optimisation of the neural circuits in-
volved in high-level tasks. Although the conditions governing syn-
aptic pruning have yet to be fully elucidated, these modifications
probably have an adaptive value and are determined, at least in
part, by the experiences of pleasure or displeasure resulting from
the various strategies used by adolescents in the new and complex
tasks that they are called upon to undertake during this period. The
development of WM fibres allowing faster or more intense connec-
tions between different areas of the brain could well contribute to
these changes. Then again, as it is a secondary phenomenon and
takes place over a protracted period, it may simply serve to estab-
lish connections between brain regions that have already under-
gone considerable maturation. It has been suggested that the
gyrification that occurs between childhood and adolescence, as op-
posed to the gyrification that is observed in the first months of life
and which is mainly mediated by genetics, may be influenced
mainly by the environment and thus by the individual’s own expe-
riences. Studies of twins have confirmed the validity of this ap-
proach. Gyrification in adolescence (White et al., 2010) may well
be triggered by the development of white matter fibre tracts con-
necting more or less widely separated areas of the brain. An indi-
vidual’s specific experiences may influence the way in which
these tracts are organized.
3.1.3. Sexual dimorphism
Recent MRI studies have reported sexual dimorphism in the
development of brain structure and function during adolescence
(Lenroot and Giedd, 2010; Schmithorst et al., 2008). First, total
brain volume is about 10% greater in males, and peaks at 10.5 years
in females and 14.5 in males (Lenroot et al., 2007). The GM trajec-
tory also peaks 1–2 years earlier in females, while males may have
a steeper rate of WM development during adolescence. Studies
using magnetization transfer ratio (MTR) values also point to a
possible sexual dimorphism during adolescence, involving an in-
crease in axonal calibre in males (Perrin et al., 2008), as opposed
to increased myelination in females (Perrin et al., 2009). Sexual
dimorphism can also be observed at a regional level. The regions
most frequently reported by imaging studies as displaying mor-
phological sex differences include the basal ganglia (larger in fe-
males) and limbic structures (larger hippocampus and smaller
amygdala in females). Concerning WM, a study of a large group
of children and adolescents found greater FA in boys, in associative
WM regions (including the frontal lobes), and greater FA in girls, in
the splenium of the corpus callosum (Schmithorst et al., 2008).
Increasing FA values reflect increasing myelination or increases
in axonal calibre and possibly increasing fibre organization, result-
ing in decreased tortuosity. This variability has notable behavioural
consequences. For instance, a study in 21 adolescents, looking at
impulse control, found that different WM regions were associated
with task performance in male and female adolescents (Silveri
et al., 2006).
3.2. Functional neuroimaging: exploration and risk-taking
Neuroimaging studies can often complement or extend purely
behavioural studies, which have yielded the following main
findings.
3.2.1. Behavioural studies
In cognitive psychology, risk-taking has been associated with an
increased tendency towards sensation-seeking and immediate re-
ward-seeking, and a lack of inhibition (Tamm et al., 2002). Some
authors, focusing on cognitive abilities, have suggested that adoles-
cents are less liable to consider the negative repercussions of re-
warded behaviour in hypothetical scenarios (Reppucci, 1999).
However, this opinion is controversial and there is substantial evi-
dence that adolescents are well aware of the risks they take, with
few differences found between adolescents and adults in the spon-
taneous mention of the costs and benefits associated with several
risky actions (Alexander et al., 1990; Beyth-Marom et al., 1993).
Moreover, there is little evidence of any systematic improvement
in logical abilities related to decision-making past 16 years (Over-
ton, 1990). Increasing adolescents’ awareness of various risks has
little impact on their decision-making outside the laboratory. Dif-
ferences between adolescents and adults may rely more on the
inability of the former to automatically engage in social rules. Cau-
ffman and Steinberg (2000) examining how a sample of over a
282 J. Dayan et al. / Journal of Physiology - Paris 104 (2010) 279–286
thousand participants aged 12–48 years scored on ‘‘socially
responsible decision-making” found that, on average, adolescents
aged below 18–19 years scored significantly lower than adults.
However, there were considerable interindividual differences in
judgments within each adolescent age group.
