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In children with attention-deficit/hyperactivity disorder (ADHD), different neurofeedback (NF) protocols have been applied, with the most prominent differentiation between EEG frequency-band (e.g., theta/beta) training and training of slow cortical potentials (SCPs). However, beyond distinctions between such basic NF variables, there are also competing assumptions about mechanisms of action (e.g., acquisition of regulation capability, generalization to daily life behavior). In the present article, we provide a framework for NF models and suppose two hypothetical models, which we call “conditioning-and-repairing model” and “skill-acquisition model,” reflecting extreme poles within this framework. We argue that the underlying model has an impact not only on how NF is applied but also on the selection of evaluation strategies and suggest using evaluation strategies beyond beaten paths of pharmacological research. Reflecting available studies, we address to what extent different views are supported by empirical data. We hypothesize that different models may hold true depending on the processes and behaviors to be addressed by a certain NF protocol. For example, the skill-acquisition model is supported by recent findings as an adequate explanatory framework for the mechanisms of action of SCP training in ADHD. In conclusion, evaluation and interpretation of NF trials in ADHD should be based on the underlying model and the way training is applied, which, in turn, should be stated explicitly in study reports.
Overwhelming evidence exists for (1) the plasticity of the human brain, especially in childhood (
In a RCT of our group, NF comprised two “standard-protocols”: theta/beta training [aiming to decrease theta (4–8 Hz) activity and to increase beta (13–20 Hz) activity] and training of slow cortical potential (SCP; associated with the bidirectional regulation of cortical excitability). Both protocols were trained in separate blocks and paralleled regarding the setting and demands upon the participants. For NF, we obtained a larger reduction of the severity of ADHD symptoms (medium effect size) compared to a computerized attention skills training (“active control group”;
In clinical practice, so-called QEEG (quantitative EEG)-based NF is also applied in ADHD. Before starting QEEG-based NF, multichannel-EEG is recorded and compared to a database of typically developing children. Frequency band and electrode location showing the greatest deviance from the “norm” are targeted during training. Related to this individualized approach, a randomized double-blind placebo-controlled trial was conducted by
From the short descriptions of these two RCTs, it becomes apparent that different NF protocols and different evaluation strategies have been applied
In the present article, we intend to provide a framework for defining NF models based on those above-mentioned aspects. To underline the relevance of the framework, which is suggested for theoretical and practical purposes, we reflect available studies and illustrate that different views are supported by empirical data.
Application of NF in children with ADHD directly evolved from considerations about distinct neurophysiological dysfunctions (reviewed for example by Albrecht et al., submitted), encompassing different brain electrical activity parameters and electrode locations. Elevated theta/beta ratios in the resting EEG, reflecting reduced tonic cortical activation (
Following a classical medical model of (psychiatric/neurodevelopmental) disorders, “repairing” the presumed cause (neurophysiological deficit) should “normalize” behavior: “The principle of NF is that over time, participants learn operant control of their EEG and change from an ‘abnormal’ state to one resembling that of typically developing children. This process is thought to eventually remediate the symptoms associated with ADHD” (
On the other hand, NF may simply be regarded as “a tool for enhancing specific cognitive or attentional states in certain situations” (
Nowadays, etiology of (psychiatric/neurodevelopmental) disorders is rather investigated on the basis of a bio-psycho-social model, considering the impact of different factors on different levels. Accordingly, regarding treatments, different areas of impact should also be taken into account. Therefore, NF does not necessarily need to address only a distinct neural dysfunction but may encompass (compensatory) mechanisms on different interacting levels, the strengthening of neural resources as well as changes of cognitive-behavioral and social variables
Particularly traditional models of NF in child and adolescent psychiatric disorders consider a stable change in the EEG signature (
Others tend to expect an improved skill to change the “
Concerning core mechanisms of NF, changes in within-session neuro-regulation (i.e., changes in EEG activity during treatment sessions) and improvements in neuro-regulation as the training proceeds are expected before changes in the clinical outcome result. Such systematic changes in EEG activity following positive reinforcement could be obtained in animals as well as in humans (e.g. Strehl, submitted). However, learning might evolve in an implicit (unconscious and automatic) and/or explicit (goal directed, controlled, and attention-demanding) way.
Implicit learning is defined as “the acquisition of knowledge that takes place largely independently of conscious attempts to learn and largely in the absence of explicit knowledge about what was acquired” (
At least it seems plausible that learning of neuro-regulation is enhanced by precise monitoring of the EEG signals being fed back, searching for a link between internal regulation and the mirrored neuronal signals, intentional building, and testing of cognitive strategies to shift generated EEG activity pattern in the required direction (for an overview of learning mechanisms in NF see Strehl, submitted). Therefore, controlled cognitive processes may also be involved in the acquisition of neuro-regulation capability (and generalization of self-regulation ability to daily life; see following section), suggesting rather an active role for the participant.
