Theta/beta neurofeedback in children with ADHD: Feasibility of a short-term setting and plasticity effects
Introduction
Neurofeedback (NF) involves a brain-computer interface which enables participants to learn to gain self-control over specific aspects of their neural activity. Neuroregulation skills are acquired through a series of repeated sessions and behavioral, cognitive and/or emotional effects can be induced based on the NF protocol applied. NF can be conducted alone or in conjunction as a neuro-behavioral training, which addresses the successful application of these skills in daily life, i.e., how and when to apply the cognitive strategies, while linking their use to cues (comparable to the use of verbal self-instructions; Gevensleben et al., 2014b). There are many forms of NF, but one specific protocol that is often used is EEG-based theta/beta NF which aims at reducing theta and enhancing beta activity - thus addressing tonic aspects of cortical activation (Ros et al., 2014). This NF protocol has been developed as an effective treatment for children with attention-deficit/hyperactivity disorder (ADHD) with evidence from randomized trials demonstrating that core symptoms of ADHD (i.e., inattention, motor hyperactivity and impulsivity; American Psychiatric Association, 2013) decreased to a larger extent compared to active control conditions like EMG biofeedback (medium effect sizes) (Arns et al., 2014).
As a rationale for applying theta/beta training in ADHD, authors typically referred to findings from earlier resting-state EEG studies comparing children with ADHD to typically developing controls (see e.g. Heinrich et al., 2007). These studies reported that children with ADHD have elevated levels of slow-wave theta activity and reduced faster-wave alpha/beta activity (corresponding to exaggerated theta/beta and theta/alpha ratios; for review see Barry et al., 2003). However, recent findings argue against considering the theta/beta ratio (TBR) in the resting EEG as a reliable EEG biomarker for ADHD, suggesting that, at best, only a subgroup of children with ADHD exhibit an excessive TBR at rest (see meta-analysis of Arns et al., 2013). During an attentive state, Heinrich et al. (2014) found an increased TBR only for children with the predominantly inattentive subtype of ADHD while children with the combined subtype showed deviations in the upper-theta/lower-alpha (5.5–10.5 Hz) range, thus not supporting a generally increased TBR in ADHD during task processing. Due to these contrasting EEG findings concerning children with ADHD, it remains open whether theta/beta training is mainly suited for a subgroup of children with ADHD and should thereby be viewed as ‘correcting’ abnormal oscillatory activity. On the other hand, theta/beta NF can alternatively be seen as a method for augmenting general brain activation or plasticity, resulting in enhanced cognitive or attentional states, consistent with the way it is practiced in so-called peak-performance applications (Gruzelier, 2014), i.e., not contingent on abnormal brain oscillations.
In previous NF studies, evidence was found for oscillation-specific effects of theta/beta training in children with ADHD by assessing pre- vs. post-training EEG recordings. Higher baseline theta activity in the resting EEG (recorded in an eyes open condition) over centro-parietal regions predicted greater reductions of ADHD symptom severity after theta/beta training (Gevensleben et al., 2009). Additionally, the decreases of theta activity inter-individually correlated with clinical improvements pre- to post-NF training. These findings were replicated by Janssen et al. (2016) in regard to the resting EEG. However their active condition (Stop Signal Task) produced a non-significant finding, which may be an issue of statistical power. Gevensleben et al. (2009) also observed a decrease in theta activity (no change of beta activity) in the resting EEG after NF, but this effect was also observed for a NF training of slow cortical potentials. Monastra et al. (2002) reported a decrease of the TBR and clinical symptoms after theta/beta training in children with ADHD characterized by a high baseline TBR. However, among other differences, pre- and post-training EEG assessments encompassed several conditions (resting and task conditions) and could therefore also represent enhanced online regulation-skills, reflective of task-specific ‘EEG states’, rather than spontaneous ‘EEG traits’.
Taken together, more clarification is needed concerning the mechanisms of action of theta/beta training in ADHD. Further efforts are required to learn more about the underlying mechanisms as well as to test potential optimizations. However, due to the length of typical NF trials for ADHD treatment (30–40 sessions), more economical evaluation strategies would be helpful to study these aspects. In this respect, short-term assessments may provide an elegant alternative. Using a single-session design in several studies (Ros et al., 2010, Ros et al., 2013, Kluetsch et al., 2014), Ros and colleagues focused on a desynchronizing form of NF, which involved inducing cortical ‘activation’ by reducing EEG spectral power, particularly of sensory ‘alpha’ (8–12 Hz) rhythms. They found that this NF protocol can be quickly learned by healthy adult participants, while demonstrating its neuroplastic effects in the direct aftermath of NF, i.e., up to 30 min after termination of training. In the Ros et al. (2010) study, post-NF resting-state changes directly correlated with the degree of EEG entrainment during NF, consistent with mechanisms of Hebbian plasticity (see Ros et al. (2014) for a review). Subsequently, Ros et al. (2013) reported a positive correlation between post-NF changes in resting-state alpha rhythm and self-reported ‘on task’ mind-wandering. Lastly, Kluetsch et al. (2014) proceeded to apply this single-session protocol to a clinical population with post-traumatic stress disorder, uncovering an association between individual alpha rhythm increase (or ‘rebound’) and improvement in subjective wellbeing. These studies provide mechanistic insights as well as clear evidence that plastic changes may occur after exposure to only one session of NF training.
In the present study, we applied a comparable short-term design for theta/beta NF training in children with ADHD. We intended to test the feasibility of this approach and to learn more about the mechanisms underlying this protocol which is frequently applied in ADHD therapy. Instead of conducting a controlled study, we chose to differentiate between good regulators (GR) and poor regulators (PR) based on the acquisition of neuroregulation ability. We hypothesized that: 1. Children with ADHD would be able to significantly decrease their TBR within two training sessions. 2. In cognitive tasks conducted directly after the training sessions, larger decreases of the TBR accompanied by improved performance would be observed in good regulators compared to poor regulators, indicating neuroplasticity.
Section snippets
Participants
Thirty-one children with a diagnosis of ADHD (according to DSM-IV criteria), aged ten to fifteen years old, participated in this study. Participants were recruited from a waiting list of families who had contacted the outpatient department of our clinic, expressing interest in receiving neurofeedback therapy. All children had normal or corrected to normal vision. Of those children, three failed to complete all three appointments and six had too many artefacts in the EEG, resulting in twenty-two
Neuroregulation measures
A main effect of TIME was found in the second NF session for both theta and TBR in which both theta and TBR decreased from the first to third puzzle. An interaction between TIME and GROUP was found for theta in both sessions, characterized by a decrease in theta for the GR and an increase for the PR (see Table 2). No significant effect of TIME or interaction of TIME × GROUP was found for beta. Looking at the course of the activity in the target bands over the trials (see Fig. 4), the theta signal
Discussion
Here, based on a traditionally applied NF protocol for ADHD, we investigated the feasibility of short-term theta/beta NF (i.e., two training sessions) for children with ADHD in order to more directly elucidate its mechanism(s). We could demonstrate that children with ADHD achieved a significant decrease of their TBR during neuroregulation trials within two sessions, which was mainly driven by decreases of theta activity. Moreover, we found an association between neuroregulation ability and
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