Theta/beta neurofeedback in children with ADHD: Feasibility of a short-term setting and plasticity effects

https://doi.org/10.1016/j.ijpsycho.2016.11.004Get rights and content

Highlights

  • The use of a short-term neurofeedback paradigm is investigated.

  • Children with ADHD can learn to neuroregulate in two neurofeedback sessions.

  • Neural plasticity was demonstrated during a reading task.

  • Results are separable by neuroregulatory ability.

Abstract

Neurofeedback (NF) is increasingly used as a therapy for attention-deficit/hyperactivity disorder (ADHD), however behavioral improvements require 20 plus training sessions. More economic evaluation strategies are needed to test methodological optimizations and mechanisms of action. In healthy adults, neuroplastic effects have been demonstrated directly after a single session of NF training. The aim of our study was to test the feasibility of short-term theta/beta NF in children with ADHD and to learn more about the mechanisms underlying this protocol.

Children with ADHD conducted two theta/beta NF sessions. In the first half of the sessions, three NF trials (puzzles as feedback animations) were run with pre- and post-reading and picture search tasks. A significant decrease of the theta/beta ratio (TBR), driven by a decrease of theta activity, was found in the NF trials of the second session demonstrating rapid and successful neuroregulation by children with ADHD.

For pre-post comparisons, children were split into good vs. poor regulator groups based on the slope of their TBR over the NF trials. For the reading task, significant EEG changes were seen for the theta band from pre- to post-NF depending on individual neuroregulation ability. This neuroplastic effect was not restricted to the feedback electrode Cz, but appeared as a generalized pattern, maximal over midline and right-hemisphere electrodes.

Our findings indicate that short-term NF may be a valuable and economical tool to study the neuroplastic mechanisms of targeted NF protocols in clinical disorders, such as theta/beta training in children with ADHD.

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

References (24)

  • H. Gevensleben et al.

    Neurofeedback in ADHD: further pieces of the puzzle

    Brain Topogr.

    (2014)
  • H. Gevensleben et al.

    Neurofeedback in attention-deficit/hyperactivity disorder - different models, different ways of application

    Front. Hum. Neurosci.

    (2014)
  • Cited by (42)

    • The ADHD effects on partial opposites in trigonometric plots obtained from the EEG signals

      2022, Chaos, Solitons and Fractals
      Citation Excerpt :

      Some of these researchers also expressed that there is a relationship between hyperactivity and the power of the low bands (δ and θ bands) similar to the relationship between inattention and the power of the β band [7,9]. In the neurofeedback studies, these researchers also represented that a neurofeedback course based on reducing the power of the theta/beta bands can force the brain to reorganize itself for improving the ADHD symptoms [13,14]. Studies, which employed nonlinear dynamic techniques such as fractal dimension [15], correlation dimension [16,17], Lyapunov exponent [5,18], entropy [19,20] and recurrence quantification analysis [7,21,22] for analyzing the EEG walks, are the second category.

    • Neurofeedback for cognitive enhancement and intervention and brain plasticity

      2021, Revue Neurologique
      Citation Excerpt :

      It relies on humans’ learning abilities and plasticity. In fact, it has been shown that neurofeedback stimulates plasticity by activating well-known reinforcement learning networks [19,20]. The effects of neurofeedback on behaviour and on brain structures are discussed next (Fig. 2).

    • A Study on Resting EEG Effective Connectivity Difference before and after Neurofeedback for Children with ADHD

      2021, Neuroscience
      Citation Excerpt :

      All subjects were volunteers, and written informed consent was signed by children and their guardians. The theta/beta NF treatment protocol (Gevensleben et al., 2009; Van Doren et al., 2017) was provided in a standardized manner. The NF intervention was carried out by a professional psychologist who specialized in NF training.

    • The plausibility of using unmanned aerial vehicles as a serious game for dealing with attention deficit-hyperactivity disorder

      2020, Cognitive Systems Research
      Citation Excerpt :

      However, the Slow Cortical Potentials (SCP) and theta/beta ratio protocols have been the most commonly used to treat ADHD (Arns, Heinrich, & Strehl, 2014; Hammond, 2011). Theta/beta protocols are based on the finding of a stronger theta power and a weaker beta power in ADHD patients during rest with open eyes (Hobbs, Clarke, Barry, McCarthy, & Selikowitz, 2007; Van Doren et al., 2017). In this case, the main objective of NFT is to increase beta and decrease theta power.

    View all citing articles on Scopus
    View full text