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 Heinrich2,3
1Child & Adolescent Psychiatry, University of Go¨ttingen, Germany; 2Child & Adolescent Psychiatry,
University of Erlangen-Nu¨rnberg, Germany; 3Heckscher-Klinikum, Mu¨nchen, Germany
Background: 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.
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) completed 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, 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.
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 hyperactivity. 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 byimpaired 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 disorder recommend a multimodal treatment, encompassing medication, cognitive behavioural and family treatments (Taylor et al., 2004). However, previous child-oriented cognitive-behavioural intervention strategies have not always proven to be sufficiently effective, especially in terms of generalisation 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 treatment options for children with ADHD, NF emerged as one of the most promising options (Heinrich, Gevensleben, & Strehl, 2007). NF is a neurobehavioural 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 children with ADHD.
A training of slow cortical potentials1 is related to phasic regulation of cortical excitability. Surfacenegative SCPs (‘negativities’) and surface-positive SCPs (‘positivities’) have to be generated over the sensorimotor cortex. Negative SCPs reflect increased excitation and occur, e.g., during states of behavioural
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 electroencephalogram (EEG) which corresponds to an alert and focused but relaxed state. Thus, this training paradigm addresses tonic aspects of cortical arousal.
The rationale of applying these paradigms in ADHD is based on findings from EEG and eventrelated 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 (hypothetical 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 randomisation,mixed multiple intervention strategies or disregard of long-term outcome. These shortcomings preclude unambiguous interpretation or generalisation 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 variables
(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 treatment effects. Since theta/beta and SCP training are thought to address different aspects of cortical regulation – both being important for an optimal attentive behaviour (Rockstroh, Elbert, Lutzenberger, & 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 differences 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-certified 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 ocal ethics committees of the participating clinics and conducted according to the Helsinki declaration. Assent was obtained from the children and written informed consent from their parents.
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