DEVELOPMENTAL MEDICINE & CHILD NEUROLOGY INVITED REVIEW

Training the anxious brain: using fMRI-based neurofeedback to

change brain activity in adolescence
ANNALISA LIPP | KATHRIN COHEN KADOSH
School of Psychology, University of Surrey, Guildford, UK.
Correspondence to Kathrin Cohen Kadosh, School of Psychology, University of Surrey, Guildford GU2 7XH, UK. E-mail: [email protected]

Anxiety disorders are a leading cause of morbidity and entail a lot of costs. Adolescence is
PUBLICATION DATA characterized by social fears and poor emotion regulation abilities which together increase
Accepted for publication 20th May 2020. the likelihood of the emergence of anxiety disorders. This emotion dysregulation is poten-
Published online 7th July 2020. tially caused by the emotion regulating brain areas, such as the prefrontal cortex and tempo-
ral cortex, that are still undergoing developmental changes throughout late adolescence.
ABBREVIATION Recently, new approaches have used functional magnetic resonance imaging-based neuro-
PFC Prefrontal cortex feedback to help participants gain control over emotion regulation brain networks by receiv-
ing real-time feedback on their brain activity and to use effective emotion regulation abilities.
In this review, we provide an overview of the developmental changes in the brain and the
corresponding behavioural changes, and explore how these can be influenced during adoles-
cence using neurofeedback. We conclude that recent studies show promising results that chil-
dren and adolescents can self-regulate emotion regulation brain networks thereby supporting
the development of effective emotion regulation abilities.

Anxiety disorders are a leading cause of morbidity in the train children and adolescents in the self-regulation of key
world.1 In the UK alone, over 8 million people (18.17% of emotion regulation brain networks, with the aim of sup-
the population) suffer from an anxiety disorder annually, porting the development of effective emotion regulation
generating annual costs of over £10 billion.2 Among the abilities and helping children and adolescents with anxiety.
many anxiety disorders (which include generalized anxiety
disorder, separation anxiety, panic disorder, obsessive–com- ANXIETY DISORDERS DURING DEVELOPMENT
pulsive disorder), social anxiety disorder is one of the most Fear is a brief and automatic response towards a specific
prevalent anxiety disorders,3 which is characterized by a stimulus (e.g. spiders) that causes physiological reactions
persistent fear and avoidance of social situations. As social such as heightened heart rate and vigilance. The key brain
interactions are integral to daily life, social anxiety disor- region of fear is the amygdala which brings sensory infor-
der, as well as subclinical social fears and worries, are espe- mation into context with the input coming from the corti-
cially impairing,4 and influence short- and long-term cal and subcortical regions.7 According to Pavlovian fear
functioning in educational achievements, social relation- conditioning, when an aversive unconditional stimulus is
ships, and mental health, increasing risks for depression, constantly paired with a previously non-fearful stimulus,
suicidal behaviour, and substance abuse.5 Cognitive-be- the non-fearful stimulus will after some time become a
havioural therapy is a common treatment for anxiety.6 fearful conditional stimulus. Likewise, fear can be
Cognitive-behavioural therapy teaches the patient to recog- unlearned by presenting the conditional stimulus multiple
nize anxious feelings, to realize which situations are caus- times without the aversive unconditional stimulus, which is
ing anxiety and to develop proper coping mechanisms.6 In called fear extinction.8 Fear is the base of anxiety disorders
most cases, between 10 and 20 sessions of cognitive-be- and is often learned early in life.
havioural therapy are sufficient;6 however in some cases, Emotion regulation refers to a person modifying his/her
pharmacological treatment such as selective serotonin emotional responses, a change which can either happen
reuptake inhibitor might be required.6 However, it has also automatically or by using conscious strategies. Fully func-
been shown that these established treatment approaches tional emotion regulation includes identifying the emo-
are very time-consuming and not always effective,6 and tional valence, recognizing that emotion regulation is
therefore do not work for all patients. In this paper, we necessary, and choosing an appropriate strategy.9 It has
will highlight the potential of a new treatment technique, been shown that emotion regulation strategies undergo sig-
called real-time functional magnetic resonance imaging nificant changes throughout development, both qualita-
(fMRI)-based neurofeedback. Neurofeedback is a novel tively (i.e. with regards to which strategy is used
intervention technique that can be used to investigate and predominantly) and quantitatively (i.e. how often a strategy