These data can be more easily understood if we consider the
process of socialization among adolescents, as relations with peers
play a major role in the construction of the ‘‘social self”. Typical
laboratory studies of risky decision-making fail to consider the so-
cial context in which risk-taking occurs in ‘‘real life” (Steinberg and
Cauffman, 1996; Steinberg, 2004, 2008, 2010). In such studies,
individual adolescents are presented with hypothetical dilemmas
under conditions of low emotional arousal and are then asked to
make and explain their decisions. In the real-world, adolescents of-
ten make decisions under conditions of emotional arousal and in
peer groups. Heightened levels of susceptibility to peer influence
have been shown to characterize adolescence even in laboratory
studies (Steinberg and Silverberg, 1986). Gardner and Steinberg
(2005) showed that the participation of peers (two friends) in a
driving simulation video game led to an increase in risky driving
for adolescents, but not for adults. Adolescents showed the same
level of risk-taking as adults when they were alone. This has
prompted some to argue that age differences in risky behaviour
may be better accounted for by differences in psychosocial func-
tioning than by differences in more cognitive aspects of risk orien-
tation, such as risk preference (Steinberg and Cauffman, 1996).
Adolescents tend to base decisions on temporally proximal out-
comes rather than on distal ones (Gardner and Herman, 1991), and
in some contexts, are better motivated by reward than by negative
reinforcement (Arnett, 1992; Gardner and Herman, 1991). In a psy-
chodynamic construct, these trends reflect the complex quests
undertaken by adolescents and their need to experience and social-
ize, at a time when the values of the past are being deeply ques-
tioned and yet the values of the future remain uncertain, and
when adolescents need their actions to be validated by their peers.
To put it more dramatically, actions focusing on immediate reward
may also be explained by ‘‘uncertainty about the meaning and the
value of life” (Winnicott, 1965).
3.2.2. Exploration and risk-taking as seen through functional
neuroimaging
Structural studies have highlighted significant changes in many
regions of the prefrontal cortex, notably the dorsolateral and ven-
tromedial regions, throughout adolescence. These changes help to
improve various executive functions which contribute to the regu-
lation of affect and behaviour. The dorsolateral part of the prefron-
tal cortex is preferentially involved in executive processes and
working memory, while the ventromedial part is involved in emo-
tional regulation (Stuss and Alexander, 2007). For their part, func-
tional studies point to a particularly highly developed functional
link between these highly evolved structures and the limbic sys-
tem during adolescence.
Studies featuring inhibition tasks can increase our understand-
ing of impulsive behaviours. Inhibition may generally be defined as
a function which, when the organism is faced with many possible
responses, favours one particular response without simultaneously
activating the others. Many behavioural studies have focused on
cognitive control, or inhibition, using flanker, Stroop or go/no-go
tasks. These tasks assess different kinds of inhibition but which
all share a common mechanism, namely the inhibition of a propo-
nent or automatic response. On the whole, children and adoles-
cents activate a larger cerebral network to perform the tasks
than adults. Thereafter, the number of brain regions that are re-
cruited decreases with age, so that only essential regions associ-
ated with the task are activated (Durston et al., 2002; Luna et al.,
2001; see Casey et al., 2008, for review). When Luna et al. (2001)
compared three age groups, they found that adolescents displayed
a greater volume of activation in the DLPFC during a response inhi-
bition task than either younger children or older adults, suggesting
a greater reliance on the frontal executive network. A recent meta-
analysis of the development of executive functions using func-
tional MRI (fMRI) highlighted the role of the dorsolateral and infe-
rior prefrontal cortices-regions which undergo major
reorganization during adolescence. We can hypothesise that syn-
aptic pruning and relative disconnection enable regions such as
the DLPFC to do the computations needed for the most efficient
executive functioning, while an increase in myelination, contin-
uing into adulthood, allows regions far from the DLPFC, such as
the lateral cerebellum (Luna et al., 2001), to join in and assist in
more consistent and automatic control of behaviour.
Other regions deserve further consideration. For instance, the
involvement of the right anterior insular cortex is specific to ado-
lescents as is not seen in either children or adults. This is remark-
able, considering the involvement of this particular region in
addiction (Naqvi and Bechara, 2009), self-regulation and executive
functions.
3.2.2.1. The role of the limbic cortex in the control of risky
behaviours. Hare et al. (2008) found that adolescents displayed
exaggerated amygdala activity relative to children and adults dur-
ing an emotional go/no-go task. They suggest that this greater
activity may reflect the need to compensate for relatively weak
anatomical connections between the brain regions involved in
the task, through greater ‘‘top-down” executive control (Stevens
et al., 2007). Conversely, the ventrolateral prefrontal cortex (VLPF)
has been shown to modulate amygdala engagement in both ado-
lescents and adults, in order to facilitate flexible attention and
behaviour when responding to environmental threats (Monk
et al., 2003, 2008). The greater activity observed in the VLPFC, a re-
gion massively interconnected with the amygdala, during a go/no-
go task suggests that both regions are strongly involved in this
form of executive control (Stevens et al., 2007).
Wood et al. (2005) have shown that the left VLPFC mediates po-
sitive representations (of a concept or object) and their emotional
assessment, whereas the right DLPFC mediates negative represen-
tations and the amygdala evaluative processing.
