A Randomized Controlled Trial to Examine the Posttreatment Efficacy of Neurofeedback,Behavior Therapy,and Pharmacology on ADHD Measures

Abstract

Objective: To examine the efficacy of neurofeedback (NF), behavior therapy (BT), and pharmacology (PH) on the improvement of ADHD-related symptoms. Method: Fifty-nine children with ADHD (M = 8.80 years, SD = 1.92 years) were randomly assigned to one of the three treatments in a pre/post assessment design. Mother- and teacher-rated ADHD scales and children were assessed using The Integrated Visual and Auditory Continuous Performance Test (IVA/CPT). Results: The three treatments were effective on the IVA/CPT, but with different trends. BT and especially NF achieved improvement on response control and attention, and PH mainly in visual attention. On the rating scales, BT improved all measures, and NF and PH had a minor but interesting influence. Conclusion: From a global perspective, behavior therapy had the most extensive results, but PH had the greatest capacity to improve overall attention. NF was able to improve both control response and inattention. Clinical implications are discussed.

Keywords

randomized controlled trial neurofeedback pharmacological treatment behavior therapy ADHD

ADHD is one of the most common neurodevelopmental disorders during childhood and adolescence. With a worldwide prevalence of approximately 5%, ADHD severely affects schooling, family, and social life, and is characterized by symptoms such as inattention, hyperactivity, and impulsiveness (American Psychiatric Association, 2013). Pharmacological treatment is the option that is usually recommended in these cases. However, parents, children, and doctors often resist the use of stimulant medications due to their potential to cause adverse effects (Peterson, McDonagh, & Fu, 2008).

Empirical studies have generally compared the efficacy of pharmacological treatment with other therapy options. So, Leung and Hung (2008), for instance, indicated in their study that the combination of methylphenidate and behavioral therapy was significantly more effective in reducing ADHD symptoms than pharmacological treatment alone. Eiraldi, Mautone, and Power (2012) later corroborated these findings.

The National Institute of Mental Health (NIMH)-funded Multimodal Treatment of Attention Deficit Hyperactivity Disorder study (MTA) found that symptoms normalized in 68% of children treated with both stimulant medications and behavioral interventions (Lofthouse, Arnold, Hersch, Hurt, & deBeus, 2012). Thus, a combined application of both is recommended, especially for school-age children with the combined ADHD subtype (Murray et al., 2008) as well as when the characteristic symptoms and impairment of the child’s general functioning are severe (National Institute for Health & Clinical Excellence, 2008).

Regarding nonpharmacological interventions in the treatment of ADHD, such as psychological interventions, Fabiano et al. (2009) and Willis, Weyandt, Lubiner, and Schubart (2011) showed that behavioral therapy (applied as parent training or classroom management) is viable and effective in ADHD treatment. Hodgson, Hutchinson, and Denson (2012) replicated and expanded the Fabiano et al. (2009) meta-analysis, comparing the efficacy of seven nonpharmacological interventions including behavioral modification, neurofeedback (NF), school programs, and parent training. They concluded that such treatments have considerable potential in the treatment of children with ADHD. More specifically, the meta-analysis of Coates, Taylor, and Sayal (2015) suggested that parenting interventions for ADHD are effective.

Various studies, including randomized controlled trials and meta-analyses, have examined the efficacy of neurofeedback as a viable option for treating ADHD in relation to pharmacological treatment, and the results to date have been promising (Arns, de Ridder, Strehl, Breteler, & Coenen, 2009; Arns, Heinrich, & Strehl, 2014; Duric, Assmus, Gundersen, & Elgen, 2012; Leins et al., 2007; Lofthouse et al., 2012). In a randomized controlled trial, neurofeedback training was found to be superior to computerized attention skills training (Gevensleben et al., 2009). Duric et al. (2012) found in a controlled and randomized clinical trial that neurofeedback treatment seemed to improve the core symptoms of ADHD, as assessed by parental reports. When neurofeedback was administered in conjunction with pharmacological treatment, the originally prescribed medication dose was observed to decrease (Lora & Moreno, 2011), while Meisel, Servera, Garcia-Banda, Cardo, and Moreno (2013) showed that effects were maintained for 6 months following treatment. Moreno-Garcia, Delgado-Pardo, Camacho-Vara de Rey, Meneres-Sancho, and Servera-Barceló (2015) showed that neurofeedback, pharmacological treatment, and behavioral therapy are effective and cause similar effects as represented in a specific electroencephalographic measure (theta/beta ratio).