© 2020 The Authors. Developmental Medicine & Child Neurology published by John Wiley & Sons Ltd on behalf of Mac Keith Press DOI: 10.1111/dmcn.14611 1239
This is an open access article under the terms of the Creative Commons Attribution License, which permits use,
distribution and reproduction in any medium, provided the original work is properly cited.
 14698749, 2020, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/dmcn.14611 by Universitaet De Montreal, Wiley Online Library on [08/06/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
is employed). For example, a cross-sectional study by Zim- What this paper adds:
mermann and Iwanski10 of participants between the ages of • Functional magnetic resonance imaging-based neurofeedback can be used
11 and 50 years used a self-report questionnaire (Negative for brain self-regulation in development.
Emotion Regulation Inventory) to investigate the partici- • The emotion regulation networks play a key role in treating social anxiety
pants’ emotion regulation strategies and emotional experi- with neurofeedback.
ences. The results showed that the range of emotion
time. The maturation of the brain is expressed by grey
regulation strategies is very limited during adolescence in
matter loss and starts in puberty. A longitudinal study by
comparison to children (quantitative difference). In partic-
Gogtay et al.17 tested participants every 2 years for four
ular, social support seeking and adaptive emotion regula-
scans in total to pinpoint developmental changes in brain
tion decrease during this period, along with increased
function. The start of recruitment was at around the age of
suppression of emotions in fear situations, and dysregula-
10 years. The results revealed an increase in grey matter
tion of emotions in anger situation. These maladaptive
during childhood and a start of reduction in adolescence.17
strategies can lead to emotional instability and higher neu-
In general, the grey matter loss begins in the back of the
roticism,10 and further research has shown that adolescents
brain and spreads towards the front. The last regions to
use maladaptive emotion regulation strategies (qualitative
fully develop at the end of adolescence are the temporal
difference), such as self-blame and rumination, and under-
cortex and dorsolateral prefrontal cortex (PFC).17 This dif-
use reappraisal which, in turn, places them at higher risk
ferential timing pattern, with key regions that have been
for anxiety disorders.9 Children and adolescents are sensi-
linked to emotion regulation and anxiety disorders devel-
tive to social stress and bullying and this can have a great
oping late in adolescence, might therefore be a reason for
impact on mental health which can have long-lasting
the high emergence of anxiety disorders and poor discrimi-
effects into adulthood.11 A reason for the great impact of
nation between safety and threat cues in adolescence.13
social stress might be that fear extinction in adolescents is
Emotional behaviour in the brain is controlled by a net-
weakened and therefore they do not unlearn the fear and
work of regions that include the PFC and the amygdala,
suffer longer from it. When fear persists for a longer per-
which exhibit both structural and functional connec-
iod it can eventually develop into an anxiety disorder. In
tions.18,19 The functional negative coupling between the
accordance with that, it has been shown that social exclu-
two regions has been suggested to reflect top-down PFC
sion, a form of social stress, can increase the likelihood of
regulation of amygdala reactivity.20,21 Interestingly, this
developing social anxiety in adolescence.11 In a longitudi-
specific relationship is only established during adolescence,
nal study by Van Oort et al.,12 young people were studied
with younger children exhibiting more positive connectivity
from the age of 10 to 12 years until the age of 14 to 18
between the regions during emotion regulation tasks.14,22,23
years. Participants filled out a self-report questionnaire
This has been demonstrated in a cross-sectional study by
(Revised Child Anxiety and Depression Scale) that covers
Gee et al.14 in which they tested participants in their child-
the symptoms of several anxiety disorders, obsessive–com-
hood through early adulthood and compared their amygdala
pulsive disorder, and depression. The results revealed that
reactivity towards fearful faces and their functional connec-
there is a decrease in anxiety symptoms during the transi-
tivity between the amygdala and medial PFC in general. In
tion from childhood to adolescence, but they increase
this case, functional connectivity means the temporal corre-
again from middle to late adolescence. Furthermore, anxi-
lation between the time courses of the amygdala and the
ety levels were consistently higher in females.12
medial PFC. Accordingly, if activation in both brain regions
Why exactly the vulnerability for anxiety disorders is
increases, we will observe a positive connectivity pattern. If,
heightened in children and adolescents is still not clear,
however, activation patterns in both regions show opposite
but one contributing factor could be a malfunction in
trends, whereby one region increases activation and the
threat learning and threat extinction learning. A study by
other brain region decreases its response, then we speak of a
Lau et al.13 showed that adults have better discrimination
negative connectivity pattern. The findings indicated that
between safety and threat cues than adolescents. Accord-
the functional connectivity between amygdala and medial
ingly, adolescents might confuse safe situations with threat-
PFC is positive in early childhood, slightly negative towards
ening ones, and therefore are anxious more often which
adolescence, and highly negative in early adulthood. Fur-
facilitates the likelihood of an anxiety disorder. This lack
thermore, amygdala reactivity decreased with age.14 The
of discrimination may be due to ongoing maturation in the
positive functional connectivity between amygdala and med-
underlying brain networks and an age-specific change in
ial PFC could be caused by poor regulation of the amygdala
brain network connectivity.14–16
by the PFC and therefore the amygdala is overreactive
which elicits emotional instability.
BRAIN DEVELOPMENT DURING CHILDHOOD AND It has also been shown that the observed developmental
ADOLESCENCE change in the connectivity pattern goes along with the pro-
The heightened vulnerability for anxiety disorders and longed acquisition of effective emotional and attention
emotion dysregulation during childhood and adolescence control strategies.24–26 In our previous research, we showed
might be explained by the brain development during this that the neural networks that process emotional face

