Emotional and cognitive changes during adolescence

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Emotional and cognitive changes during adolescence
Deborah Yurgelun-Todd1,2
Adolescence is a critical period for maturation of
neurobiological processes that underlie higher cognitive
functions and social and emotional behavior. Recent studies
have applied new advances in magnetic resonance imaging to
increase understanding of the neurobiological changes that
occur during the transition from childhood to early adulthood.
Structural imaging data indicate progressive and regressive
changes in the relative volumes of specific brain regions,
although total brain volume is not significantly altered. The
prefrontal cortex matures later than other regions and its
development is paralleled by increased abilities in abstract
reasoning, attentional shifting, response inhibition and
processing speed. Changes in emotional capacity, including
improvements in affective modulation and discrimination of
emotional cues, are also seen during adolescence. Functional
imaging studies using cognitive and affective challenges have
shown that frontal cortical networks undergo developmental
changes in processing. In summary, brain regions that underlie
attention, reward evaluation, affective discrimination, response
inhibition and goal-directed behavior undergo structural and
functional re-organization throughout late childhood and early
adulthood. Evidence from recent imaging studies supports a
model by which the frontal cortex adopts an increasingly
regulatory role. These neurobiological changes are believed to
contribute, in part, to the range in cognitive and affective
behavior seen during adolescence.
Addresses
1 Brain Imaging Center, McLean Hospital, 115 Mill Street, Belmont, MA
02478, USA
2 Harvard Medical School, Boston, MA 02115, USA
Corresponding author: Yurgelun-Todd, Deborah
(ytodd@mclean.harvard.edu)
Current Opinion in Neurobiology 2007, 17:251–257
This review comes from a themed issue on
Cognitive neuroscience
Edited by Keiji Tanaka and Takeo Watanabe
Available online 26th March 2007
0959-4388/$ – see front matter
# 2007 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.conb.2007.03.009
Introduction
The adolescent years are characterized by the maturation
of emotional and cognitive abilities that provide the
developing individual with capacities needed for inde-
pendent functioning during adulthood [1]. During ado-
lescence, maturing individuals show increasing capacity
to attend selectively to information and to control their
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behavior [2,3]. This period of growth is marked by an
increased ability to read social and emotional cues and an
increased appreciation and dependence on interpersonal
relationships [4]. Until recently, relatively limited
research existed on the neurobiological changes that
accompany the cognitive and emotional changes that
occur during the transition between childhood and early
adulthood. Over the past decade, the application of
magnetic resonance imaging techniques has enabled
investigators to examine the specific areas and circuits
within the brain that are involved in the development of
emotional and cognitive abilities. This review will high-
light the progress made in understanding brain matura-
tional changes that are thought to underlie adolescent
behavior.
Adolescence is a critical period for maturation of brain
processes that underlie higher cognitive functions and
social and emotional behavior [1]. During this develop-
mental stage, emotional responses have not yet consoli-
dated, and children in late childhood and adolescence
explore a variety of styles and methods of affective
expression. Significant improvements in cognitive proces-
sing speed and intellectual functioning are also evident
throughout late childhood and adolescence, with the most
dramatic improvements occurring in the development of
executive functions including abstract thought, organiz-
ation, decision making and planning, and response inhi-
bition [5–8]. Recent neuroimaging studies have provided
evidence for changes in brain structure and function that
are thought to parallel improvements in cognitive abilities
and emotional processing.
Magnetic resonance scanning techniques
It has long been recognized that adolescent behavior is
marked by intense affective expression, impulsive
responses and gains in intellectual abilities that seem
not to be integrated into life choices. Neurobiological
studies, including research that measured cerebral meta-
bolic changes and rates of glucose utilization during
cortical development, have indicated that the cerebral
cortex undergoes a dynamic course of metabolic matu-
ration that persists until late adolescence [9]. However,
over the past decade magnetic resonance imaging (MRI)
methods, including structural MRI and functional MRI
(fMRI), have become important modalities for research
on brain development as they have been able to provide a
more detailed picture of how the brain changes. The
application of these methods to the study of children and
adolescents provides an extraordinary opportunity to
advance our understanding of the neurobiological
changes and functional abilities associated with brain
Current Opinion in Neurobiology 2007, 17:251–257
252 Cognitive neuroscience
maturation. Specifically, MRI provides higher spatial
resolution, superior contrast and soft-tissue imaging capa-
bility, improved fine gray–white matter distinctions and
greater differentiation of white matter changes when
compared with other techniques [10]. Because it uses
no ionizing radiation, MRI methods are well suited for
repeated studies of subjects and are safe to use in children
and adolescents. Additionally, MRI techniques give
investigators the flexibility of imaging in multiple planes
without having to reposition a subject physically. MRI
methods have therefore been used to verify and expand
initial findings from other neuroimaging investigations
that involved exposure to radiation.