Casey et al. (2008) have postulated that high risk-taking during
adolescence is due to discrepant development between limbic and
prefrontal top-down control regions. They base their conclusions
on animal studies (Laviola et al., 1999) and imaging studies (Spear,
2000, 2002; Ernst et al., 2005; Galvan et al., 2006, 2007). According
to this model, adolescent behaviour is governed mainly by limbic
regions, as they are functionally more mature (i.e., imbalance of
limbic relative to prefrontal control), whereas in children the lim-
bic and prefrontal regions are both still developing and in adults,
these systems are fully mature. According to the authors, in emo-
tionally salient situations, the limbic system will win over control
systems in adolescents.
Although no firm conclusion can yet be drawn from these stud-
ies, it is probable that the limbic system play a major role of regu-
lation during adolescence. However, this role looks complex. Given
the need for exploratory behaviours and risk-taking, the mature
limbic system may well play a positive role, regulating and moder-
ating an immature frontal system.
3.2.2.2. The reward system: discrepant hypotheses about the role of the
ventral striatum in risk-taking. In the experimental exploration of
reward processing, different emotional and cognitive processes
can be described. Some authors differentiate between risk-seeking
(general approach to rewards) and risk-taking (positive engage-
ment in the context of uncertainty). Other authors make a distinc-
tion between anticipation and consummation. For instance,
J. Dayan et al. / Journal of Physiology - Paris 104 (2010) 279–286 283
anticipating the opportunity to respond for monetary gain acti-
vates regions of the ventral striatum (VS), an archaic region of
the brain, whereas notification of successful responses recruits a
region of the medial frontal cortex (MFC), a region dedicated to
complex tasks (Knutson et al., 2001a,b). The VS responds more
automatically to appetitive cues (Knutson et al., 2001a), whereas
the MFC appears to direct its energy towards appropriate goal ob-
jects (Elliott et al., 2000). Some studies (Spear, 2000) posit that the
striatum is relatively hyporesponsive to rewards during adoles-
cence, such that heightened reward-seeking behaviour is needed
to achieve the same activation as in adults. An alternative and pref-
erential hypothesis suggests that during adolescence, the striatal
reward system is hyperresponsive, resulting in greater reward-
seeking. Disproportionately increased activation of the VS motiva-
tional circuit may result from the influence of defective or imma-
ture inhibitory circuits (Chambers et al., 2003). Alternatively,
adolescents may be particularly motivated by the potential for
immediate reinforcement. For example, the maturation of the cau-
date (a subdivision of the striatum, together with the putamen) is
delayed in children with disorders characterized by delayed grati-
fication deficits (Castellanos et al., 2002).
3.2.2.3. Dopaminergic activity. Dopaminergic activity makes a con-
siderable contribution to changes in prefrontal-striatal-limbic
pathways (i.e., reward system) during adolescence. The peak ob-
served during adolescence or early adulthood, which declines
thereafter, predicts the increase in exploratory, risk-taking behav-
iour, and thus in reward-seeking, which cannot yet be controlled
by the immature frontal regions (Wahlstrom et al., 2010). When
Steinberg (2010) measured risky behaviours using laboratory par-
adigms, they reported a peak in performance at around 15 years.
As suggested by Steinberg (2010), this temporal disjunction exerts
a favourable influence from a developmental point of view. How-
ever, studies conducted on late adolescence, comparing adoles-
cents with young adults, are too sparse for us to pinpoint the
subsequent decline in risk-taking behaviours. Moreover, some
individuals are more vulnerable to the potentially negative conse-
quences of this neurobehavioural shift than others and their neural
responses to rewards may be different. For instance, individuals
whose genetic predispositions result in higher levels of dopamine
in neural synapses, particularly in circuits involved in reward pro-
cessing, demonstrate increased levels of brain activation in re-
sponse to rewards (Dreher et al., 2009; Hariri, 2009). However,
there are not yet any converging data on these predispositions,
which may also stem from negative experiences in infancy or early
childhood. Some studies, for instance, have reported contradictory
data about the maturation of WM and risk-taking (Berns et al.,
2009; Olson et al., 2009). Social, environmental and educational
factors may also contribute to this heterogeneity, in addition to
maturational ones. Hence, further studies are essential if we are
to understand these apparent inconsistencies.
