Behavioral disorders in children were first described in the early 1930’s by scientists and qualified as Minimal Brain dysfunction Syndrome (MBS) in 1947 by Strauss and Lehtinen. The first attempt of medication came from Dr. Charles Bradley in 1937 who observed a dramatic dosage-dependent improvement of school-related behaviors and attentiveness after administration of amphetamine. During the 1940s and 1950s, psychometric measures began to be used to help identify the MBD disorder in children. Some of these scales are still used by clinician to evaluate evolution of ADHD-symptoms : the Weshler Intelligence Scale for Children (WISC) and its revised version (WISC-R) or the TOVA (Test of variables of Attention).
The denomination “Attention-Deficit Disorder” (ADD) appeared in the Diagnostic and Statistical Manual of the American Psychiatric Association-III in 1980. The DSM-III established 4 main categories of the disorder: ADD with or without hyperactivity, conduct disorder and learning disabilities. Each child may fall into any category, or a combination of these, which conditions the efficacy of treatment. Later, the classification of ADHD has been reviewed by scientists and three subtypes have been defined: inattentive-type (ADHD-I), hyperactivity-type or combined-type (ADHD-CT).
EEG correlates in ADHD
The first evidence of electrical brain activity abnormalities measured in electroencephalography (EEG) in MBD patients was presented in 1938 by Jasper, Solomon and Bradley who reported generalized slowing of EEG activity. Later, research findings showed differences in EEG pattern between ADHD children and normal children especially regarding frontal and central activity. The largest EEG study of ADHD to date found that children with ADHD displayed increased theta power, slight elevation in frontal alpha power and decreases in beta mean frequency (Chabot RJ 1996). More recent studies are consistent with these findings and have also reported increased frontal theta activity as well as higher theta/beta ratio (Monastra VJ 2001, Bakhshayesh AR 2011, Heinrich H 2014). In addition to these, it seems that EEG-patterns are modulated by ADHD-subtypes; Clark et al. showed that ADHD-CT exhibit more absolute and relative theta and higher theta/beta ratio than inattentive type (Clarke AR 1998) and later Heinrich observed higher upper-theta and lower-alpha in the combined type as well as higher theta/beta ratio on F3 and Fz in the inattentive group.
Changes in Event-Related Potentials and Slow Cortical Potentials (SCP) have also been reported in ADHD children with attenuation of P300 components and deviant SCP. Lubar observed significant lower amplitudes in term of P200, P300 and late component amplitudes on an oddball paradigm, as P200 were believed to be associated with stimulus selection and P300 with understanding of the stimulus (Lubar 1991). In the continuity of these studies, in 2001 Lazzaro monitored 54 unmedicated ADHD adolescents and observed enhanced P200 and reduced N200 amplitudes along with delayed N200 and P300 latencies, consistent with deficits in information processing (Lazzaro I 2001). They also observed a correlation between pre-stimulus theta activity and disturbances in ERPs suggesting that one could modulate the others.
The introduction of biofeedback in the treatment of ADHD
Preliminary findings have indicated that training individuals to control their electrical activity may have beneficial effects on reducing symptoms of ADHD. From 1973 to 1991, Lubar et al. conducted research and biofeedback experiment on hyperkinetic ADD-ADHD children (Lubar 1991) and showed that with SensoriMotor Rythms (SMR) and beta training at 16-20Hz, patients improved their focus and concentration. To this purpose, a variety of protocols has been developed to reduce ADHD symptoms by modulation of cerebral activity: theta/beta protocols consisting on inhibiting theta activity and enhancing beta activity ratio (Monastra VJ 2001, C. C. Arns M. 2013, Heinrich H 2014), SCP training (Strehl U 2006), combination of both theta/beta and SCP trainings (Monastra V.J 2002, Fuchs T 2003, Drechsler R 2007, Meisel V 2014), SMR training (Lubar 1991, Lubar JF 1995, Fuchs T 2003, Lansbergen MM 2011), beta training (Kropotov JD 2005) or upper alpha enhancing (Escolano C 2014).