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expressions fine-tune continuously throughout childhood During neurofeedback training, participants learn to gain
and adolescence,27–29 and that individual differences in trait control over specific brain areas by receiving feedback on
anxiety affect how adolescents process emotional faces, and their brain activity.33 Participants are either encouraged to
learn about threat and safety signals.30,31 find a strategy to influence their brain activity on their
A study by McRae et al.32 attempted to connect brain own by trial and error or they get an instruction by the
activity with cognitive reappraisal ability in children, ado- experimenter beforehand (e.g. ‘Think of happy things’).33
lescents, and young adults. The participants viewed nega- In anxiety disorders where emotion regulation seems to be
tive or neutral pictures and had to either look at the dysfunctional, the PFC and amygdala can be targeted for
pictures or reappraise their emotions in case of a negative neurofeedback training. During the training, brain activity
picture. The results revealed that there was no difference is recorded by an fMRI or an electroencephalogram and
in emotional reactivity when negative pictures were the participant receives visual or audible feedback about
viewed, but that the ability to reappraise the negative his/her brain activity in a real-time setting. The participant
affect significantly increased with age. Moreover, the learns to influence his/her brain activity either by trial and
improved cognitive reappraisal with age was associated error or is taught certain strategies beforehand.33 (See
with higher activation of the ventrolateral PFC.32 Paret et al.38 for more information on the different neuro-
feedback research designs and approaches.) After some
USING NEUROFEEDBACK TO PINPOINT PLASTICITY training, the participant becomes aware of the activity
IN THE DEVELOPING EMOTION REGULATION BRAIN within the target areas and can change the activity con-
NETWORKS sciously.40 Ideally, successful self-regulation of brain activ-
Kohn et al.18 have proposed a three stage-model of emo- ity will turn into behavioural changes.41 As anxiety
tion regulation in the brain. The first stage involves rec- disorders are mostly associated with disrupted functional
ognizing and evaluating a stimulus. The amygdala and connectivity between the PFC and amygdala and not their
ventral striatum are responsible for generating the emo- separate activity levels, neurofeedback with real-time fMRI
tion and passing on the information to the ventrolateral is advantageous, because of its high spatial resolution.33
PFC, where the emotion is consciously perceived and Several studies have demonstrated that neurofeedback
evaluated. When there is a need for emotion regulation, training can be an effective method for reducing anxiety
the ventrolateral PFC will send a signal to the dorsolat- symptoms.42–46 For example, in Scheinost et al.,43 patients
eral PFC in the second stage. Finally, premotor areas, with contamination anxiety performed neurofeedback
angular gyrus, and superior temporal gyrus are stimulated training. They learned to self-regulate their orbitofrontal
to execute the regulation. This final stage may elicit activ- cortex which led to lower limbic circuitry connectivity and
ity in the ventral striatum and amygdala which in turn higher dorsolateral PFC connectivity. At the same time,
causes the generation of a new emotion.18 One possibility contamination anxiety symptoms decreased, and the change
to influence this process of emotion regulation is by neu- persisted for several days. Another study by Zilverstand
rofeedback training. Neurofeedback utilizes the latest et al.45 achieved an improvement of symptoms in spider
developments of real-time data processing and pattern phobia by training participants to down-regulate their
analysis to train participants in the self-modulation of insula activity via neurofeedback. Moreover, the study
neural networks.33 One example of self-modulation of proved that neurofeedback training was more effective than
neural networks can be seen in Figure 1. The strength of cognitive appraisal without giving feedback on brain activ-
this technique lies in its high spatial resolution (including ity. Further, Kimmig et al.42 conducted a near-infrared
the ability to probe deep subcortical structures and whole- spectroscopy neurofeedback study in patients with social
brain coverage), as well as the extraction of information anxiety disorder. Throughout 15 training sessions, the par-
from distributed activation patterns,34 and the mapping of ticipants learned to voluntarily regulate their dorsolateral
functionally connected networks.35 This is particularly PFC either up or down over a course of 6 to 8 weeks.
critical in development when functional brain networks After the training, the participants showed lower symptom
change significantly27 and the fine-tuning patterns for severity. Recently, a study by Zhao et al.46 examined a sub-
these functional networks differ for typically and atypically clinical sample with high levels of anxiety and conducted
developing populations.36–38 If implemented successfully, three sessions of neurofeedback training. During the train-
the neurofeedback approach holds much promise for ing, they received feedback on their functional connectivity
brain-based intervention approaches that aim to influence between the ventrolateral PFC and amygdala, while in the
and shape the emerging networks in the developing brain. sham condition the participants got feedback on their func-
That is, it allows us to target not only cortical and sub- tional connectivity between the amygdala and motor cor-
cortical task-relevant regions, but it also offers the neces- tex. Unlike the sham group, the active group increased the
sary flexibility to accommodate the frequent changes in functional connectivity and their anxiety levels significantly
brain network configurations that are typical for emerging decreased.
networks.38 Hereby, it is important to choose an appro- With regards to the developing brain, our research
priate experimental design and intervention schedule for group was the first to show that children and adolescents
participants during their development.38,39 can be taught to regulate activity in emotion regulation

