Is Neurofeedback an Efficacious Treatment for ADHD? A Randomised Controlled Clinical Trial

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DOI: 10.1111/j.1469-7610.2008.02033.x · Source: PubMed
Abstract
For children with attention deficit/hyperactivity disorder (ADHD), a reduction of inattention, impulsivity and hyperactivity by neurofeedback (NF) has been reported in several studies. But so far, unspecific training effects have not been adequately controlled for and/or studies do not provide sufficient statistical power. To overcome these methodological shortcomings we evaluated the clinical efficacy of neurofeedback in children with ADHD in a multisite randomised controlled study using a computerised attention skills training as a control condition. 102 children with ADHD, aged 8 to 12 years, participated in the study. Children performed either 36 sessions of NF training or a computerised attention skills training within two blocks of about four weeks each (randomised group assignment). The combined NF treatment consisted of one block of theta/beta training and one block of slow cortical potential (SCP) training. Pre-training, intermediate and post-training assessment encompassed several behaviour rating scales (e.g., the German ADHD rating scale, FBB-HKS) completed by parents and teachers. Evaluation ('placebo') scales were applied to control for parental expectations and satisfaction with the treatment. For parent and teacher ratings, improvements in the NF group were superior to those of the control group. For the parent-rated FBB-HKS total score (primary outcome measure), the effect size was .60. Comparable effects were obtained for the two NF protocols (theta/beta training, SCP training). Parental attitude towards the treatment did not differ between NF and control group. Superiority of the combined NF training indicates clinical efficacy of NF in children with ADHD. Future studies should further address the specificity of effects and how to optimise the benefit of NF as treatment module for ADHD.
Is neurofeedback an efficacious treatment for
ADHD? A randomised controlled clinical trial
Holger Gevensleben,
1
Birgit Holl,
3
Bjo
¨
rn Albrecht,
1
Claudia Vogel,
2
Dieter Schlamp,
3
Oliver Kratz,
2
Petra Studer,
2
Aribert Rothenberger,
1
Gunther H. Moll,
2
and Hartmut Heinrich
2,3
1
Child & Adolescent Psychiatry, University of Go
¨
ttingen, Germany;
2
Child & Adolescent Psychiatry,
University of Erlangen-Nu
¨
rnberg, Germany;
3
Heckscher-Klinikum, Mu
¨
nchen, Germany
Background: For children with attention deficit/hyperactivity disorder (ADHD), a reduction of inat-
tention, impulsivity and hyperactivity by neurofeedback (NF) has been reported in several studies. But
so far, unspecific training effects have not been adequately controlled for and/or studies do not provide
sufficient statistical power. To overcome these methodological shortcomings we evaluated the clinical
efficacy of neurofeedback in children with ADHD in a multisite randomised controlled study using a
computerised attention skills training as a control condition. Methods: 102 children with ADHD, aged
8 to 12 years, participated in the study. Children performed either 36 sessions of NF training or a
computerised attention skills training within two blocks of about four weeks each (randomised group
assignment). The combined NF treatment consisted of one block of theta/beta training and one block of
slow cortical potential (SCP) training. Pre-training, intermediate and post-training assessment
encompassed several behaviour rating scales (e.g., the German ADHD rating scale, FBB-HKS) com-
pleted by parents and teachers. Evaluation (‘placebo’) scales were applied to control for parental
expectations and satisfaction with the treatment. Results: For parent and teacher ratings, improve-
ments in the NF group were superior to those of the control group. For the parent-rated FBB-HKS total
score (primary outcome measure), the effect size was .60. Comparable effects were obtained for the two
NF protocols (theta/beta training, SCP training). Parental attitude towards the treatment did not differ
between NF and control group. Conclusions: Superiority of the combined NF training indicates clinical
efficacy of NF in children with ADHD. Future studies should further address the specificity of effects and
how to optimise the benefit of NF as treatment module for ADHD. Keywords: Neurofeedback, attention
deficit/hyperactivity disorder (ADHD), slow cortical potentials (SCPs), theta/beta training, randomised
controlled trial (RCT), EEG.
Attention deficit/hyperactivity disorder (ADHD)
is characterised by developmentally inappropriate
levels of inattention, impulsiveness and hyperactiv-
ity. It is one of the most common psychiatric disorders
in children and adolescents (prevalence: about 5%;
Rothenberger, Do
¨
pfner, Sergeant, & Steinhausen,
2004; Polaczyk, Silva de Lima, Horta, Biederman, &
Rohde, 2007). ADHD is often accompanied by
impaired social adjustment, academic problems and
high likelihood of psychiatric diagnosis leading to
lower adaptive functioning in major life activities in
adulthood (Gilberg et al., 2004). So far, medication
(methylphenidate) is the most effective treatment
though it has disadvantages and limitations, like a
considerable rate of non-responders, side-effects and
reservations against medication (Taylor et al., 2004;
Banaschewski et al., 2006). Even in responders, there
is still room for improvement.
European clinical guidelines for hyperkinetic dis-
order recommend a multimodal treatment, encom-
passing medication, cognitive behavioural and
family treatments (Taylor et al., 2004). However,
previous child-oriented cognitive-behavioural inter-
vention strategies have not always proven to be
sufficiently effective, especially in terms of general-
isation and long-term effects (Abikoff, 1991; Pelham,
Wheeler, & Chronis, 1998). Thus there remains a
need for effective treatment strategies in improving
attentional and self-management capabilities in
children with ADHD.