Benefits of the neurofeedback
Recently reviewed (Loaiza JG 2014, Loo SK 2005, H. H. Arns M 2014), most studies exhibit reduction of ADHD symptoms after neurofeedback training (Lévesque J 2006, Bakhshayesh AR 2011, Drechsler R 2007, Leins U 2007, Gevensleben H. 2009, Heinrich H 2014) and improvement on parents and teacher’s rating scales (Kropotov JD 2005, Strehl U 2006, Leins U 2007, Gevensleben H. 2009, Arns M. 2009, Meisel V 2014). Papers also exhibit improvement on IQ scores although it is not a specific marker of ADHD. Regarding modulation of electrical activity, studies report reduction of SMR EEG power after neurofeedback sessions (D. W. Arns M 2012), increase in beta waves and inhibition of theta waves (Gevensleben H. 2009), and enhancement of relative upper alpha power in frontocentral sites (Escolano C 2014).
ERP changes have also been reported after training sessions. Later, ERP based neurofeedback protocols revealed correlation between enhanced performances on task and reduction of P300 component (Wangler S 2011), Some studies reported enhanced P300 amplitudes in a Go/Nogo task after relative beta training (Kropotov JD 2005) and significant increase in N200 and P300 amplitude after individualized neurofeedback treatment (Arns M 2012) as others observed a decrease of the P3 after neurofeedback during an Attention Network Test (ANT).
Efficacy of neurofeedback in the reduction of ADHD symptoms have sometimes been compared with effects of medication. Many studies report positive and similar effects of neurofeedback (Monastra V.J 2002, Fuchs T 2003, Duric NS 2012) compared to psychostimulant. Meisel et al. in 2014 compared the efficacy of neurofeedback and medication based on teacher and parent reports using a randomized controlled trial design. A significant academic performance improvement have been detected only in the neurofeedback group (Meisel V 2014).
Limitations and coming improvement
Although these results seems promising, most of these studies have been disputed due to the lack of scientific rigor and limitations such as lack of control groups, small number of participants, confounding of several treatment, no exclusion of patients with psychiatric or neurologic disorder, absence of blindness of the evaluators or lack of randomization assignment to groups (Micoulaud-Franchia JA 2011); only in three studies the group assignment was randomized (Heinrich H. 2004, Lévesque J 2006, Gevensleben H. 2009).
Recent studies attempt to overstep these limitations and introduce a control group experiencing a placebo training similar to the neurofeedback training but with a non EEG-synchronized feedback. These studies based on the random presentation of EEG changes exhibited significant improvement in ADHD symptoms (inattention and impulsivity) for both neurofeedback and placebo group with no significant differences between the two groups (Lansbergen MM 2011, Vollebregt MA. 2013). In what is the most methodologically rigorous study on EEG biofeedback treatment outcome, using random assignment to groups and a placebo control group with examiner blindness to treatment assignment, no compelling evidence of efficacy for EEG biofeedback was found. Biofeedback group didn’t exhibit significant better results than the control group (Fine AH 1994).
Apart from the efficacy of neurofeedback treatment, long-term effects have been examined in follow-up studies. Studies in neurofeedback training showed a significant improvement in ADHD symptoms and a modulation in cortical activity which remain effective after 6 months (Strehl U 2006, Leins U 2007, Gevensleben H 2010) or even after 2 years (Gani C 2008). Recently, Meisel et al. conducted a 2-month and 6-month follow-up study and revealed : a reduction of inattentive and hyperactive symptoms after 2 and 6 months according to mothers and teachers, a significant reduction of child’s functional impairments at the end of the neurofeedback training and after 2 months, a significant improvement in reading and writing and similar effect of neurofeedback and medication suggesting that neurofeedback could be a good alternative to medication (Meisel V 2014).
Another actual challenge is the personalization of neurofeedback protocols. Arns et al. revealed that ADHD patients presented a large variability in qEEG profiles within a “behaviorally homogenous population” with 47% of patients showing increased theta activity, only 6% showing decreased beta activity and 22% showing increased beta activity (Arns 2008). To improve efficacy of treatment, actual studies aim to adapt protocols to ADHD children regarding their EEG-patterns and adjust reward threshold of EEG-neurofeedback training to children’s performances (Lansbergen MM 2011).
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