However, conclusions about the effectiveness of neurofeedback, especially compared with the most commonly accepted treatments (pharmacology [PH] and behavior therapy [BT]), remain controversial. For example, in their respective revisions, Pigott and Cannon (2014) concluded that neurofeedback is a useful treatment in place of stimulant medication and behavior therapy as first-line treatments, while Loo and Makeig (2012) only recognized that in recent years, despite the considerable growth in the number and quality of research reports on neurofeedback, the studies reviewed did not yet support this treatment as a first-line, stand-alone modality. In a similar vein, the Society of Clinical Child and Adolescent Psychology considers neurofeedback to be at Level 3, as a “possibly efficacious treatment” of ADHD (Evans, Owens, & Bunford, 2014). Therefore, many more studies are needed to know whether neurofeedback can level up.

One of the main methodological issues encountered when comparing the effectiveness of these treatments could be the use of different measures of ADHD symptoms. Rating scales for parents and teachers have been the most common procedure and often the only one used. However, it seems advisable to add at least some neuropsychological task. For example, the Integrated Visual and Auditory Continuous Performance Test (IVA/CPT; Sandford & Turner, 2002) has been used to define attention and behavior problems by comparing children with a diagnosis of ADHD with children with no history of the disorder (Moreno-García, Delgado-Pardo, & Roldán-Blasco, 2015) and to evaluate the efficacy of neurofeedback (Moreno, Delgado, Aires, & Meneres, 2013; Yan et al., 2008).

In the aforementioned context, the purpose of this study was to compare the differential efficacies of neurofeedback, pharmacological intervention, and behavior therapy in the reduction of ADHD symptoms as measured by rating scales and neuropsychological variables. The specific objectives included the following: (a) determine the ability of neurofeedback, behavior therapy, and pharmacological treatment to reduce ADHD symptomatology using computerized (IVA/CPT) assessment tools and rating scales administered to parents and teachers; and (b) compare the effects of neurofeedback versus behavior therapy and pharmacological treatment on attentional and behavioral variables from three independent sources of information: children with a diagnosis of ADHD, parents, and teachers.

Method

Participants

In the screening phase, 146 children with ADHD were recruited from the pediatric primary care units of Sevilla South Sanitary District (Seville, Spain). Of these children, 35 declined to participate, and 52 were excluded for not meeting the inclusion criteria (see Figure 1): (a) being between 7 and 14 years old, (b) presenting a score above the 90th percentile on the teacher version of the ADHD Rating Scale–IV (ADHD RS-IV) and above the 80th percentile on the parent version, (c) patients being drug naïve before the first consultation, (d) presenting no evidence of psychiatric disability or mental retardation (Kauffman Brief Intelligence Test), (e) presenting no comorbid disorders with ADHD (Child Behavior Checklist, CBCL), and (f) having no patient past or present medical illness or chronic medical condition that could contraindicate pharmacological treatment.

Figure 1.

Distribution of study participants.

The remaining 59 children were randomized to one of the conditions of administered treatments. During treatment two children dropped out. Therefore, 57 children completed the study (19 in each of the three treatment conditions). The Human Research Ethics Committee of the University of Seville previously approved this investigation, and informed consent was obtained in all cases. Table 1 contains the participants’ descriptive data.

Table 1.

Participant Demographic and Clinical Characteristics.

	Neurofeedback group(N = 19)	Behavioral group(N = 19)	Pharmacological group(N = 19)
Age (M ± SD)	9.21 ± 1.9	8.11 ± 1.3	9.21 ± 2.2
% Sex (boys/girls)	79/21	74/26	79/21
Clinical presentation DSM-5 (N)
Combined presentation	7 (36.84%)	5 (26.31%)	8 (42.10%)
Inattentive presentation	8 (42.10%)	11 (57.89%)	8 (42.10%)
Hyperactive–impulsive presentation	4 (21.05%)	3 (15.78%)	3 (15.78%)
IQ (K-BIT)* (M ± SD)
Crystallized (verbal)	106.79 ± 12.8	100.81 ± 12	101.70 ± 12.5
Fluid (nonverbal)	101.93 ± 11.8	97.94 ± 17.7	93.3 ± 10.8
IQ composite	103.36 ± 13	96.94 ± 14.5	94.70 ± 12.9

Note. Diagnostic and Statistical Manual of Mental Disorders (5th ed.; DSM-5; American Psychiatric Association, 2013).

Intelligent Quotient from Kaufman Brief Intelligence Test.

Materials and Procedure

IVA/CPT

This tool evaluates attention and control of responses to auditory and visual stimuli (Sandford & Turner, 2002). The results are presented in standardized coefficients with an average score of 100 and a standard deviation of 15. We analyzed three global scales related to response control (Full Scale Response Control, Auditory Response Control, and Visual Response Control), along with three others also related to attention (Full Scale Attention, Auditory Attention, and Visual Attention). We also analyzed the primary care scales (with both auditory and visual stimuli) related to response control and attention. Scales pertaining to response control include Prudence (commission errors), Consistency (ability to respond reliably based on reaction time), and Stamina (ability to sustain response speed by comparing the mean reaction time of the first 200 vs. the last 200 trials). Scales pertaining to attention include Vigilance (omissions), Focus (reaction time variability), and Speed (hits reaction time).