In the search for additional or alternative treat-
ment options for children with ADHD, NF emerged as
one of the most promising options (Heinrich,
Gevensleben, & Strehl, 2007). NF is a neurobehavi-
oural treatment aimed at acquiring self-control over
certain brain activity patterns and implementing
these skills in daily-life situations. Two training
protocols training of slow cortical potentials (SCPs)
and theta/beta training are typically used in chil-
dren with ADHD.
A training of slow cortical potentials
1
is related to
phasic regulation of cortical excitability. Surface-
negative SCPs (‘negativities’) and surface-positive
SCPs (‘positivities’) have to be generated over the
sensorimotor cortex. Negative SCPs reflect increased
Conflict of interest statement: No conflicts declared.
1
SCPs lasting from several hundred milliseconds to several
seconds are related to the level of excitability of underlying
cortical regions. They originate in the apical dendritic layers of
the neocortex (Birbaumer, Elbert, Canavan, & Rockstroh,
1990).
Journal of Child Psychology and Psychiatry **:* (2009), pp **–** doi:10.1111/j.1469-7610.2008.02033.x
2009 The Authors
Journal compilation 2009 Association for Child and Adolescent Mental Health.
Published by Blackwell Publishing, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden, MA 02148, USA
excitation and occur, e.g., during states of behav-
ioural or cognitive preparation. Positive SCPs are
thought to indicate reduction of cortical excitation of
the underlying neural networks and appear, e.g.,
during behavioural inhibition.
In theta/beta training the goal is to decrease
activity in the theta band (4–8 Hz) and to increase
activity in the beta band (13–20 Hz) of the electro-
encephalogram (EEG) which corresponds to an alert
and focused but relaxed state. Thus, this train-
ing paradigm addresses tonic aspects of cortical
arousal.
The rationale of applying these paradigms in
ADHD is based on findings from EEG and event-
related potentials (ERP) studies. For the contingent
negative variation (CNV; a typical SCP), reduced
amplitude was measured during cued continuous
performance tests (CPT) in children with ADHD (for
review see Banaschewski & Brandeis, 2007). This
finding may be seen in line with the dysfunctional
regulation/allocation of energetical resources model
of ADHD (Sergeant, Oosterlaan, & Van der Meere,
1999).
In the resting EEG, increased slow wave activity
(theta, 4–8 Hz) and/or reduced alpha (8–13 Hz) and
beta (13–30 Hz) activity, especially in central and
frontal regions, might be associated with ADHD,
probably reflecting under-arousal of the central
nervous system (for review see Barry, Clarke, &
Johnstone, 2003). However, empirical evidence is
contradictory and different findings might depend on
technical and motivational factors among others.
On the other hand, notwithstanding a (hypotheti-
cal neurophysiological) dysfunction, NF can be seen
simply as a tool for enhancing specific cognitive or
attentional states in certain situations, as it is
practised in peak performance applications in arts or
sports (Egner & Gruzelier, 2003; Landers et al.,
1991). In this respect, children with ADHD may
learn compensatory strategies in NF training,
underlining the necessity to support participants in
acquiring self-regulation abilities and implementing
them in critical life situations.
A series of studies provide evidence for positive
effects of NF treatment in children with ADHD. For
theta/beta training as well as for SCP training a
decrease of behavioural problems and improved
cognitive performance have been reported (Drechsler
et al., 2007; Fuchs, Birbaumer, Lutzenberger,
Gruzelier, & Kaiser, 2003; Heinrich, Gevensleben,
Freisleder, Moll, & Rothenberger 2004; Monastra,
Monastra, & George, 2002; Strehl et al., 2006).
However, the studies conducted thus far have
obvious shortcomings, such as small sample sizes,
lack of an adequate control group, no randomisa-
tion, mixed multiple intervention strategies or dis-
regard of long-term outcome. These shortcomings
preclude unambiguous interpretation or generalisa-
tion of the results (Heinrich et al., 2007; Loo &
Barkley, 2005).
In the present trial, the main aim was to control for
unspecific effects (e.g., the fact that training is an
attention-demanding task) and confounding vari-
ables (e.g., parental engagement). Therefore, we
chose a computerised attention skills training (AST)
as a control condition, with both trainings being
conceived as similarly as possible. Sample size was
calculated to be large enough to reach sufficient
statistical power to reveal at least moderate treat-
ment effects. Since theta/beta and SCP training are
thought to address different aspects of cortical reg-
ulation both being important for an optimal
attentive behaviour (Rockstroh, Elbert, Lutzenber-
ger, & Birbaumer, 1990; Heinrich et al., 2007) we
intended to integrate both protocols in the NF
training, also allowing us to compare the protocols at
the intra-individual level.
We hypothesised that improvements in the NF
group exceeded the training effects in the control
group with respect to all ADHD symptom domains.
We expected comparable ‘global’ effects for the two
NF training protocols but were also interested to
know whether a distinct pattern may occur at the
symptom level.
Methods and materials
Subjects
One hundred and two children with ADHD, aged 8 to
12 years (mean age: 9.6 ± 1.2 years), participated in an
NF training or an attention skills training (training
period: May 2005 to December 2007). Patients of the
outpatient departments of the participating clinics with
no urgent need for medication were informed about the
project and families who had heard about the study
from local professionals applied to take part. Subjects
were randomly assigned to one of the two study groups
(ratio NF:AST = 3:2). There were no pre-training differ-
ences between the NF and AST groups concerning
demographic, psychological and clinical variables (see
Tables 1 and 2).