4. Discussion
The results of neuroimaging studies are consistent with the
main concepts of psychoanalysis on adolescence, namely a transi-
tion to adulthood with a more integrated self and the development
of social skills. Laboratory studies have shown that adolescents
generally have a greater risk-taking propensity than adults,
although there is considerable interindividual variability. While
ignorance of the actual level of risk cannot be a major factor in
risk-taking by typically developing adolescents, given that their
knowledge of the risks is roughly similar to that of their elders
(Furby and Beyth-Marom, 1992; Klaczynski, 2004), sensation-seek-
ing and, above all, sensitivity to the peer group do seem to play an
important role, unlike in adults. As stated by Winnicott, adoles-
cents need to gain experience of life, if they are to learn how to live
and, more especially, if they are to find out whether life is worth
living. They must abandon many of the childhood certainties,
including the feeling of being protected by their parents, and must
also de-idealize the latter. This teleological conception of action
has been taken up by several researchers in the cognitive field,
who see risk-taking as an adaptive mechanism allowing certain
cortical structures to be optimised, particularly those involved in
social cognition.
However, several important concepts specific to psychoanalysis
are not used as tools for analysing action. This is particularly true of
‘‘drive”, including sex drive, which can in no way be reduced to the
concept of ‘‘motivation”. Furthermore, the psychoanalytic ap-
proach focuses on cathexis. As stated by Erikson (1956), the cure
process emerges amid the integration of diverse elements of per-
sonal experience, such as identity and intimacy, the past and the
present, and the world of internal object representations and
external relationships. Adolescents may sometimes modify the
way they relate to the world through their experience of the course
of treatment and through transference.
Neuroscience research tends to isolate the mechanisms of ac-
tion and seek out their brain substrates. As this information does
not arise from an individual’s own experience, unlike that relating
to a psychoanalytic cure, he or she cannot directly take this knowl-
edge on board and integrate it into his or her psychic functioning. It
can therefore be useful only as an external constraint: for example,
the training, medication, or even electrical stimulation that is
sometimes offered in cases of depression or addiction. Psychoana-
lytic referents and processes would appear to be useful tools for
decoding behaviours, and possibly for modifying them at the
risk-taking stage. They are, however, of little or no direct use at
the addictive stage.
5. Conclusion
Psychoanalytic concepts of risk-taking in adolescents are sup-
ported by the findings of brain development studies. Risk-taking
promotes the exploration of adult roles, may increase self-esteem
(see Hoge and McCarthy, 1984), and promotes reproductive suc-
cess. Risk-taking contributes to the efficient shaping of the most
highly evolved parts of the brain that are responsible for the ‘‘sapi-
ence” which characterizes the human species.
The interrelations between cognition and emotion remain rela-
tively poorly understood, and the study of adolescent brain devel-
opment would appear to offer the best conditions for studying
them. Neuroimaging studies have shown that neural circuitry
undergoes major reorganization during adolescence, particularly
in those regions of the brain relating to executive functions, the self
and social cognition, and that the ‘‘emotional brain” may play a
role in that reorganization.
References
Alexander, C.S., Kim, Y.J., Ensminger, M., Johnson, K.E., Smith, B.J., Dolan, L., 1990. A
measure of risk taking for young adolescents: reliability and validity
assessments. J. Youth Adolescence 19 (6), 559–569.
Arnett, J., 1992. Reckless behavior in adolescence: a developmental perspective.
Dev. Rev. 12 (4), 339–373.
Bauman, A., Phongsavan, P., 1999. Epidemiology of substance use in adolescence:
prevalence, trends and policy implications. Drug Alcohol Depen. 55, 187–207.
Berns, G.S., Moore, S., Capra, C.M., 2009. Adolescent engagement in dangerous
behaviors is associated with increased white matter maturity of frontal cortex.
PLoS One 4 (8), e6773.
Beyth-Marom, R., Austin, L., Fischoff, B., Palmgren, C., Jacobs-Quadrel, M., 1993.
Perceived consequences of risky behaviors: adults and adolescents. Dev.
Psychol. 29, 549–563.
Blos, P., 1958. Preadolescent drive organization. J. Am. Psychoanal. Assoc. 6, 47–56.
Blos, P., 1962. On adolescence: A psychoanalytic interpretation. Free Press of
Glencoe, New York.
284 J. Dayan et al. / Journal of Physiology - Paris 104 (2010) 279–286
Blos, P., 1967. The second individuation process of adolescence. Psychoanal. St.
Child 22, 162–186.
Blos, P., 1980. The life cycle as indicated by the nature of the transference in the
psychoanalysis of adolescents. Int. J. Psycho-Anal. 61, 145–151.
Blos, P., 1989. The place of the adolescent process in the analysis of the adult.
Psychoanal. St. Child 44, 3–18.
Bornstein, R.F., 2005. Reconnecting psychoanalysis to mainstream psychology:
challenges and opportunities. Psychoanal. Psychol. 22, 323–340.
Brook, J.S., Balka, E., Whiteman, M., 1999. The risks for late adolescence of early
adolescent marijuana use. Am. J. Public Health 89, 1549–1554.