Application of fMRI in combination with cognitive and
emotional challenge paradigms provides a safe and effec-
tive means to observe region-specific changes in the
brain. Because fMRI images are characterized by both
high spatial and rapid temporal resolution [11], two
notable advantages of this method are the precise func-
tional localization due to increased image quality and the
minimization of error due to interindividual anatomic
variability. Additionally, the noninvasive nature of fMRI
enables the acquisition of multiple sets of scans on the
same individual, providing a notable advantage for longi-
tudinal studies. Intrasubject averaging of data can also be
used to increase the signal-to-noise ratio and improve test
sensitivity. The increased temporal resolution in fMRI
compared with other neuroimaging modalities such as
positron emission tomography (PET) or single-photon
emission computed tomography (SPECT) suggests that
fMRI is more likely to identify alterations in cerebral
hemodynamics associated with thought processing or
mood changes.
Structural brain organization
Clarification of how behavior and cognition develop
requires focus on the relationship between maturational
Figure 1
Axial images illustrating placement of 11 cm3 regions of interest (green) in th
splenium on the (a) echoplanar image, (b) fractional anisotropy map and (c)
Reproduced from [21�].
Current Opinion in Neurobiology 2007, 17:251–257
changes in the structural organization of the developing
brain and associated changes in functioning. Although
little increase in brain size occurs after age 5 years [12,13],
throughout late childhood and adolescence the brain
continues to undergo subtle remodeling that involves
simultaneous progressive and regressive maturational
changes.
Brain development during adolescence typically demon-
strates significant decreases in cortical gray matter and
increases in white matter [14–18]. Giedd et al. [15]
reported that the increase in whitematter occurs linearly
during development, whereas gray matter increases
during pre-adolescence, peaks early in the frontal cortex
during adolescence, but then decreases during post-ado-
lescence. Likewise, Sowell et al. [19] reported that the
maturational changes observed in those aged 12–16 years
and 23–30 years were larger in dorsal, medial and lateral
regions of the frontal lobes than in the parietal and
occipital lobes. It has been well established that increases
in white matter reflect, in part, increased myelination,
which might be associated with age-related improve-
ments in cognitive processing [18]. Changes in white
matter microstructure have also been studied using a
newer magnetic resonance technique, diffusion tensor
imaging (DTI). Imaging data obtained using DTI
methods have demonstrated that anisotropy — a measure
that reflects myelin-related restriction of water diffusion
across axons — in frontal white matter was significantly
lower in children than in adults, suggesting less myelina-
tion in children [20].
One recent study examined the association between
white matter organization, as measured by DTI, and
impulse control in both boys and girls (Figure 1,
Table 1) [21�]. This investigation found that DTI values
correlated most strongly with self-report measures of
impulse control in male subjects whereas they correlated
e genu, forward-projecting arms of the genu (left and right) and
trace map of the diffusion tensor in an adolescent subject.
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Emotional and cognitive changes during adolescence Yurgelun-Todd 253
Table 1
Correlations between fractional anisotropy, trace, impulse control and Stroop-derived interferencea
Impulse control Derived interference
Females Males Females Males
Fractional anisotropy
Genu - - r = –0.743, P < 0.005 -
Left anterior - - r = –0.748, P < 0.005 -
Right anterior - r = –0.897, P < 0.005 - -
Splenium r = –0.596, P = 0.05 - - -
Trace
Genu - - r = 0.831, P < 0.001 -
Left anterior - - - -
Right anterior - - - -
Splenium - - r = 0.486, P < 0.05b
a Dashes indicate that there was no significant correlation. Significant relationships were observed between white matter integrity (fractional
anisotropy), with boys showing a stronger relationship with self-report of impulse control (a behavioral measure) and girls showing a stronger
relationship with the ability to inhibit an incorrect answer (a cognitive measure). This study underscores the role of white matter in impulse control, and
corroborates emerging evidence for sex differences in the developing brain. Using data from [21�].
b r and P values are for females and males grouped together.
most strongly with cognitive measures of inhibitory con-
trol in female subjects. These findings support a relation-
ship between changes in white matter microstructure and
impulse control during development.