All patients fulfilled DSM-IV criteria for ADHD
(American Psychiatric Association, 1994). Diagnoses
were based on a semi-structured clinical interview
(CASCAP-D; Do
¨
pfner, Berner, Flechtner, Lehmkuhl, &
Steinhausen 1999) and confirmed using the Diagnostic
Checklist for Hyperkinetic Disorders/ADHD (Do
¨
pfner &
Lehmkuhl, 2000) by a child and adolescent psychiatrist
or a clinical psychologist, supervised by a board-certi-
fied child and adolescent psychiatrist. Children with
comorbid disorders other than conduct disorder,
emotional disorders, tic disorder and dyslexia were
excluded from the study. All children lacked gross
neurological or other organic disorders. All children
were drug-free and without concurring psychotherapy
for at least 6 weeks before starting the training. Most of
the children (N=87, see Table 1) were drug-naı
¨
ve.
The study follows the CONSORT guidelines for
randomised trials (Boutron et al., 2008). It was
approved by the local ethics committees of the partici-
pating clinics and conducted according to the Helsinki
2 Holger Gevensleben et al.
2009 The Authors
Journal compilation 2009 Association for Child and Adolescent Mental Health.
declaration. Assent was obtained from the children and
written informed consent from their parents.
Design of the study
Both trainings consisted of two blocks of 18 sessions
(conducted as nine double sessions of about
2 · 50 minutes each, separated by a short break), with
two to three double sessions a week, adapted to the
families’ routine activities during their weekly schedule
(2.74 ± .62 double-sessions per week; no significant
differences between the groups). Thus, each block las-
ted for three to four weeks. Pre-training assessment
took place during the week prior to the course. Inter-
mediate and post-training assessment was done about
one week after the last session of the first and second
training blocks, respectively. The NF training consisted
of an SCP block and a theta/beta block (balanced
order).
Subjects were randomly assigned to the groups by
the administering psychologist. Children trained in
pairs but children from different treatment groups were
not paired together. Each centre prepared time slots for
Table 1 Demographic and clinical characteristics of the NF
group and the control group: at the pre-training level there
were no significant differences between the groups. Dropouts
(see text) are not included in the table
NF group
n=59
AST group
n=35
No. of patients treated
by centre (Erlangen/
Go
¨
ttingen/Mu
¨
nchen)
23/19/17 16/08/11
Age (years; month) 9;10 ± 1;3 9;4 ± 1;2
Sex (boys/girls) 51/8
(86.4%/13.6%)
26/9
(74.3%/25.7%)
IQ (HAWIK-III, Tewes
et al. 2000)
106.1 ± 13.2 104.5 ± 12.9
DSM-IV subtype
Combined type 39 (66.1%) 27 (77.1%)
Inattentive type 20 (33.9%) 8 (22.9%)
Drug-naive 54 (91.5%) 33 (97.1%)
Associated disorders
Conduct disorder 10 (16.9%) 7 (20.0%)
Emotional disorder 3 (5.1%) 3 (8.6%)
Tic disorder 3 (5.1%) 0 (.0%)
Dyslexia 12 (20.3%) 10 (28.6%)
Table 2 Parents and teachers behaviour ratings (mean values ± standard deviation)
Behaviour ratings
NF group (n=59) AST group (n=35)
Effect-size
(Cohen’s d)
t-test
(1-sided)Pre-training Change Pre-training Change
Parents
FBB-HKS
Total score 1.50 ± .45 ).39 ± .37 1.49 ± .50 ).14 ± .44 .60 p<.005
Inattention 1.97 ± .51 ).48 ± .47 1.83 ± .52 ).19 ± .55 .57 p<.005
Hyperactivity/ impulsivity 1.14 ± .66 ).31 ± .44 1.25 ± .68 ).12 ± .42 .45 p<.05
FBB-SSV
Oppositional behaviour 1.06 ± .66 ).25 ± .44 1.11 ± .66 ).07 ± .53 .38 p<.05
Delinquent and physical
aggression
.13 ± .13 ).02 ± .12 .15 ± .13 +.03 ± .15 .37 p<.05
SDQ
Total score 16.0 ± 4.8 )2.29 ± 4.95 16.2 ± 4.9 ).03 ± 3.90 .51 p<.01
Emotional symptoms 3.54 ± 2.02 ).37 ± 1.89 3.50 ± 2.60 +.03 ± 2.04
Conduct problems 2.74 ± 1.80 ).39 ± 1.65 3.03 ± 1.68 ).09 ± 1.79
Hyperactivity 6.93 ± 1.81 )1.29 ± 1.84 7.00 ± 1.76 ).24 ± 1.62 .60 p<.005
Peer problems 2.79 ± 2.23 ).24 ± 1.77 2.65 ± 2.02 +.27 ± 1.59 .30 p<.1
Prosocial behaviour 7.32 ± 2.28 +.06 ± 1.51 7.32 ± 2.00 ).18 ± 1.81
Problem situations in
family (HSQ-D)
40.6 ± 24.5 )9.3 ± 20.1 30.2 ± 18.3 )5.0 ± 14.1
Homework (HPC-D) 35.9 ± 9.1 )5.2 ± 9.5 37.8 ± 16.9 )5.2 ± 8.8
Teachers
FBB-HKS
Total score 1.25 ± .59 ).29 ± .33 1.37 ± .66 )
.03 ± .47 .64 p<.01
Inattention 1.71 ± .62 ).35 ± .51 1.75 ± .59 ).06 ± .64 .50 p<.05
Hyperactivity/ impulsivity .87 ± .82 ).21 ± .42 1.90 ± .89 .01 ± .59 .40 p<.1
FBB-SSV
Oppositional behaviour .67 ± .76 ).13 ± .37 .74 ± .82 +.01 ± .45 .34
Delinquent and physical
aggression
.06 ± .11 ).01 ± .08 .09 ± .15 ).03 ± .09
SDQ
Total score 13.3 ± 6.1 )2.00 ± 4.30 15.2 ± 6.7 )1.35 ± 4.47
Emotional symptoms 2.00 ± 2.31 ).39 ± 2.17 2.78 ± 2.39 ).82 ± 2.10
Conduct problems 1.87 ± 1.99 ).36 ± 1.52 2.44 ± 2.31 ).24 ± 1.92
Hyperactivity 6.18 ± 2.27 )1.01 ± 1.57 7.11 ± 2.65 ).18 ± 1.88 .48 p<.05
Peer problems 3.21 ± 2.41 ).22 ± 1.84 2.89 ± 2.89 ).12 ± 2.03
Prosocial behaviour 5.79 ± 2.80 +.53 ± 2.25 5.61 ± 2.62 ).12 ± 1.73
Change = post-training minus pre-training values (negative change scores indicate improvement, except SDQ-Prosocial behaviour).