ADHD RS-IV

Mothers and teachers competed the ADHD RS-IV, which consists of 18 items comprising two subscales, inattention and hyperactivity-impulsivity, and a total score (DuPaul, Power, Anastopoulos, & Reid, 1998). Higher scores are indicative of more ADHD-related problems.

Attention Deficit Disorders Evaluation Scale (ADDES)

Parents were asked to complete this scale individually to enable a more extensive evaluation of inattentive and hyperactive/impulsive symptoms than can be acquired using just the ADHD RS-IV scale (McCarney & Arthaud, 2004).

Procedure

We designed the study as an open randomized controlled group with pre- and posttreatment phases. Participants were randomly assigned to three experimental conditions corresponding to administered treatments (neurofeedback, behavioral therapy, and pharmacology) and were evaluated with the same instruments and under identical conditions before and after the therapeutic intervention. Pretreatment evaluation was conducted approximately 1 week before treatment began, and posttreatment evaluation was conducted after the intervention was complete in all cases, that is, after 20 weeks of intervention. In no cases were other treatments concurrently administered.

Treatment groups

NF

This treatment was conducted using The Atlantis II® (Brainmaster Technologies, Inc.; Bedford, Ohio, USA), with an impedance check (below 5 Kohms) that automatically controls artifacts (>120 microvolts). Electroencephalogram (EEG) was analyzed in two frequency bands (theta = 4-7 Hz, beta = 15-20 Hz). EEG recordings were obtained using the unipolar signal Cz for participants between the ages of 7 and 11, and for older participants, EEG recordings used the monopolar signal FCz, based on the international 10-20 system with ear references. Following the guidelines for the recommended treatment program (Monastra et al., 2005), participants received four theta/beta training sessions per week for a total of 40 sessions, wherein each session consisted of six 4-min runs. At the beginning of each session, baseline values were determined (30 s). Each session began with an introductory period (2-5 min) for the purpose of getting familiar with the procedure. Later, periods of training and EEG feedback, with an initial duration of 120 s, were developed, which increased according to the learning curves of each child. Participants were rewarded for being below the threshold 70% of the time in theta and up to 20% of the time in beta.

Behavioral therapy

Participants assigned to the behavioral therapy group received an intervention consisting of parent training that included 10 group sessions, teacher training that included five training sessions, and individualized child treatment that included 15 sessions of cognitive therapy. Each child session lasted 50 min. Parents participated in weekly 90-min sessions based on the Parent Training Program (Barkley, 1987). Each 90-min teacher group session focused on two aspects, training on behavior modification strategies in the classroom (three sessions) and specific curricular adaptations for ADHD (two sessions; Eiraldi et al., 2012). Teachers and parents received advice on implementing and reinforcing the behavior strategies acquired at home and at school.

Pharmacological treatment

Participants assigned to the pharmacological treatment group received the ADHD treatment prescribed by the pediatrician who conducted their follow-up during the referenced 20 weeks. Pharmacological intervention has been adjusted to a common action protocol, which included an analytical, physical, and neurological examination, somatometry and an initial assessment of the intensity of ADHD symptoms prior to treatment, as well as periodical dosage revisions and recorded side effects. All patients in this group received methylphenidate in its different formulations (immediate, intermediate release, or osmotic controlled release oral system, OROS).

Data Analysis

With regard to the first objective, which focused on the therapeutic change induced by the different treatments separately in relation to the two evaluation periods (pre- and posttreatment), a comparison of means was conducted for related groups (paired samples t test), and in absence of the required assumptions, Wilcoxon t tests were applied. For the second objective, where the differential efficacy of the three therapeutic options was examined, we utilized ANOVA (single factor ANOVA) with subsequent post hoc contrasts between treatments. We used Bonferroni correction to control the alpha error. When the required model assumptions were unmet, we applied Welch’s test or the nonparametric Kruskal–Wallis test.

As a measure of the efficacy of each treatment, the difference between the pre- and posttreatment means (the “change” variable) was used, and effect sizes (Cohen’s d) were calculated. Thus, results were generated from comparing and contrasting three treatments (NF, BT, and PH) × three sources of information (children, mothers, and teachers) × three different instruments: IVA/CPT, ADHD RS-IV, and ADDES.

Results

Comparing Pre- and Posttreatment Assessments

Table 2 contains the pre–post differences in IVA/CPT variables separately for each therapeutic condition.

Table 2.

Pre–Post Comparison of the IVA/CPT Measures in Each Treatment.