Casey, B.J., Getz, S., Galvan, A., 2008. The adolescent brain. Dev. Rev. 28, 62–77.
Castellanos, F.X., Lee, P.P., Sharp, W., Jeffries, N.O., Greenstein, D.K., Clasen, L.S.,
Blumenthal, J.D., James, R.S., Ebens, C.L., Walter, J.M., Zijdenbos, A., Evans, A.C.,
Giedd, J.N., Rapoport, J.L., 2002. Developmental trajectories of brain volume
abnormalities in children and adolescents with attention-deficit/hyperactivity
disorder. JAMA 288 (14), 1740–1748.
Cauffman, E., Steinberg, L., 2000. (Im)maturity of judgment in adolescence: why
adolescents may be less culpable than adults. Behav. Sci. Law 18 (6), 741–
760.
Chambers, R.A., Taylor, J.R., Potenza, M.N., 2003. Developmental neurocircuitry of
motivation in adolescence: a critical period of addiction vulnerability. Am. J.
Psychiat. 160, 1041–1052.
Degenhardt, L., Chiu, W.T., Sampson, N., Kessler, R.C., Anthony, J.C., Angermeyer, M.,
Bruffaerts, R., de Girolamo, G., Gureje, O., Huang, Y., Karam, A., Kostyuchenko, S.,
Lepine, J.P., Mora, M.E., Neumark, Y., Ormel, J.H., Pinto-Meza, A., Posada-Villa, J.,
Stein, D.J., Takeshima, T., Wells, J.E., 2008. Toward a global view of alcohol,
tobacco, cannabis, and cocaine use: findings from the WHO World Mental
Health Surveys. PLoS Med. 5 (7), e141.
Dreher, J.C., Kohn, P., Kolachana, P., Weinberger, D.R., Berman, K.F., 2009. Variation
in dopamine genes influences responsivity of the human reward system. Proc.
Natl. Acad. Sci. USA 106 (2), 617–622.
Durston, S., Thomas, K.M., Yang, Y., Ulug, A., Zimmerman, R., Casey, B.J., 2002. A
neural basis for the development of inhibitory control. Dev. Sci. 5, 9–16.
Elliott, R., Dolan, R.J., Frith, C.D., 2000. Dissociable functions in the medial and
lateral orbitofrontal cortex: evidence from human neuroimaging studies. Cereb.
Cortex.
Erikson, E.H., 1956. The problem of ego identity. J. Am. Psychoanal. Assoc. 4, 56–121.
Ernst, M., Nelson, E.E., Jazbec, S., McClure, E.B., Monk, C.S., Leibenluft, E., Blair, J.,
Pine, D.S., 2005. Amygdala and nucleus accumbens activation in response to
receipt and omission of gains in adults and adolescents. Neuroimage 25, 1279–
1291.
Freud, S., 1985. In: Masson, J.M. (Ed.), The Complete Letters of Sigmund Freud to
Wilhelm Fliess, 1887–1904. Harvard University Press, Cambridge, pp. 287–289.
Freud, S., 1900. The Interpretation of Dreams. Avon, New York. pp. 1980.
Freud, S., 1905. Three Essays on the Theory of Sexuality. Basic Books, New York. pp.
123–243.
Freud, S., 1912. On the Universal Tendency to Debasement in the Sphere of Love
(Contributions to the Psychology of Love II). The Standard Edition of the
Complete Psychological Works of Sigmund Freud, Volume XI (1910): Five
Lectures on Psycho-Analysis, Leonardo da Vinci and Other Works, pp. 177–190.
Freud, S., 1927. The Future of an Illusion. The Standard Edition of the Complete
Psychological Works of Sigmund Freud, Volume XXI (1927–1931): The Future of
an Illusion, Civilization and its Discontents, and Other Works. Hogarth Press,
London, pp. 1–56.
Furby, L., Beyth-Marom, R., 1992. Risk taking in adolescence: a decision-making
perspective. Dev. Rev. 12, 1–44.
Gaddini, E., 1992. In: Limentani, A. (Ed.), A Psychoanalytic Theory of Infantile
Experience. Routledge, London.
Galvan, A., Hare, T., Parra, C., Penn, J., Voss, H., Glover, G., Casey, B.J., 2006. Earlier
development of the accumbens relative to orbitofrontal cortex might underlie
risk-taking behavior in adolescents. J. Neurosci. 26, 6885–6892.
Galvan, A., Hare, T., Voss, H., Glover, G., Casey, B.J., 2007. Risk-taking and the
adolescent brain: who is at risk? Dev. Sci. 10, F8–F14.
Gardner, W., Herman, J., 1991. Adolescents’ AIDS risk taking: a rational choice
perspective. In: Gardner, W., Millstein, S., Wilcox, B. (Eds.), Adolescents in the
AIDS Epidemic. Jossey-Bass, San Francisco, pp. 17–34.