Effect sizes (Cohen’s d) .3 are reported. All t-tests and effect sizes refer to comparisons between the groups.
Neurofeedback training in children with ADHD
3
2009 The Authors
Journal compilation 2009 Association for Child and Adolescent Mental Health.
each treatment and the participants were allocated via
lots to these treatment slots.
Parental estimations were controlled via evaluation
scales (‘placebo scales’; questionnaires assessing
expectations, evaluation and satisfaction with the
treatment). Parents were explicitly not informed about
the treatment condition of their child and, as a rule, did
not enter the room during treatment.
Assuming a detectable effect size slightly above .5 for
the primary outcome measure
2
(German ADHD
rating scale, FBB-HKS total score; Do
¨
pfner &
Lehmkuhl, 2000) and a dropout rate of 5%, we calcu-
lated that we needed to include about 100 children to
reach a power of .8 (one-sided, .05-level test; ratio
NF:AST = 3:2).
Design of the training programs
Both training programs were designed as similarly as
possible concerning the setting and the demands
placed upon the participants. Treatment of both groups
entailed computer-game-like tasks that demanded
attention, development of strategies for focusing one’s
attention and practising of acquired strategies at home
and in school. Both treatments were introduced to the
parents and children as experimental, but promising
treatment modules for ADHD.
The children of both treatment groups completed
their trainings in pairs, with each child working at one
computer. About three tasks at the computer lasting
for about 25–30 minutes were accomplished in one
session.
The training programs were administered by the
same clinical psychologists with the support of a stu-
dent assistant who were instructed to take a neutral
attitude concerning the effects of the individual train-
ing programs. In both trainings, the therapists had to
introduce the next task, discuss problems with the
task and the use of strategies (‘What did you do to
succeed?’, ‘What was your strategy?’, ‘How did it
work?’, ‘Did you spend much effort?’, ‘Were you
focused or did something distract you?’, ‘How could
you deal with that?’). In addition, the trainers were
asked to motivate and praise the children. Thus, the
quality and quantity of interaction were comparable
for both trainings.
From the 8th session on, children of both groups had
to practise one of their strategies in a specific situation
for about 10 minutes each day in daily-life situations
(e.g., while reading a book, while playing football).
Children were instructed to identify situations in which
these strategies would be important, aimed at increas-
ing the children’s responsibility for attention control in
certain situations. Exercises were documented by
keeping a log and controlled at the beginning of the next
session. Homework was kept identical in quantity and
quality between the groups. Parents were instructed to
support the children with the transfer of the learned
strategies to everyday life. This parent counselling did
not exceed two hours.
Neurofeedback training
The neurofeedback system SAM (Self-regulation and
Attention Management), which was developed by our
study group, was used for neurofeedback training.
It contains several feedback animations to keep
the training diversified and appropriate for children.
During training, children sat in front of a monitor and
controlled a kind of computer game by modulating their
brain electrical activity. In the course of the SCP train-
ing the task was to find appropriate strategies to direct
a ball upwards (negativity trials) or downwards (posi-
tivity trials). In the theta/beta-protocol a bar on the left
of the screen (representing theta activity) had to be
reduced while simultaneously a bar on the right
(representing beta activity) had to be increased.
In each SCP training session approximately 120 trials
were performed. Negativity (50%) and positivity trials
(50%) were presented in random order. A trial lasted for
8 seconds (baseline period: 2 s, feedback period: 6 s).
Intertrial interval was set to 5 ± 1 s.
Trials of the theta/beta training lasted for 5 minutes
at the start of training and were extended to 10 minutes
as the training proceeded. Feedback was calculated
from Cz (reference: mastoids, bandwidth: 1–30 Hz for
theta/beta training and .01–30 Hz for SCP training,
respectively, sampling rate: 250 Hz). Baseline values
were determined at the beginning of each session
(3 minutes). An adjustment within a session was not
scheduled. Vertical eye movements, which were
recorded with electrodes above and below the left eye,
were corrected online using slightly different regres-
sion-based algorithms for theta/beta training (Sem-
litsch, Anderer, Schuster, & Presslich, 1986) and SCP
training (Kotchoubey, Schleichert, Lutzenberger, &
Birbaumer, 1997). For segments containing artefacts
exceeding ±100 lV in the EEG channel and ±200 lVin
the EOG channel, no feedback was calculated.