Measures	Pretreatment		Posttreatment		t	d
Measures	M	SD	M	SD	t	d
Neurofeedback
FS_RC	98.15	8.72	103.61	10.03	−2.50*	0.69
A_RC	101.57	11.88	108.35	11.65	−2.94*	0.78
V_RC	94.84	11.73	102.23	10.59	−3.73**	1.03
PR_A	103.85	11.21	108.14	8.34	−2.18*	0.58
PR_V	98.92	12.63	105.15	12.22	−2.81*	0.78
CON_A	97.28	13.23	101.28	15.56	−2.12	0.56
CON_V	93.23	13.33	101.53	11.40	−2.39*	0.66
STA_A	101.50	20.27	111.42	13.42	−2.95*	0.78
STA_V	98.38	13.49	104.84	16.49	−2.50*	0.69
FS_AT	92.30	13.37	95.92	15.21	−2.27*	0.63
A_AT	93.78	17.38	97.92	20.55	−2.15	0.57
V_AT	92.76	10.98	98.38	10.61	−2.91*	0.80
VIG_A	88.92	19.50	92.85	20.83	−1.77	0.47
VIG_V	92.12	12.54	97.30	14.12	−2.34*	0.63
FOC_A	92.00	11.85	101.14	14.55	−3.30**	0.88
FOC_V	92.76	9.24	99.07	6.33	−3.20**	0.89
SPE_A	107.78	15.04	111.35	13.81	−2.20*	0.58
SPE_V	99.46	12.73	102.38	12.56	−3.01	0.83
Pharmacology
FS_RC	95.75	21.19	106.00	7.46	−1.78	0.63
A_RC	87.70	23.71	101.70	19.68	−2.47*	0.78
V_RC	100.12	16.03	107.37	6.86	−1.96	0.69
PR_A	90.30	22.56	105.50	15.50	−3.41**	1.07
PR_V	94.87	12.02	100.62	9.22	−1.67	0.59
CON_A	95.75	11.58	100.75	12.33	−1.93	0.68
CON_V	79.70	19.62	95.30	13.82	−3.13	0.99
STA_A	109.87	25.26	116.12	17.78	−1.88	0.66
STA_V	107.4	25.50	109	23.49	−0.44	0.14
FS_AT	74.87	22.85	99.87	19.35	−4.78**	1.69
A_AT	76.55	25.07	100.55	24.86	−4.96***	1.65
V_AT	80.50	17.18	102.12	13.89	−3.35*	1.18
VIG_A	59.90	35.70	92	27.75	−4.44**	1.40
VIG_V	84.20	18.56	95	15.32	−2.93*	0.92
FOC_A	92.12	15.31	103.5	9.94	−1.86	0.65
FOC_V	73.37	22.39	97.87	17.82	−3.20**	1.14
SPE_A	101.00	9.14	112.2	11.47	−2.78*	0.88
SPE_V	92.87	7.77	104.25	11.18	−2.43*	0.86
Behavior therapy
FS_RC	97.40	16.62	102.00	13.78	−2.20	0.69
A_RC	89.40	15.76	100.46	15.92	−4.35***	0.95
V_RC	100.5	18.29	105.00	13.96	−1.58	0.49
PR_A	99.33	15.96	108.53	12.59	−2.59*	0.67
PR_V	101.80	17.24	109.40	10.33	−1.76	0.55
CON_A	82.06	16.36	92.26	16.24	−3.64**	0.94
CON_V	103.8	13.25	107.30	11.88	−2.48*	0.78
STA_A	96.80	15	105.20	17.07	−3.21**	0.83
STA_V	94.90	17.37	97.60	15.32	−1.71	0.54
FS_AT	84.40	15.98	92.30	16.30	−2.29*	0.72
A_AT	74.53	20.66	88.13	21.66	−3.46**	0.89
V_AT	92.60	11.94	99.30	10.70	−2.09	0.66
VIG_A	69.42	9.40	90.35	21.11	−2.69*	0.72
VIG_V	100.8	15.02	107.50	10.73	−2.57*	0.81
FOC_A	87.13	18.09	96.93	16.32	−3.26**	0.85
FOC_V	95.10	10.88	101.90	6.83	−1.79	0.56
SPE_A	100.66	14.50	103.60	12.65	−2.10	0.50
SPE_V	86.90	6.83	93.20	14.77	−2.69*	0.85

Note. d = Cohen’s effect size. IVA/CPT = Integrated Visual and Auditory Continuous Performance Test; FS_RC = Full Scale Response Control; A_RC = Auditory Response Control; V_RC = Visual Response Control; PR_A = Auditory Prudence; PR_V = Visual Prudence; CON_A = Auditory Consistency; CON_V = Visual Consistency; STA_A = Auditory Stamina; STA_V = Visual Stamina; FS_AT = Full Scale Attention; A_AT = Auditory Attention; V_AT = Visual Attention; VIG_A = Auditory Vigilance; VIG_V = Visual Vigilance; FOC_A = Auditory Focus; FOC_V = Visual Focus; SPE_A = Auditory Speed; SPE_V = Visual Speed.

p ≤ .05. **p ≤ .01. ***p ≤ .001.