A further, often neglected notion is the superior cognitive level of expectations and attributions of patients: how do the participants perceive the training and participate in the exercises, what is the role of motivational, attributional, and personality factors for the course and outcome of the training (
Training effects should not be restricted to the environment where the NF training is conducted. NF strives for behavioral changes in daily life. If NF repairs an underlying neural dysfunction and/or learning happens automatically and unconsciously then generalization should occur automatically: “...
If NF relies on controlled learning and acquisition of skills and outcome depends on attributions and motivation, additional effort to transfer novel skills into daily life appears necessary in order to improve efficacy and clinical value.
The assumptions reflected in the previous section impact the way NF training is applied.
Assuming a distinct neurophysiological dysfunction to be addressed in NF training in children with ADHD has implications for the indication of NF. Primarily, subjects with a manifest neurophysiological dysfunction (e.g., enhanced theta and/or reduced beta activity) are expected to improve behavior after NF training addressing this particular dysfunction (e.g.,
If, on the other hand, NF is expected to exert its effects via (compensatory) mechanisms on different (neurophysiological and cognitive-behavioral) levels pre-selection based on distinct neurophysiological profiles does not play an essential role. Room for improvement in self-regulation on the neurophysiological and cognitive-behavioral level provides rough indication criteria, hopefully in the future differentiated and optimized by knowledge about moderators of outcome (neurophysiological, cognitive, and social predictors of improvement such as distinct EEG parameters, personality variables, and supporting social conditions). Treatment focuses on neurophysiological functioning during the treatment sessions but also targets further variables on the cognitive-behavioral (self-efficacy, achievement motivation) and social level (social reinforcement), interacting with the achievement in neuro-regulation capability. Further effort (via cognitive-behavioral interventions such as education/instructions, positive/social reinforcement, transfer tasks/home work and parent/teacher counseling) is spent to ensure enhancement of general behavioral self-regulation capability (
Mechanisms of the acquisition of neuro-regulation capability beyond basic operant mechanisms (reaction-consequence-contingency; positive reinforcement; for an overview see
In concurring approaches the need for active and effortful engagement is emphasized: “
To assume that generalization of effects occurs automatically (via change of “EEG trait”) makes further efforts obsolete. Enduring and general change in significant EEG pattern after NF training should lead to enduring and general change in daily behavior automatically.
On the other hand, if NF is interpreted as a neuro-behavioral treatment aimed at developing skills not only for self-regulation of brain activity but also for general behavior in daily life, additional elements are introduced in the training (
Concurring assumptions and resulting ways of application regarding NF (in attention-deficit/hyperactivity disorder, ADHD).
“Conditioning-and-repairing model” | “Skill-acquisition model” | |
Indication | Specific neurophysiological deficit | No specific deficit |
Mechanisms of learning |
Automatic, unconscious (implicit) learning (operant conditioning of EEG pattern) | Controlled, effortful acquisition of regulation skills (explicit learning) |
Significance of psychological and social variables and personality traits as moderators/mediators | Susceptibility to basic learning mechanisms (operant conditioning), no higher-order cognitive processes involved. | Effects moderated/mediated by cognitive-attributional variables; generalization of effects moderated by social support, positive reinforcement of target behavior |
Effects of the treatment | Automatic change in EEG-trait (tonic change). | Change in EEG-state (phasic changes), acquisition of self-regulation skills, enhancement of neurophysiological functioning |
Instructions, acquisition of self-regulation | No active trainer, no specific instructions/no effort needed, passive participant | Active coaching, support in the search for regulation strategies, active participant, effort to enhance self-regulation skills |
Generalization | Automatic transfer to daily life → no effort necessary to support generalization | Transfer-trials; tasks for generalization of effects (e.g., homework) |
Setting | Unimodal treatment (Repairing the EEG deficit “normalizes” behavior.) | Module in a multimodal treatment, |
The so called “
Alternatively the so called “
The distinction of specific vs. non-specific variables of a treatment also relies on the underlying model. Continuous monitoring of behavior, contingent feedback, and positive reinforcement might be considered powerful variables of NF. During NF, monitoring, feedback, and reinforcement impact the neurophysiological as well as the cognitive-behavioral level. In view of a conditioning-and-repairing model, reinforcement on the cognitive-behavioral level (praise by the trainer, pride about a good score, both leading to enhanced self-efficacy) constitutes an unspecific variable. On the background of a “skill acquisition model,” these are basic variables and essential prerequisites of further treatment variables (neuro-regulation).