Gardner, M., Steinberg, L., 2005. Peer influence on risk taking, risk preference, and
risky decision making in adolescence and adulthood: an experimental study.
Dev. Psychol. 41, 625–635.
Giorgio, A., Watkins, K.E., Chadwick, M., James, S., Winmill, L., Douaud, G., De
Stefano, N., Matthews, P.M., Smith, S.M., Johansen-Berg, H., James, A.C., 2010.
Longitudinal changes in grey and white matter during adolescence. Neuroimage
49, 94–103.
Glover, E., 1932a. Common problems in psychoanalysis and anthropology: drug
ritual and addiction. Brit. J. Med. Psychol. 12, 109–131.
Glover, E., 1932b. On the aetiology of drug-addiction. Int. J. Psycho-Anal. 13, 298–
328.
Gogtay, N., Giedd, J.N., Lusk, L., Hayashi, K.M., Greenstein, D., Vaituzis, A.C., Nugent
3rd, T.F., Herman, D.H., Clasen, L.S., Toga, A.W., Rapoport, J.L., Thompson, P.M.,
2004. Dynamic mapping of human cortical development during childhood
through early adulthood. Proc. Natl. Acad. Sci. USA 101, 8174–8179.
Hare, T.A., Tottenham, N., Galvan, A., Voss, H.U., Glover, G.H., Casey, B.J., 2008.
Biological substrates of emotional reactivity and regulation in adolescence
during an emotional go-nogo task. Biol. Psychiat. 63 (10), 927–934.
Hariri, A.R., 2009. The neurobiology of individual differences in complex behavioral
traits. Annu. Rev. Neurosci. 32, 247–255.
Hoge, D.R., McCarthy, J.D., 1984. Influence of individual and group identity salience
in the global self-esteem of youth. J. Pers. Soc. Psychol. 47 (2), 403–414.
Hopper, E., 1981. Forms of instrumental adjustment. In: Social Mobility: A Study of
Social Control and Insatiability. Blackwell, Oxford, pp. 225–241.
Johnson, B., 1999. Three perspectives on addiction. J. Am. Psychoanal. Assoc. 47,
791–881.
Johnson, J.G., Cohen, P., Pine, D.S., Klein, D.F., Kasen, S., Brook, J.S., 2000. Association
between cigarette smoking and anxiety disorders during adolescence and early
adulthood. JAMA 284 (18), 2348–2351.
Johnston, L.D., O’Malley, P.M., Bachman, J.G., Schulenberg, J., 2007. Monitoring the
Future National Survey Results on Drug Use, 1975–2006, vol. II.
Kapusta, N.D., Plener, P.L., Schmid, R., Thau, K., Walter, H., Lesch, O.M., 2007.
Multiple substance use among young males. Pharmacol. Biochem. Behav. 86,
306–311.
Khantzian, E.J., 1997. The self-medication hypothesis of substance use disorders: a
reconsideration and recent applications. Harv. Rev. Psychiat. 4 (5), 231–244
(review).
Klaczynski, P.A., 2004. A dual-process model of adolescent development:
implications for decision making, reasoning, and identity. Adv. Child Dev.
Behav. 32, 73–123 (review).
Knutson, B., Fong, G.W., Adams, C.M., Varner, J.L., Hommer, D., 2001a. Dissociation
of reward anticipation and outcome with event-related fMRI. Neuroreport 12
(17), 3683–3687.
Knutson, B., Adams, C.M., Fong, G.W., Hommer, D., 2001b. Anticipation of increasing
monetary reward selectively recruits nucleus accumbens. J. Neurosci. 21 (16).
Krystal, H., 1982. Adolescence and the tendencies to develop substance
dependence. Psychoanal. Inq. 2, 581–617.
Laviola, G., Adriani, W., Terranova, M.L., Gerra, G., 1999. Psychobiological risk factors
for vulnerability to psychostimulants in human adolescents and animal models.
Neurosci. Biobehav. Rev. 23 (7), 993–1010.
Lebel, C., Walker, L., Leemans, A., Phillips, L., Beaulieu, C., 2008. Microstructural
maturation of the human brain from childhood to adulthood. Neuroimage 40
(3), 1044–1055 (Epub 2008).
Lenroot, R.K., Giedd, J.N., 2010. Sex differences in the adolescent brain. Brain Cogn.
72 (1), 46–55.
Lenroot, R., Gogtay, N., Greenstein, D., Wells, E., Wallace, G., Clasen, L., Blumenthal,
J.D., Lerch, J., Zijdenbos, A.P., Evans, A.C., Thompson, P.M., Giedd, J.N., 2007.