As already noted, structural volumetric neuroimaging
studies suggest that, although total brain volume is rela-
tively established by early school-age years [13], remo-
deling of gray and white matter occurs throughout
adolescence and into early adulthood [12]. In addition
to reporting remodeling changes, recent structural volu-
metric studies have found that the dorsolateral prefrontal
cortex does not reach its full volume until the early
twenties [22], a finding of particular significance given
that many complex cognitive processes continue to
develop even into the early adult years [23].
The human prefrontal cortex mediates the highest cog-
nitive capacities, including reasoning, planning and beha-
vioral control [24]. This relatively large and complex
associative brain region has been shown to develop along
with other higher-order association regions as children
mature from adolescence into adulthood [24–26]. Struc-
tural neuroimaging studies using growth mapping tech-
niques suggest that the prefrontal cortex matures more
slowly than other regions of the brain [25,27] and that its
development parallels the improvements in cognitive
control and behavioral inhibition that emerge during
the adolescent transition into adulthood [27]. To date,
only a limited number of studies have correlated age-
related changes in brain tissue volume with behavioral
indices. One study of children and adolescents found that
greater total cerebral volume, and cortical gray matter
volume in particular, was associated with higher scores on
a standard measure of intellectual ability [13]. Frontal
lobe maturation, particularly thinning of cortical gray
matter, has been associated with better performance on
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verbal memory tests in children aged 7–16 years [28] and
the volume of the prefrontal cortex in healthy adolescents
has been associated with greater ability to inhibit beha-
vioral responses [29]. Rather than correlate structural
brain alterations during adolescence with cognitive and
emotional behavioral measures, many investigators have
applied functional neuroimaging techniques to examine
developmental changes.
Functional magnetic resonance imaging
Studies comparing adult and adolescent cortical function
indicate that adolescents process information differently,
often enlisting different brain regions than adults [30–32].
Difficulty with executive cognitive functioning and beha-
vioral self-regulation, including difficulties with planning,
attention, foresight, abstract reasoning, judgment, self-
monitoring and motor control, have been found in adoles-
cents, and several fMRI studies have examined the func-
tional neuroanatomy underlying executive processing in
children, adolescents and adults. Results of studies that
examine age-related differences in brain activation
have not always been consistent. Several investigations
have reported similar patterns of prefrontal brain activity in
children and adults on tasks of working memory [33,34],
response inhibition [29,35] and verbal fluency [36]. By
contrast, several studies have underscored differences
between these age groups on similar tasks of executive
function, with children failing to recruit the same prefron-
tal brain areas as adult subjects [8,37–39].
Several methodological differences between studies
might have contributed to these conflicting findings,
including task performance mismatch between age
groups and the absence of an adult comparison group
in some investigations [33,34]. Notably, in the only study
that segregated performance from age-related prefrontal
brain activation, Schlaggar et al. [39] found that adults but
Current Opinion in Neurobiology 2007, 17:251–257
254 Cognitive neuroscience
not children significantly activated the dorsal prefrontal
cortex on a single-word processing task. Although other
age-group differences in prefrontal activation were also
found, these were related to accuracy of task performance
independently of age. The results of this study emphasize
the importance of separating age-group differences in
brain activation into those attributable to maturation
versus those secondary to accuracy of performance [39].
Levels of brain maturation and task performance might
also contribute to differences in the volume of prefrontal
Figure 2
Age-related changes in regional brain activation. (a) The regions of interest,
MRI. Within these regions of interest, several prefrontal cortex regions dem
level dependent (BOLD) activity in a group of adolescent children viewing p
relationship between the fMRI response (% signal change) to fearful faces at t
separately for each gender. The figure on the left shows the age-related incr
hemisphere for males (r = 0.51, P = 0.16) and females (r = 0.80, P = 0.009), a
frontal gyrus of the right hemisphere for males (r = 0.89, P = 0.007) and femal
not significant within either amygdala. The left scatterplot displays the relation
and females (r = 0.11, P = 0.78) during fearful face trials. The right scatterplot
amygdala for males (r = 0.52, P = 0.23)and females (r = 0.71, P = 0.07) in re
Current Opinion in Neurobiology 2007, 17:251–257
activation between age groups. In two studies that com-
pared children with adults, children were found to recruit
a greater area of the dorsolateral prefrontal cortex during a
working memory task [29], and more of the right inferior
frontal gyrus during a word generation task [36]. A sub-
sequent study that compared three age groups found that
adolescents produced a greater volume of activation in
the dorsolateral prefrontal cortex than did both younger
children and older adults during a response inhibition
task, which suggested a greater reliance on the frontal
executive network [35]. Studies that have quantified the
including the prefrontal cortex and amygdala, are shown traced on a T1
onstrated significant (P < 0.005) age-related increases in blood oxygen
hotographs of faces expressing fear. (b) The scatterplots show the
he maximally correlated voxel in the prefrontal cortex of each hemisphere
ease in fearful face responses within the superior frontal gyrus of the left
nd the right scatterplot shows the age-related increase in the middle
es (r = 0.90, P = 0.006). (c) Age-related correlations for fearful faces were
ship between age and left amygdala activity for males (r = 0.46, P = 0.22)
shows the correlation between age and BOLD signal intensity in the right
sponse to fearful faces. Reproduced from [49].