Transfer trials, i.e., trials without contingent feed-
back, were also conducted (about 40% at the beginning
of a training block and about 60% at the end of a
training block).
The children of the NF group were required to prac-
tise their focused state (which was practised in the
sessions) at home, in different situations (one situation
per day, e.g., ‘try to be very focused while reading’, ‘try
to stay focused on the ball while playing football this
afternoon’).
Attention skills training
The attention skills training was based on ‘Skillies’
(Auer-Verlag, Donauwo
¨
rth, Germany), an award-win-
ning German learning software, which primarily exer-
cises visual and auditory perception, vigilance,
sustained attention, and reactivity. In ‘Skillies’, the
children had to sail to several islands. On each island, a
defined task each requiring different attention-based
skills has to be solved; e.g., on an island named
‘Coloured Reef’, fish of different colours swim from one
side of the screen to the other and back. All fish must be
the same colour. The colour can be modified by clicking
on a fish. With every change of direction the fish change
their colour (fixed order). Thus, the main aim of this
task is to improve vigilance and reactivity.
2
This estimation was derived from the effects described in a
SCP training study (Heinrich et al., 2004) and a sensorimotor
training study (Banaschewski et al., 2001).
4 Holger Gevensleben et al.
2009 The Authors
Journal compilation 2009 Association for Child and Adolescent Mental Health.
The training was complemented by some self-direc-
ted interventions from cognitive therapy to assure
comparability to NF, i.e., the children were to compile
(meta-)cognitive strategies such as focusing attention,
careful processing of tasks and impulse control.
Corresponding to the NF group, children of the AST
group should practise one of the strategies needed to
solve a task of the computer-game (‘watch like a
hawk’), in daily-life situations (as described in the NF
section above).
Parameterisation
Parent and teacher ratings were assessed at three
points (pre-training, intermediate, post-training). Pre-
training questionnaires were evaluated the week before
the first training session, intermediate and post-train-
ing ratings followed about one week after the last ses-
sion of the first and second block, respectively.
German ADHD rating scale (FBB-HKS; Do
¨
pfner &
Lehmkuhl 2000): The FBB-HKS is a 20-item ques-
tionnaire related to DSM-IV and ICD-10 criteria for
ADHD and hyperkinetic disorders, frequently used in
Germany in the evaluation of medical and cognitive
behavioural treatment of ADHD (i.e., Sevecke, Do
¨
pf-
ner, & Lehmkuhl, 2004). It was completed by parents
and teachers. The severity of each item was rated
from 0 to 3. Outcome measures were the main FBB-
HKS total score, i.e., the mean value of all items as
well as subscores for inattention and hyperactivity/
impulsivity. The FBB-HKS total score of the parents
constituted the primary outcome measure of the
study.
German Rating Scale for Oppositional Defiant/Con-
duct Disorders (FBB-SSV; Do
¨
pfner & Lehmkuhl,
2000), which allows parameterising oppositional
behaviour and delinquent and physical aggression.
Strength and Difficulties Questionnaire (SDQ; Ger-
man version; Woerner, Becker, & Rothenberger,
2004), which addresses both positive and negative
attributes.
The Home Situations Questionnaire (HSQ, German
version) was used to assess behaviour problems of the
child in specific home situations. The HSQ consists of
16 situations in which problematic child behaviour
can occur. Parents rate whether the problem behav-
iour is present in that setting; if so, they rate its
severity on a 9-point scale. (Do
¨
pfner, Schu
¨
rmann, &
Fro
¨
lich, 2002).
Problem behaviour during homework was assessed
using the Homework Problem Checklist (HPC, Ger-
man version). This parent checklist consists of 20
items, rated on a 4-point frequency scale (Do
¨
pfner
et al., 2002).
Evaluation scales (Froemke Inventory, 2005; unpub-
lished): a 9-item questionnaire developed by our
working group. The first part is made up of items
about the assumptions of parents regarding the type
of treatment their child receives (neurofeedback,
attention skills training, or a combination of both).
The second part comprises evaluative questions
about the helpfulness of the training (treatment ade-
quacy, satisfaction, and effectiveness) and the moti-
vation of their child on a five-point-scale (0 = in no
way/never; 4 = absolute/ever). All items are easy to
understand and easy to answer. Psychometric prop-
erties of the scales are unexamined.
If post-training ratings of the parents were missing,
intermediate ratings were included in the analysis (last-
observation-carried-forward approach, LOCF).
Data analysis
Since we had directed hypotheses (larger improvements
in the NF group compared to the AST group), one-sided
Student’s t-tests were applied for the analysis of train-
ing effects. For these between-group comparisons,
change scores (post-training minus pre-training) of
parents and teachers ratings were used. Intra-group
pre-post comparisons were tested for the primary out-
come measure (t-test, one-tailed). For comparison of
pre-training measures of the NF and AST group and the
evaluation of the treatment by the parents (‘placebo
scales’), two-sided t-tests were computed.
For the comparison of the NF protocols, an ANOVA
with within-subject factor ‘protocol’ (theta/beta vs.
SCP) and between-subject factor ‘order’ (of the proto-
cols) was calculated.
To compare the ratio of responders (25% reduction
of the primary outcome measure) in the NF group and
the control group, the odds ratio was calculated.
For all statistical procedures significance was as-
sumed if p<.05.