When analyzing the performance of children treated by NF on the IVA/CPT, we found significant differences in 15 of 18 measures. Improvement was similar for both visual (all the measures) and auditory stimuli (all except three, two of which had p = .05). Children showed significant improvement on all global measures (except for Auditory Attention, p = .05). Effect sizes were large for four visual measures (Visual Response Control, Visual Focus, Visual Speed, and Visual Attention) and one auditory measure (Auditory Attention). Most of the remaining effect sizes were medium. In summary, NF generated improvement on almost all the IVA/CPT measures with a larger average global effect size (d = 0.80). Overall, effects sizes ranged from 0.47 to 1.03.

When analyzing the effects of PH treatment on the IVA/CPT, we found significant differences in 11 of the 18 measures, with large or very large effect sizes. Children significantly improved on all Attention Global Scales, but only on one Response Control Global Scale (Auditory). In addition, we found significant differences in auditory stimuli but not visual for four variables: Response Control, Prudence, Stamina, and Vigilance. Differences were found in both visual and auditory stimuli on Full Scale Attention, Focus, and Speed. Therefore, two results should be highlighted: First, improvements in response control were only significant for auditory stimuli, and second, improvements in attention ability were more extensive (for auditory and visual stimuli) and relevant. As shown in Table 2, the average effect size for attention was very large (d = 1.42), while for response control, the average was medium (d = 0.73).

When analyzing the effects of BT treatment on the IVA/CPT, we also found significant differences in 11 of 18 measures. The improvements in Global Scales were for Auditory Response Control and Auditory Attention, although improvements were also significant for Full Scale Attention (p = .047). It is noteworthy that significant differences were found on all the primary scales with auditory stimuli (except for Focus, p = .054). However, this was the case only for three measures with regard to visual stimuli. As shown in Table 2, the average effect size for behavior therapy was d = 0.75 (medium), and slightly larger for attention variables (d = 0.77) than for behavior variables (d = 0.72).

Table 3 shows pre–post differences in mother and teacher ADHD measures separately for each therapeutic condition.

Table 3.

Pre–Post Comparisons of ADHD Rating Scales in Each Treatment.

	Neurofeedback (N = 19)						Pharmacology (N = 19)						Behavior therapy (N = 19)
	Pre		Post		T	d	Pre		Post		t	d	Pre		Post		t	d
	M	SD	M	SD	T	d	M	SD	M	SD	t	d	M	SD	M	SD	t	d
ADHD RS-IV mothers’ report
HI	17.43	4.98	14.21	6.77	2.08	0.59	12.40	8.69	8.80	5.82	1.25	0.42	15.38	6.66	9.94	5.42	3.43**	0.76
IN	17.64	4.63	15.86	6.81	1.01	0.34	19.30	5.41	14.40	3.83	2.11	0.85	19.75	5.07	14.31	6.41	3.46**	0.64
TS	35.07	8.18	30.07	13.05	1.62	0.43	31.70	13.30	23.20	9.64	1.72	0.55	35.13	11.08	24.25	1.22	3.75**	0.70
ADHD RS-IV teachers’ report
HI	17	9.09	10.86	8.35	3.15*	1.34	9.83	7.88	6.83	4.57	1.16	0.37	12.10	7.53	12.10	7.53	3.61**	0.74
IN	20.43	4.89	14.14	5.30	2.33	0.94	17.50	8.09	15.67	4.03	0.58	0.22	13.90	5.19	13.90	5.19	3.46**	1.54
TS	37.43	9.55	25	12.83	3.11*	1.21	27.33	14.80	22.50	7.06	0.95	0.31	26.00	11.90	26.00	11.90	3.88**	1.11
ADDES mothers’ report
HI	47.38	20.86	38.63	19.42	2.20*	0.58	33.55	22.22	21.00	20.01	2.44*	0.71	44.94	28.38	30.63	24.22	3.21**	0.79
IN	54.25	14.90	45.63	16.29	2.29*	0.61	50.91	14.43	38.09	21.61	2.49*	0.72	55.88	20.90	36.25	20.29	2.93***	0.73

Note. RS-IV = Rating Scales–IV; HI = hyperactivity/impulsivity; IN = inattention; TS = total score; ADDES = Attention Deficit Disorders Evaluation Scale.

After NF treatment, significant differences were observed in five of eight measures. Teachers perceived improvements in hyperactivity, inattention, and total score with large effect sizes. Instead, there were no significant differences on the parent form of the ADHD RS-IV, and the significant differences found on the ADDES were associated with medium effect sizes for both hyperactivity and inattention subscales.