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Emotional and cognitive changes during adolescence Yurgelun-Todd 255
magnitude of prefrontal activation during tests of execu-
tive function have reported linear increases from child-
hood through adolescence and young adulthood in the
superior [40], middle [2,8,41] and inferior [8] portions of
prefrontal cortex. Klingberg et al. [40] report that the
positive correlation between increasing age and magni-
tude of activation persists after controlling for perform-
ance accuracy. However, it has also been reported that
children and young adolescents activate the right inferior
frontal gyrus more powerfully than adults do during word
generation [36]. Overall, studies of cognitive function
indicate that brain maturation and physiological responses
continue to change through late childhood and young
adulthood. Studies of executive functions in adolescent
subjects point to an increase in frontal activation with
improved performance.
During adolescence, social relationships take on a new
importance and the adolescent child becomes adept at
reading social and emotional cues, and modulating his or
her own affective responses [4]. It has been shown that
children have difficulty managing interference from com-
peting distractions and the level of difficulty seems to be
correlated with the immaturity of posterior and frontal
association cortices [42�]. As children mature, they show
an increased ability to attend to incoming information
and control their behavior in a goal-directed manner
[2,3,27,43]. This development seems to emerge in con-
junction with a progressive frontalization of functional
activity associated with inhibitory processing [8]. The
period of adolescence is a time of considerable physio-
logical change, as sex-specific pubertal hormones
bring about changes in physical stature, reproductive
organs and other secondary sexual characteristics [1].
Neuroendocrine changes during puberty also seem to
be associated with changes in brain organization and cog-
nitive function [44], and with cerebral metabolism [45].
Frontalization of inhibitory capacity is hypothesized to
provide a greater top-down modulation of activity within
more primitive subcortical and limbic emotion-processing
regions, such as the amygdala. Hariri and colleagues
[46,47] have demonstrated that increased prefrontal
activity is associated with significant modulation of amyg-
dala responses to affective stimuli, particularly with
regard to fearful and angry faces. It is possible that these
affective processing abilities emerge developmentally
because functional neuroimaging results have shown that
adults produce greater activity than do adolescents in the
orbitofrontal cortex when displaying focused attention
towards emotional stimuli [48]. Moreover, a recent fMRI
study analyzed the correlation between age and prefrontal
cortex activity in a sample of healthy adolescents as they
viewed fearful faces (Figure 2) [49]. Age was significantly
correlated with bilateral prefrontal activity for a sample of
females, but was significantly related only to right pre-
frontal activity for the males. The results lend further
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support to the hypothesis that emotional processing
capacity during adolescence is related to the progressive
acquisition of greater functional activity within the pre-
frontal cortex.
Conclusion
In summary, previous research has suggested that cogni-
tive development through the adolescent years is associ-
ated with progressively greater efficiency of executive
control capacities, and that this efficiency is paralleled
by increased activity within focal prefrontal regions
[8,43]. Furthermore, with increasing age, prefrontal
activity becomes more focal and specialized while irrele-
vant and diffuse activity in this region is reduced
[42�,43,50�]. Additional imaging evidence in the affective
domain suggests that the development of prefrontal modu-
lation over emotional processing continues to develop
throughout the adolescent years and into early adulthood.
The maturation of prefrontal networks plays a critical role
in the cognitive and emotional behaviors displayed by
adolescents.
Acknowledgements
Thank you to Alexandra McCaffrey for her assistance in the preparation of
this manuscript. This work was supported by grants from the National
Institute of Drug Abuse (NIDA) RO1 DA12483, the National Institute of
Mental Health (NIMH) R01 MH069840, and a grant from the Charles H
Hood Foundation (DYT).
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