Results
From the 102 children with ADHD who were initially
assessed and randomly assigned to a training group,
8 children had to be excluded (NF: n=5; AST: n=3)
due to immediate need for medical treatment (n=3),
organisational problems of the parents (n=2), loss
of motivation (n=1) or protocol violation (n=2).
Hence, 94 children were included in the analysis
(NF: n=59; AST: n=35) with last-observation-car-
ried-forward in 7 children (NF: n=4; AST: n=3).
With mean FBB-HKS total scores of about 1.5,
ADHD symptomatology was moderately pronounced
in both groups.
Parent ratings
Parent and teacher ratings are summarised in
Table 2.
FBB-HKS: Improvement of the NF group in the
FBB-HKS total score (primary outcome measure)
was superior compared to the AST group
(t(91) = )2.88; p<.005). This effect reached a med-
ium effect size of .60 (Cohen’s d).
3
In both treatment
groups, a significant improvement resulted (NF:
t(57) = )7.90; p<.001, CI(95%):).49, ).29; AST:
(t(34) = )1.95; p=.03, CI(95%):).29, .01).
3
Considering boys only, the effect size was .56. So, slightly
(but not significantly) different gender ratios in the two groups
did not affect the main result of our study.
Neurofeedback training in children with ADHD
5
2009 The Authors
Journal compilation 2009 Association for Child and Adolescent Mental Health.
On the subscale level, improvements in inattention
and hyperactivity/impulsivity of about 25–30% in
the NF group were significantly larger compared to
about 10% in the AST group (inattention:
t(91) = )2.71; p<.005); hyperactivity/impulsivity:
t(91) = )2.01; p<.05).
Referring to oppositional and conduct behaviour,
the reductions in both FBB-SSV subscales in the NF
group exceeded the changes in the AST group (oppo-
sitional behaviour: t(91) = )1.82; p<.05; delinquent
and physical aggression: t(91) = )1.81; p<.05).
For the SDQ total score as well as for the hyper-
activity subscale, the decrease in the NF group was
significantly larger than in the AST group (total
score: t(91) = )2.25; p<.01), hyperactivity:
t(91) = )2.71; p<.005). For the remaining SDQ
subscales, no significant effects were observed.
Concerning problematic behaviour in family situa-
tions (HSQ-D) and homework problems (HPC-D), both
groups did not differ significantly from each other
(HSQ-D: t(83) = )1.05, n.s.; HPC: t(87) = .02; n.s.).
Post-hoc t-tests (two-tailed) conducted for the two
groups separately indicated improvements in the NF
group (HPC: t(55) = )4.08, p<.001; HSQ:
t(52 = )3.36; p<.001) as well as the AST group (HPC:
t(32) = )3.40, p<.002; HSQ: t(31) = )2.02, p<.1).
The responder rate in the NF group was superior to
the rate in the AST group. Thirty children of the NF
group (51.7%) and 10 children of the AST group
(28.6%) improved more than 25% in the primary
outcome measure (odds ratio: 2.68, p<.05:
CI(95%) = 1.10–6.48).
Parental evaluation/placebo scales: Evaluation
scales of 90 participants assessed at the end of the
training were available. There was no significant
difference between the groups in parents’ attitude
towards the treatment (e.g., effectiveness: NF group:
3.19 ± .82; AST group: 3.13 ± .90; t(88) = .30;
p=.77) and how parents rated the motivation of
their children (‘My child does not like the training’:
NF group: .64 ± .77; AST group: .56 ± 1.13;
t(88) = .37; p=.71).
Forty-two percent of the parents in the NF group
and 37% of the parents in the control group could
not reliably quote treatment assignment of their
child (i.e., these parents voted ‘I don’t know which
training my child attends’, ‘My child attends a com-
bination of a NF and an AST training’ or the parents
just estimated the wrong group).
Teacher ratings
For about 70% of the children, pre-training and post-
training ratings of the same teacher could be as-
sessed. Missing data, which did not differ signifi-
cantly between the two groups (v
2
-test: p=.25),
resulted from school or teacher changes or lack of
compliance. For the FBB-HKS total score, the
reduction in the NF group was superior to the effect
in the AST group (t(60) = )2.55; p<.01). A signifi-
cant effect was also found for the inattention sub-
scale (t(60) = )1.94; p<.05) and a trend for the
hyperactivity/impulsivity subscale (t(60) = )1.59;
p<.1). Effect sizes of .40 to .64 (medium effect sizes)
were in the same range as for the parent ratings (see
Table 2).
Analysing FBB-SSV and SDQ ratings of the
teachers, a significant effect resulted for the hyper-
activity subscale of the SDQ (t(54) = )1.72; p<.05).
Comparison of theta/beta and SCP training
For both training protocols (theta/beta, SCP), par-
ents rated comparable improvements in the FBB-
HKS total score as well as in the inattention and the
hyperactivity/impulsivity subscales (see Table 3).
Statistics revealed a trend towards better improve-
ment in the FBB-HKS total score, when theta/beta
training preceded SCP training (F(1,50) = 3.00;
p<.1).
Discussion
In the present study, the effects of neurofeedback
training for children with ADHD were evaluated
in comparison to a computerised attention skills
training aiming to provide further information about
the efficacy of neurofeedback. In contrast to previous
studies, the control treatment was designed to par-
allel the neurofeedback treatment as closely as pos-
sible with respect to unspecific factors, using larger
Table 3 Theta/beta-training vs. SCP-training (FBB-HKS, parent rating). Each participant of the NF group took part in a SCP- and a
theta/beta-protocol block (balanced order). The table shows differences (absolute scores) between the ratings before and after a
block
FBB-HKS change Theta/beta training SCP training ANOVA
Total score ).22 ± .40 ).19 ± .42 Protocol: F(1,50) = .09, n.s.