Sexual dimorphism of brain developmental trajectories during childhood and
adolescence. Neuroimage.
Liston, C., Watts, R., Tottenham, N., Davidson, M.C., Niogi, S., Ulug, A.M., Casey, B.J.,
2006. Frontostriatal microstructure modulates efficient recruitment of
cognitive control. Cereb. Cortex 16 (54), 553–560.
Luna, B., Thulborn, K.R., Munoz, D.P., Merriam, E.P., Garver, K.E., Minshew, N.J.,
Keshavan, M.S., Genovese, C.R., Eddy, W.F., Sweeney, J.A., 2001. Maturation of
widely distributed brain function subserves cognitive development.
Neuroimage 13, 786–793.
Monk, C.S., McClure, E.B., Nelson, E.E., Zarahn, E., Bilder, R.M., Leibenluft, E., Charney,
D.S., Ernst, M., Pine, D.S., 2003. Adolescent immaturity in attention-related brain
engagement to emotional facial expressions. Neuroimage 20 (1), 420–428.
Monk, C.S., Telzer, E.H., Mogg, K., Bradley, B.P., Mai, X., Louro, H.M.C., Chen, G.,
McClure-Tone, E.B., Ernst, M., Pine, D.S., 2008. Amygdala and ventrolateral
prefrontal cortex activation to masked angry faces in children and adolescents
with generalized anxiety disorder. Arch. Gen. Psychiat. 65, 568–576.
Naqvi, N.H., Bechara, A., 2009. The hidden island of addiction: the insula. Trends
Neurosci. 32 (1), 56–67.
Olson, E.A., Collins, P.F., Hooper, C.J., Muetzel, R., Lim, K.O., Luciana, M., 2009. White
matter integrity predicts delay discounting behavior in 9- to 23-year-olds: a
diffusion tensor imaging study. J. Cogn. Neurosci. 21 (7), 1406–1421.
Overton, W., 1990. Competence and procedures: constraints on the development of
logical reasoning. In: Overton, W. (Ed.), Reasoning, Necessity, and Logic:
Developmental Perspectives. Erlbaum, Hillsdale, NJ, pp. 1–32.
Palmer, R.H.C., Young, S.E., Hopfer, C.J., Corley, R.P., Stallings, M.C., Crowley, T.J.,
Hewitt, J.K., 2009. Developmental epidemiology of drug use and abuse in
adolescence and young adulthood: evidence of generalized risk. Drug Alcohol
Depen. 102 (1–3), 78–87.
Perrin, J.S., Hervé, P.Y., Leonard, G., Perron, M., Pike, G.B., Pitiot, A., Richer, L.,
Veillette, S., Pausova, Z., Paus, T., 2008. Growth of white matter in the
adolescent brain: role of testosterone and androgen receptor. J. Neurosci. 28
(38), 9519–9524.
Perrin, J.S., Leonard, G., Perron, M., Pike, G.B., Pitiot, A., Richer, L., Veillette, S.,
Pausova, Z., Paus, T., 2009. Sex differences in the growth of white matter during
adolescence. Neuroimage 45 (4), 1055–1066.
Reppucci, N.D., 1999. Adolescent development and juvenile justice. Am. J. Commun.
Psychol. 27 (3), 307–326.
Riggs, N.R., Chou, C.P., Li, C., Pentz, M.A., 2007. Adolescent to emerging adulthood
smoking trajectories: when do smoking trajectories diverge, and do they
predict early adult nicotine dependence? Nicotine Tob. Res. 9 (11),
1147–1154.
Ritvo, S., 1971. Late adolescence—developmental and clinical considerations.
Psychoanal. St. Child 26, 241–263.
Schmithorst, V.J., Wilke, M., Dardzinski, B.J., Holland, S.K., 2005. Cognitive functions
correlate with white matter architecture in a normal pediatric population: a
diffusion tensor MRI study. Hum. Brain Mapp. 26 (2), 139–147.
Schmithorst, V.J., Holland, S.K., Dardzinski, B.J., 2008. Developmental differences in
white matter architecture between boys and girls. Hum. Brain Mapp. 29 (6),
696–710.
J. Dayan et al. / Journal of Physiology - Paris 104 (2010) 279–286 285
Segal, H., 1957. Notes on symbol formation. Int. J. Psychoanal. 38, 391–397.
Shaw, P., Lerch, J., Greenstein, D., Sharp, W., Clasen, L., Evans, A., Giedd, J.,
Castellanos, F.X., Rapoport, J., 2006. Longitudinal mapping of cortical thickness
and clinical outcome in children and adolescents with attention-deficit/
hyperactivity disorder. Arch. Gen. Psychiat. 63 (5), 540–549.