There is no doubt that RCT are necessary to evaluate efficacy of NF in the treatment of children with ADHD. In pharmacological research, double-blind, placebo-controlled trials are considered the gold standard in the evaluation of efficacy. Concerning the mechanisms of action of pharmacological treatment, placebo conditions should allow a valid separation of specific from non-specific effects. Blindness to the treatment condition and placebo-control are meant to level the expectations of the participants about the treatments. This is reasonable in the evaluation of efficacy of treatments, if a treatment does not rely on the participant’s expectations and active engagement.
Larger effects of NF compared to placebo training would indicate efficacy and specificity of NF. Unfortunately, previous placebo-controlled trials found no superiority of NF in children with ADHD (see
Following a “
Following the “
Though no NF study in the fields of ADHD to date directly investigated the moderating effects of those basic variables, the results of latest placebo-controlled trials (as reported above) are in line with the aforementioned assumption.
Active control conditions may be preferable (e.g., computerized attention training, EMG biofeedback training including a feedback of artifacts derived from the EEG;
A comparison of different NF protocols can be regarded as another evaluation strategy which may be applied irrespective of the underlying model. Larger clinical improvements for one NF protocol than another provides clear evidence for specific effects (e.g.,
In the “Mechanisms and Applications – Models of NF in Children with ADHD” section, we assembled concurring assumptions about the indication, mechanisms of change, and effects of NF. In the following we will highlight some empirical evidence concerning each of the above mentioned notions. Empirical evidence concerning certain aspects of NF is rare and contradictory. Most studies evaluated outcome of NF rather than treatment processes. Hence, valid data concerning prerequisites and predictors of outcome as well as mechanisms of change (learning, generalization) often is missing. We will focus on standard protocols of NF in children with ADHD (theta/beta and SCP training) and lend some findings from trials with healthy adults if indicated. Our aim is not to give an exhaustive review of the existing literature but to substantiate our aforementioned considerations and to elucidate the eligibility of the presented models of NF in order to encourage further research elucidating mechanisms of NF. A comprehensive overview concerning the empirical validation of NF in healthy adults is provided by
An elevated theta/beta ratio (enhanced theta activity, reduced beta activity) has been considered a neurophysiological marker of children with ADHD (
On the other hand,
A reduced CNV has been reported in the major part of studies in children with ADHD (for review see Albrecht et al., submitted) though complexity (
Generally it should be kept in mind that the mentioned “neuronal deficits” represent only some neuronal correlates of disturbed behavior but do not give a full explanation of the complex ADHD picture. Hence, the thinking of “just repairing” appears to be rather simplistic. Moreover, as ADHD is considered a clinically and pathophysiologically heterogeneous condition, it appears rather likely that a deviant neurophysiological pattern is not shared by all children with ADHD.
We found a decrease in theta activity (no change of beta activity) in the resting EEG after NF, irrespective of the treatment protocol (SCP- vs. theta/beta training;
On the other hand, it has to be considered that, during training, children practiced to get into an “active,” attentive state (in contrast to the resting condition) and that no effects were observed for beta activity and the theta/beta ratio, respectively, which were also targeted during training.
In healthy adults, associations between distinct NF protocols and changes in the spectral topography of the resting EEG do not support the change of EEG trait notion (
Evidence for protocol-specific general and lasting change in resting EEG activity (that we would consider a change of EEG trait) is inconclusive. However, sustainability of NF induced tonic resting EEG changes might depend on the number of treatment sessions. Maybe more sessions than conducted in previous trials would be necessary to achieve enduring change
All in all, there is valid evidence that SCP training attenuates an initial deficit in regulation of cortical excitability in children with ADHD. There is also evidence that a link between the neurophysiological and the cognitive-behavioral level contributed to improved clinical outcome.
Investigation of implicit learning mechanisms relies on dissociation paradigms to prevent awareness of the learning process. No serious attempt has been practice in neuro-regulation until now in order to assess, in how far neuro-regulation might evolve implicitly in first and foremost.
In a recent summary of their efforts to elucidate the acquisition of regulation capability
However, the forced acquisition of neuro-regulation skills during scientific trials or clinical applications in humans and even in rodents proceeds not implicitly (out of awareness) but intentional and goal-directed (
Therefore, although acquisition of neuro-regulation encompasses mechanisms of procedural learning, there is no clear evidence until now, that neuro-regulation primarily results from implicit learning (automatic, out of conscience, not goal-directed).