Order: F(1,50) = 3.00, p<.1
P · O: F(1,50) = .13, n.s.
Inattention ).26 ± .52 ).24 ± .56 Protocol: F(1,50) = .03, n.s.
Order: F(1,50) = 1.89, n.s.
P · O: F(1,50) = 1.78, n.s.
Hyperactivity/impulsivity ).18 ± .41 ).15 ± .43 Protocol: F(1,50) = .17, n.s.
Order: F(1,50) = 1.99, n.s.
P · O: F(1,50) = 1.31, n.s.
6 Holger Gevensleben et al.
2009 The Authors
Journal compilation 2009 Association for Child and Adolescent Mental Health.
sample sizes and a randomised group assignment.
Neurofeedback was not confounded with additional
interventional strategies such as medication, cogni-
tive skills training or parental counselling.
Behaviour ratings by parents and teachers
revealed a superiority of the NF training in decreas-
ing ADHD symptomatology. Medium effect sizes of
about .6 for the FBB-HKS in parent and teacher
ratings indicate that NF effects are substantial and of
practical importance. Our results confirm findings
of previous NF studies even under strict control
conditions.
Positive effects do not appear to be restricted to
core ADHD symptoms, but also affected accompa-
nying problems of social adaptation as indicated by
the decreases in the FBB-SSV subscales, the SDQ
total score, the HSQ and HPC rating.
Control condition
Children in the control group repeatedly practised
attentional tasks and their application in daily life.
Thus, the control training targets attention man-
agement skills directly, i.e., it may have specific
aspects (Subrahmanyam, Greenfield, Kraut, &
Gross, 2001). Compared to a placebo condition, the
use of an attention skills training may have raised
the bar for the NF training.
According to scientific standards, a double-blind,
placebo-controlled design is suggested to isolate
specific effects and is lacking in NF research (Loo &
Barkley, 2005). However, such a design, in which
participants as well as raters are actually ‘blind’, is
hard to realise for an NF study and must even be
questioned for medication studies, which are usually
not controlled for the validity of the blinding proce-
dure (Margraf et al., 1991).
Beyond ethical considerations discussed, e.g., in
Heinrich et al. (2007), regulation of brain electrical
parameters poses certain practical problems for the
placebo design. It is difficult to gain mastery over
cortical self-regulation. For example, in SCP training
up to 60% of the trials are regulated successfully if a
subject has appropriate regulation strategies (Leins,
2004), which leaves 40% or more of the trials
unsuccessful. Being aware of the possibility of
practising a placebo condition may lead to an
enhanced impression of uncontrollability, which in
turn may result in a loss of motivation and dimin-
ished effort (learned helplessness) and thus worsen
treatment outcome.
Specific vs. unspecific training effects
The control training was designed to be comparable
with respect to training setting, demands upon par-
ticipants and therapeutic support in general. Since
parents of the NF group and the control group did
not differ in expectations or satisfaction with the
treatment, these factors should not have influenced
the results. Thus, our findings support the notion
that, first and foremost, specific factors account for
the superiority of the NF training.
On the other hand, mainly due to the non-blind
design, it is possible that additional factors not
considered in our study may have affected the
results; e.g., we did not assess the children’s attitude
towards and satisfaction with the training directly.
It cannot entirely be ruled out that expectations,
comprehension and effort may have been different
between the children of the two groups, even though
both trainings were paralleled.
Besides controlling for these factors in future
studies, further evidence for the specificity of train-
ing effects may be gained by relating neurophysio-
logical measures (e.g., estimates of NF regulation
capabilities or pre- to post-training changes in EEG
and ERP parameters) to the clinical outcome.
NF training setting
The improvement in the primary outcome measure
(FBB-HKS total score) of about 26% after neuro-
feedback training is comparable to our previous
study (Heinrich et al., 2004), as well as behavioural
improvements obtained by other groups (Strehl
et al., 2006; Drechsler et al., 2007; Fuchs et al.,
2003). Actually, we had expected larger effects of
about 30–35% since the children had more training
sessions and practised both theta/beta training
(aiming at tonic aspects of cortical arousal) and SCP
training (related to phasic regulation of excitability
underlying attentive behaviour). However, one block
of 18 sessions might have been too short to build up
stable regulation competence. The two protocols
were not coordinated but trained in different blocks
in order to compare the two protocols at the intra-
individual level. To all appearances, several children
seemed to be unable to distinguish regulation and
transfer strategies of the SCP vs. the theta/beta
protocol, but this information was not assessed
systematically.
In addition, in order to avoid confounding vari-
ables we abstained from some basal elements to
enhance effectiveness, such as combination with
cognitive/learning strategies and involvement of
parents and teachers (Pelham et al., 1998; Drechsler
et al., 2007).
Owing to these restrictions of our training setting,
it may not be appropriate to indirectly compare the
efficacy of NF based on our results with RCTs of
other treatment approaches (e.g., long-acting medi-
cations with effect sizes of about .6 to 1.0; Banas-
chewski et al., 2006).
Responders vs. non-responders
As a consequence of the non-optimal training
setting, the rate of responders (about 52%) in the
neurofeedback group, though superior compared to
Neurofeedback training in children with ADHD 7
2009 The Authors
Journal compilation 2009 Association for Child and Adolescent Mental Health.
the control condition (about 29%), fell short of our
expectations.