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(a) Left insula MNI ([x, y, z]: –39, 14, 7)

Pre Pre
SMA MCC SMA IPL
IPL MCC
MFG MFG

lINS rINS lINS rINS

lAMY lAMY

Regulate Rest

(b) Right insula MNI ([x, y, z]: 36, 15, 3)

Pre Pre
SMA MCC SMA MCC IPL
IPL

MFG MFG

lINS rINS lINS rINS

lAMY lAMY

Regulate Rest

Figure 1: Results from a previous neurofeedback study by Cohen Kadosh et al.,47 where children and adolescents aged 7–17 years were training to
upregulate activity in the anterior insula, a key emotion regulation region using positive imagery. Granger causality analysis was then used to assess
the effective connectivity in the emotion regulation network as a function of percent signal change in the bilateral insula during the up-regulation con-
dition (a) and the down-regulation condition (b). All arrows indicate significant correlations, whereas the red arrows indicate significant differences in
amygdala–insula regulation. Reprinted from Cohen Kadosh et al.47 with permission from Elsevier. lAMY, left amygdala; lINS, left insula; rINS, right insula;
IPL, left inferior parietal lobule; MCC, mid cingulate cortex; MFG, middle frontal gyrus; MNI, Montreal Neurological Institute template; Pre, precentral
sulcus; SMA, supplementary motor area.

regions.47 One of the key findings was that the self-regula- directly modulate emotion regulation network connectivity
tion effects were not limited to the neurofeedback target in females aged 14 to 17 years.48 Specifically, we were able
region but had also a differential effect on the overall emo- to successfully train participants to modulate the functional
tion regulation brain network. This showcases the suitabil- coupling of the PFC and the amygdala towards a more
ity of this approach to affect and modulate the underlying negative connectivity pattern, which resembles the connec-
networks in the developing brain. In a second study, we tivity pattern found in the mature brain48 and away from
then used functional connectivity-based neurofeedback to the positive connectivity patterns that predominates in

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younger children and anxious adults.21 We also found sev- relationship at the brain and behavioural level, and the
eral brain–behaviour correlations. For example, we found longevity of these effects across time and sex.38,39
that trait anxiety levels were positively correlated with ini-
tial functional connectivity, with lower trait anxiety levels CONCLUSION
predicting more negative functional connectivity. This Anxiety disorders are one of the most common mental dis-
result is in line with the finding that lower levels of PFC– orders and often emerge in late childhood or adoles-
amygdala functional connectivity can predict anxiety levels cence.49 They are associated with emotional dysregulation
in anxious participants. We further extended this finding that is most likely related to dysfunctional functional con-
by showing that baseline state anxiety levels were nega- nectivity between the PFC and amygdala.50 As key emo-
tively correlated with neurofeedback-related change (i.e. tion regulation brain regions such as the PFC develop
the lower the baseline state anxiety, the higher the neuro- continuously into late adolescence and early adulthood,
feedback-related change in functional connectivity this maturational change is also likely to be reflected in
throughout the training). This suggests that neurofeedback emotion regulation abilities. Here we have provided some
success could be increased if participants, and especially first evidence of how neurofeedback can be successfully
those with high levels of state anxiety, are relaxed and used to help children and adolescents to learn to self-regu-
comfortable during the intervention. Further studies are late key emotion regulation brain networks, and to support
now needed to pinpoint the specific characteristics of the the development of effective emotion regulation abilities.

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