Using the ADHD RS-IV scales, no significant differences were found in the mother and teacher reports of children who received PH treatment. However, significant differences were observed on ADDES mothers scales, with medium effect sizes.

After BT treatment, significant differences were observed on all teacher and parent measures. In particular, large effect sizes were found on attention and total score teacher measures. The remaining measures yielded effect sizes equal to or higher than 0.64.

Between-Treatment Comparisons Based on Pre–Post Changes

For the second objective, the results of the intertreatment comparisons based on ANOVA showed that there have not been significant differences among the three treatments on the parent and teacher rating scales. Instead, significant differences were found on six of nine variables measured by the IVA/CPT (see Table 4).

Table 4.

Post Hoc Comparisons Between Treatments on IVA/CPT Variables.

Change variable	Treatments	M difference	SE	p	95% CI	d
Full Scale Attention	NF vs. PH	−21.38	4.64	.001	[9.56, 33.20]	2.09
	NF vs. BT	−4.28	4.34	.998	[−15.34, 6.78]	0.50
	PH vs. BT	17.10	4.90	.005	[4.62, 29.57]	1.47
Auditory Attention	NF vs. PH	−19.85	5.40	.002	[−33.44, .6.7]	1.80
	NF vs. BT	−9.45	4.69	.156	[−21.27, 2.35]	0.76
	PH vs. BT	10.40	5.33	.177	[−3.00, 23.80]	0.75
Visual Attention	NF vs. PH	15.63	5.22	.017	[2.32, 28.94]	1.19
	NF vs. BT	−1.08	4.89	1.00	[−13.54, 11.37]	0.12
	PH vs. BT	14.55	5.51	.041	[0.49, 28.60]	1.03
Auditory Vigilance	NF vs. PH	23.12	7.93	.019	[3.13, 43.11]	1.00
	NF vs. BT	−10.22	7.38	.525	[−28.82, 8.36]	0.96
	PH vs. BT	−33.35	8.06	.001	[−53.66, 13.04]	1.07
Visual Vigilance	NF vs. PH	−19.19	6.09	.011	[−34.67, 3.70]	1.19
	NF vs. BT	−0.78	5.55	1.00	[−14.90, 13.33]	0.10
	PH vs. BT	18.40	6.30	.020	[2.39, 34.42]	1.07
Auditory Speed	NF vs. PH	−7.62	3.33	.084	[−16.00, .74]	0.84
	NF vs. BT	0.63	2.99	1.00	[−687, 8.15]	0.18
	PH vs. BT	8.26	3.28	.050	[0.009, 16.52]	0.97

Note. d = Cohen’s effect size; IVA/CPT = Integrated Visual and Auditory Continuous Performance Test; CI = confidence interval; NF = neurofeedback; PH = pharmacology; BT = behavior therapy.

The results revealed that treatments differed significantly only on the variables related to attention (not in response control), and these differences are quite favorable to PH intervention. Then, as observed in Table 4, the post hoc analysis performed with Bonferroni correction at a confidence level of .05 indicates that PH treatment was superior to NF and BT on Full Scale Attention, Auditory Attention, and Visual Vigilance and was superior to BT on Visual Attention. BT was superior to NF on Full Scale Attention and Auditory Attention, and was superior to PH only on Vigilance Auditory. NF was superior to PH in Visual Attention and Vigilance Auditory. Post hoc differences did not reach significance for Auditory Speed, but PH was superior to NF and BT with large effect sizes, which was similar to those found on the aforementioned measures.

Discussion

The first objective of this study was to determine the differential efficacy of neurofeedback, pharmacology, and behavior therapy on ADHD neuropsychological measures and parent/teacher rating scales. In relation to this objective, we can conclude that the three treatments were separately able to generate changes and improvements on most of the measures. Regarding neurofeedback and methylphenidate, data are consistent with those obtained by Fuchs, Birbaumer, Lutzenberger, Gruzelier, and Kaiser (2003), and we can now add the positive data pertaining to behavior therapy. However, the scope of these improvements varied according to how efficacy was assessed (inattention or hyperactivity/impulsivity measured by the IVA/CPT or rating scales) and the source of information obtained (mothers or teachers).

In terms of a child’s performance on the IVA/CPT task, the three treatments may be considered relatively effective with similar effect sizes, but they also may include some different trends. Thus, coinciding with Arns et al. (2009), neurofeedback improves response control (impulsivity) and attention, although the improvement is greater when the child responds to visual stimuli, as deBeus and Kaiser (2011) noted previously. Instead, the effect of pharmacological treatment can especially be observed on attention symptomatology, regardless of the type of stimulation used. However, there is a differential effect on response control (i.e., hyperactivity/impulsivity behaviors) depending on the type of stimulation presented, and a greater response inhibition was observed when children were asked to respond to auditory stimuli. These results are consistent with findings from Fuchs et al. (2003) and Duric et al. (2012), although the data now come from a randomized trial.