But what differentiates responders from non-
responders, i.e., from children who could benefit
from NF training but to a smaller degree or not at
all? In a further step it should be investigated if
clinical, psychosocial factors as well as neuropsy-
chological and physiological parameters may predict
the outcome of NF training. Thus, it could be possi-
ble to establish criteria that indicate in which cases
NF could be particularly useful as well as identify
factors that require particular attention during the
training.
General differences between the NF protocols, i.e.,
theta/beta and SCP training, could not be obtained
in our study. However, this does not preclude that an
individual child could benefit more from one protocol
than the other. Our data also suggest that a certain
order of protocols might be advantageous. So the
above-mentioned issue of response prediction
should also be extended to the question of which
factors could influence improvement following a
distinct protocol or which combination of protocols
might be appropriate for an individual child.
NF in a multimodal treatment setting
Owing to the heterogeneity of children with ADHD
and a multiplicity of behavioural and psychosocial
factors, it does not seem reasonable to expect suffi-
cient clinical improvement in all children following
neurofeedback as the only intervention, particularly
if more severely impaired children than those who
participated in our study are considered. Further
research will show how to combine NF optimally with
additional cognitive behavioural and social inter-
vention strategies, parental counselling, and medi-
cation within the framework of a multimodal
treatment setting. For example, medication might
help children benefit more from NF training, or NF
could help reduce medication dosage or prevent
relapse.
Conclusion
Our results indicate that NF may be considered as
a clinically effective module in the treatment of
children with ADHD. Further studies are needed not
only to replicate our findings but also to control for
factors not covered in our study, to further isolate
specific effects of NF and to address inter alia how
to optimise NF training, also taking the long-term
outcome into account.
Note
Trial registry: ISRCTN87071503 Comparison of
neurofeedback and computerised attention skills
training in children with attention-deficit/hyper-
activity disorder (ADHD). (http://www.controlled-
trials.com/ISRCTN87071503).
Acknowledgements
The authors thank Christa Dahlmann, Martin
Deinzer, Susanne Wangler and all student assis-
tants for their valuable support as well as all par-
ticipating families for their contribution and effort.
This study was supported by the German Research
Foundation (with a joint grant to H.H., G.H.M, and
A.R.; HE 4536/2, MO 726/2, RO 698/4).
Correspondence to
Hartmut Heinrich, Heckscher-Klinikum, Deisen-
hofener Straße 28, D-81539 Mu
¨
nchen, Germany;
Tel: (+49)89/9999-1116; Fax: (+49)89/9999-1111;
Email: hheinri@arcor.de
Key points
For children with ADHD, a reduction of inattention, impulsivity and hyperactivity by neurofeedback (NF)
has been reported in several studies. To overcome methodological shortcomings of previous studies, we
evaluated clinical efficacy in a randomised controlled study using a computerised attention skills training
as a control condition.
For parent and teacher ratings, improvements in the neurofeedback group were superior to those of the
control group (medium effect size).
This is the first randomised controlled trial on neurofeedback in children with ADHD indicating clinical
efficacy with sufficient statistical power.
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    • "This decision modifies the next stimulation to be streamed down to the subject, thus closing the interactive loop. This type of interactive service could permit online cognitive telerehabilitation, such as neuro-feedback applied to a multitude of pathologies (e.g., attention deficit hyperactivity disorder [30, 31], autism spectrum [32, 33], cerebral palsy [34], and mental impairment [35]). Notice that IP protocols offer synchronization mechanisms in all links and interfaces ofFig. "
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    • "Some of these results are controversial. A number of studies reported positive outcome of neurofeedback training (Leins et al., 2007; Gevensleben et al., 2009; Steiner et al., 2011; Wangler et al., 2011), whereas others questioned these findings. In the camp of neurofeedback advocates, Arns et al. (2009) analyzed literature on neurofeedback therapy for ADHD and concluded that this treatment was " efficient and specific " (Arns et al., 2009). "
    [Show abstract] [Hide abstract] ABSTRACT: We have witnessed a rapid development of brain-computer interfaces (BCIs) linking the brain to external devices. BCIs can be utilized to treat neurological conditions and even to augment brain functions. BCIs offer a promising treatment for mental disorders, including disorders of attention. Here we review the current state of the art and challenges of attention-based BCIs, with a focus on visual attention. Attention-based BCIs utilize electroencephalograms (EEGs) or other recording techniques to generate neurofeedback, which patients use to improve their attention, a complex cognitive function. Although progress has been made in the studies of neural mechanisms of attention, extraction of attention-related neural signals needed for BCI operations is a difficult problem. To attain good BCI performance, it is important to select the features of neural activity that represent attentional signals. BCI decoding of attention-related activity may be hindered by the presence of different neural signals. Therefore, BCI accuracy can be improved by signal processing algorithms that dissociate signals of interest from irrelevant activities. Notwithstanding recent progress, optimal processing of attentional neural signals remains a fundamental challenge for the development of efficient therapies for disorders of attention.
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    • "Some of these results are controversial. A number of studies reported positive outcome of neurofeedback training (Leins et al., 2007; Gevensleben et al., 2009; Steiner et al., 2011; Wangler et al., 2011), whereas others questioned these findings. In the camp of neurofeedback advocates, Arns et al. (2009) analyzed literature on neurofeedback therapy for ADHD and concluded that this treatment was " efficient and specific " (Arns et al., 2009). "
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