Silveri, M.M., Tzilos, G.K., Pimentel, P.J., Yurgelun-Todd, D.A., 2006. Trajectories of
adolescent emotional and cognitive development: effects of sex and risk for
drug use. Ann. NY Acad. Sci. 1021, 363–370.
Sowell, E.R., Delis, D., Stiles, J., Jernigan, T.L., 2001a. Improved memory functioning
and frontal lobe maturation between childhood and adolescence: a structural
MRI study. J. Int. Neuropsychol. Soc. 7, 312–322.
Sowell, E.R., Thompson, P.M., Tessner, K.D., Toga, A.W., 2001b. Mapping continued
brain growth and gray matter density reduction in dorsal frontal cortex: inverse
relationships during postadolescent brain maturation. J. Neurosci. 21 (22),
8819–8829.
Spear, L.P., 2000. The adolescent brain and age-related behavioral manifestations.
Neurosci. Biobehav. Rev. 24, 417–463.
Spear, L.P., 2002. The adolescent brain and the college drinker: biological basis of
the propensity to use and misuse alcohol. J. Stud. Alcohol (Suppl. 14), 71–81.
Steinberg, L., 2004. Risk-taking in adolescence: what changes, and why? Ann. NY
Acad. Sci. 1021, 51–58.
Steinberg, L., 2008. A social neuroscience perspective on adolescent risk-taking.
Dev. Rev. 28, 78–106.
Steinberg, L., 2010. A dual systems model of adolescent risk-taking. Dev. Psychobiol.
52 (3), 216–224.
Steinberg, L., Cauffman, E., 1996. Maturity of judgment in adolescence: psychosocial
factors in adolescent decision making. Law Hum. Behav. 20, 249–272.
Steinberg, L., Silverberg, S.B., 1986. The vicissitudes of autonomy in early
adolescence. Child Dev. 57, 841–851.
Stevens, M.C., Kiehl, K.A., Pearlson, G.D., Calhoun, V.D., 2007. Functional neural
networks underlying response inhibition in adolescents and adults. Behav.
Brain Res. 181 (1), 12–22.
Stuss, D.T., Alexander, M.P., 2007. Is there a dysexecutive syndrome? Philos. Trans.
Roy. Soc. London B Biol. Sci. 362 (1481), 901–915 (review).
Tamm, L., Menon, V., Reiss, A.L., 2002. Maturation of brain function associated with
response inhibition. J. Am. Acad. Child Adolescence Psychiat. 41 (10), 1231–
1238.
Tamnes, C.K., Ostby, Y., Walhovd, K.B., Westlye, L.T., Due-Tønnessen, P., Fjell, A.M.,
2010. Intellectual abilities and white matter microstructure in development: a
diffusion tensor imaging study. Hum. Brain Mapp..
Van De Ven, M.O., Greenwood, P.A., Engels, R.C., Olsson, C.A., Patton, G.C., 2010.
Patterns of adolescent smoking and later nicotine dependence in young adults:
a 10-year prospective study. Public Health 124 (2), 65–67 (Epub 2010).
Wagner, F.A., Anthony, J.C., 2002. From first drug use to drug dependence:
developmental periods of risk for dependence upon marijuana, cocaine, and
alcohol. Neuropsychopharmacology 26 (4), 479–488.
Wahlstrom, D., Collins, P., White, T., Luciana, M., 2010. Developmental changes in
dopamine neurotransmission in adolescence: behavioral implications and
issues in assessment. Brain Cogn. 72 (1), 146–159.
Wechsler, H., Kuo, M., 2000. College students define binge drinking and estimate its
prevalence: results of a national survey. J. Am. Coll. Health 49 (2), 57–64.
White, T., Su, S., Schmidt, M., Kao, C.Y., Sapiro, G., 2010. The development of
gyrification in childhood and adolescence. Brain Cogn. 72 (1), 36–45 (Epub 2009
November 25 review).
Winnicott, D.W., 1965. The maturational processes and the facilitating
environment: studies in the theory of emotional development. Int. Psycho-
anal. Library 64, 1–276.
Winters, K.C., Stinchfield, R.D., Lee, S., Latimer, W.W., 2008. Interplay of
psychosocial factors and the long-term course of adolescents with a
substance use disorder. Subst. Abus. 29 (2), 107–119.
Wood, J.N., Romero, S.G., Knutson, K.M., Grafman, J., 2005. Representation of
attitudinal knowledge: role of prefrontal cortex, amygdala and
parahippocampal gyrus. Neuropsychologia 43 (2), 249–259.
Zinberg, N., 1975. Addiction and ego function. Psychoanal. Study Child 30, 567–588.
286 J. Dayan et al. / Journal of Physiology - Paris 104 (2010) 279–286