Regarding behavior therapy, findings are particularly relevant because it is not a treatment usually proposed for improving neuropsychological measures. The results show a therapeutic success similar to the response control and attention variables, particularly with auditory stimuli. Effect sizes were slightly lower than those for pharmacology, and they were similar to neurofeedback.

The ADHD primary symptomatology assessed by the parent and teacher scales was also significantly improved for the three treatments, although behavioral therapy was appreciably superior.

The effects of neurofeedback can mainly be observed on hyperactive/impulsive symptomatology. In comparison with previous studies, the effect sizes for both hyperactive–impulsive as well as attention symptoms were closer to those found in Leins et al. (2007). When the sources consulted were parents, results obtained were similar to Gevensleben et al. (2009), but they were different from those found in other studies (Duric et al., 2012). Compared with Leins et al. (2007), neurofeedback yielded better results when the teacher provided the information. The effects of pharmacological treatment have been relevant to mother’s inattention measures and on the ADDES hyperactivity subscale, but teachers have shown no improvement. Therefore, to some extent, neurofeedback and pharmacology showed similar results, as in the Duric et al. (2012) study, but the superiority of neurofeedback on teacher forms of the ADHD measures should be highlighted. Finally, behavior therapy showed a significant improvement on all rating scales, once again demonstrating its effectiveness on such ADHD measures (Coates et al., 2015; Fabiano et al., 2009; Hodgson et al., 2012; Willis et al., 2011).

The second objective of this study was to compare the improvement of posttreatment change among the three treatments. There were no significant differences on rating scales or in response control, but pharmacology was quite superior in attention ability measured by IVA/CPT: Its improvement was larger than BT and/or NF on five variables (not influenced by the type of stimulus presented). Neurofeedback and behavior therapy were only able to be superior in two and three measures, respectively.

The main implications of these findings are clinical: Pharmacology, behavior therapy, and neurofeedback can be effective in improving ADHD primary symptomatology, but with differential effects. Our data are quite consistent with previous studies, and neurofeedback was able to improve attention, hyperactivity, and impulsivity measures, especially with visual stimuli and on teacher rating scales. Meanwhile, pharmacology was particularly powerful in improving attention ability and attention behaviors on the mothers’ rating scales. However, its effects are quite lower for response control and hyperactivity. By contrast, the effect of behavior therapy is more widespread among all the measures used. As it might be expected, the intervention improves all inattention and hyperactivity rating scale measures. However, and perhaps more surprisingly, it also has positive effects on response control and attention abilities.

Therefore, from a global point of view, we could consider that behavior therapy has the most desirable results (although it can be promptly surpassed on some measures by the other two treatments). According to Pfiffner, Villodas, Kaiser, Rooney, and McBurnett (2013), the strategies that are currently applied at school for ADHD are not based on scientific evidence, as they do not consider the cognitive limitations from which these students suffer. The application of these strategies is not systematic enough to consolidate therapeutic effects despite evidence of the need for interventions that promote self-control. The results found in this study support the combined treatment of ADHD with systematic behavioral training for parents and teachers as the main axis, and depending on the characteristics of each case, we have the power of pharmacology to improve overall inattention and the neurofeedback capacity to also improve control response in cognitive tasks.

Moreover, results from another implication can also be highlighted from the results on educative practice. The findings of this study suggest that adults must provide aural instructions to guide the child’s performance and behavior because as can be noted, aural stimulation improves a child’s attention to the task and helps reduce errors of omission. In response control, only measures based on auditory stimuli have been improved by pharmacology. Therefore, more emphasis should be placed on the assessment and intervention of auditory stimuli in ADHD.

The main limitations of this study are as follows: (a) Samples were too small to rely on statistical significance, although the results based on effect sizes could reasonably compensate for this fact; (b) a similar study should be performed on different ADHD subtypes because this variable can have a decisive influence; (c) greater control of comorbid symptoms of ADHD participants would also be highly desirable; and (d) follow-up studies are necessary to properly analyze treatment effects.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research study has been funded by Plan Nacional i+d+i (National Research, Development and Innovation Program; PSI2008–06008-C02–01).

Author Biographies

Inmaculada Moreno-García, PhD, is a senior lecturer from the Department of Personality and Psychological Assessment and Treatment, at the University of Seville. His research focuses on treating disorders of children and adolescents, specifically behavioral therapy and neurofeedback applied to ADHD and behavioral disorders.