Acquisition of neuro-regulation seems to depend on attention (
Due to the fact that implicit and explicit processes usually interact in skill learning (
After a single session of NF (voluntary alpha-attenuation),
In
On the other hand, the finding of
Concerning ADHD, the outcome of SCP training may differ depending on whether transfer tasks rather address attentional or motor aspects. In several studies, SCP training induced comparable reductions of inattentive and hyperactive/impulsive behavior (e.g.,
There is strong evidence for the efficacy and specificity of certain NF approaches in ADHD, particularly SCP training applied as a neuro-behavioral treatment. Evidence results from trials using active control conditions, comparing different NF protocols and also by taking changes on the neurophysiological level into account. Hence, we argue that the guiding question today is, how to optimally use NF techniques to enhance efficacy of NF and how to optimize training for a certain participant (“personalized medicine”).
In the present article, we outlined that different models exist how NF may work (with the “conditioning-and-repairing model” and the “skill-acquisition model” representing two extreme poles) and that the underlying model unfolds implications for the application of the training as well as for the evaluation design of a RCT. These aspects may contribute to the divergent findings and interpretations regarding NF in ADHD. We recommend the following points for (future) NF trials in ADHD:
As long as there is no detailed knowledge about the mechanisms of NF (in circumscribed fields of application) the assumptions about the mechanisms on which the application of NF is based shall be expatiated according to the framework proposed.
It has to be checked that potential operators and moderators of efficacy are not attenuated by the design of the trial or the application of the NF protocol.
Evaluation and interpretation of NF trials shall be based on the underlying model and the way training is applied.
Besides these aspects related to our framework, it is important that the application of NF follows the principles of learning theory (
Reflecting the available literature, we suppose that
NF is indicated whenever self-regulation ability should be enhanced and there is valid knowledge about neurophysiological target patterns.
The acquisition of regulation capabilities advances in a goal-directed manner with implicit and explicit learning mechanisms interacting closely.
Learning of neuro-regulation does not solely rely on neurophysiological preconditions but is significantly moderated by attributions, personality, and motivational factors and relies on personal effort.
exhaustive rehearsal presumably leads to improved and automated regulation skills accompanied by changes in functional and structural brain “
Concerning the aspect of generalization, empirical findings indicate that different models may be valid depending on the NF protocol and mechanisms to be addressed by the training. We hypothesize:
Distinct and circumscribed bottom-up mechanisms are enhanced by improved neurophysiological functioning alone (e.g., related to encoding or procedural learning in an experimental task).
Complex attentional and social behaviors (encompassing different top–down and bottom–up mechanisms) rely to a larger extent on self-regulation skills and will not change to a clinically significant level due to distinct neurophysiological changes alone but have to be addressed on different levels. Neurophysiological changes must spread out beyond NF-trained neuronal circuits and be accompanied by changes in cognitive-behavioral patterns to achieve enhanced self-regulation in complex environments.
We are aware that evidence for these propositions is weak, However, they may serve as a clue for future studies that should target possible moderators (e.g., neurophysiological profile, comorbidity, social support, treatment setting) and mediators of change (e.g., neuro-regulation, changes in attributions, and behavioral skills) as well as obligatory vs. optional variables of a specific NF approach and model, respectively.
The scope should be widened from outcome to process evaluation to study an interplay of variables on different levels. This may not only comprise behavioral (e.g., severity of ADHD core symptoms and associated domains) and neurophysiological factors (neuro-regulation data over the course of the training; brain electrical activity at rest and during task performance in the lab) but also psychological and environmental aspects. In this context, we suggest to consider appropriate evaluation scales and to manipulate factors systematically as part of the research protocol (e.g., enhancing or diminishing treatment credibility or self-efficacy by specific instructions).
Conducting such studies would allow to fill gaps in current models of NF in ADHD gradually and to judge which model is suitable for which application (under which conditions).
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
There are also significant differences in the implementation of feedback protocols concerning aspects like fixed vs. variable thresholds, discrete vs. continuous feedback, discussed elaborately by
Changes of cognitive-behavioral and social variables are also reflected in changes of underlying neural networks.
As “trait” we understand individual EEG patterns considered stable over time and situations, usually measured in resting conditions and representing an idiosyncratic EEG signature of a person. As “state” we define EEG activity based on the EEG trait, triggered by distinct situations and assessed during an active condition (typically during task performance).
In other areas, placebo-controlled designs were applied successfully (
Ethical aspects also argue against the use of a placebo condition (
Increases in gamma activity in the resting EEG of Buddhist practitioners doing meditation training for 10.000–50.000 h over 15–40 years (