Susana Meneres-Sancho, BSc in Psychology, PhD, MD, is a researcher at University of Seville and an expert in early childhood intervention. Her investigation comprises childhood psychopathology, especially in ADHD treatment.

Carlos Camacho-Vara de Rey, PhD, is a senior lecturer from the Department of Experimental Psychology at the University of Seville. His active research fields are: Applied Statistics in Psychology and Social Sciences, Multilevel Regression, Structural equation models and Dynamic models (System dynamics).

Mateu Servera, PhD, is a senior lecturer from the Department of Psychology at the University of the Balearic Islands (UIB). His teaching and research focuses on childhood psychopathology, especially ADHD in relation to improving its conceptualization and diagnosis through clinical scales and neuropsychological tasks.

References

American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Publishing.

Arns

de Ridder

Strehl

Breteler

Coenen

(2009). Efficacy of neurofeedback treatment in ADHD: The effects on inattention, impulsivity, and hyperactivity. A meta-analysis. Clinical EEG and Neuroscience, 40, 180-189. doi:10.1177/155005940904000311

Arns

Heinrich

Strehl

(2014). Evaluation of neurofeedback in ADHD: The long and winding road. Biological Psychology, 95, 108-115. doi:10.1016/j.biopsycho.2013.11.013

Barkley

R. B.

(1987). Defiant children: A clinician manual for parent training. New York: Guilford Press.

Coates

Taylor

J. A.

Sayal

(2015). Parenting interventions for ADHD: A systematic literature review and meta-analysis. Journal of Attention Disorders, 19, 831-843. doi:10.1177/1087054714535952

deBeus

Kaiser

D. A.

(2011). Neurofeedback with children with attention-deficit hyperactivity disorder: A randomized double-blind placebo-controlled study. In Coben

Evans

J. R.

(Eds.), Neurofeedback and neuromodulation techniques and applications (pp. 127-152). London, England: Academic Press.

DuPaul

Power

T. J.

Anastopoulos

A. D.

Reid

(1998). ADHD-Rating Scales DSM-IV for parents and teachers. New York, NY: Guilford.

Duric

N. S.

Assmus

Gundersen

Elgen

I. B.

(2012). Neurofeedback for the treatment of children and adolescents with ADHD: A randomized and controlled clinical trial using parental reports. BMC Psychiatry, 12, Article 107. doi:10.1186/1471-244X-12-107

Eiraldi

R. B.

Mautone

J. A.

Power

T. J.

(2012). Strategies for implementing evidence-based psychosocial interventions for children with attention-deficit/hyperactivity disorder. Child and Adolescent Psychiatric Clinics of North America, 21, 145-159. doi:10.1016/j.chc.2011.08.012

10.

Evans

S. W.

Owens

J. S.

Bunford

(2014). Evidence-based psychosocial treatments for children and adolescents with Attention-Deficit/Hyperactivity Disorder. Journal of Clinical Child & Adolescent Psychology, 43, 527-551. doi:10.1080/15374416.2013.850700

11.

Fabiano

G. A.

Pelham

W. E.

Coles

E. K.

Gnagy

E. M.

Chronis-Tuscano

O’Connor

B. C.

(2009). A meta-analysis of behavioral treatments for attention-deficit/hyperactivity disorder. Clinical Psychology Review, 29, 129-140. doi:10.1016/j.cpr.2008.11.001

12.

Fuchs

Birbaumer

Lutzenberger

Gruzelier

J. H.

Kaiser

(2003). Neurofeedback treatment for attention-deficit/hyperactivity disorder in children: A comparison with methylphenidate. Applied Psychophysiology Biofeedback, 28, 1-12. doi:10.1023/A:1022353731579

13.

Gevensleben

Holl

Albrecht

Vogel

Schlamp

Kratz

. . . Heinrich

(2009). Is neurofeedback an efficacious treatment for ADHD? A multisite, randomized controlled clinical trial. The Journal of Child Psychology and Psychiatry, and Allied Disciplines, 50, 67-768. doi:10.1111/j.1469-7610.2008.02033.x

14.

Hodgson

Hutchinson

A. D.

Denson

(2012). Non-pharmacological treatments for ADHD: A meta-analytic review. Journal of Attention Disorders, 18, 275-282. doi:10.1177/1087054712444732

15.

Leins

Goth

Hinterberger

Klinger

Rumpf

Strehl

(2007). Neurofeedback for children with ADHD: A comparison of SCP and theta/beta protocols. Applied Psychophysiology & Biofeedback, 32, 73-88. doi:10.1007/s10484-007-9031-0

16.

Lofthouse

N. L.

Arnold

L. E.

Hersch

Hurt

deBeus

(2012). A review of neurofeedback treatment for pediatric ADHD. Journal of Attention Disorders, 16, 351-372. doi:10.1177/1087054711427530

17.

Loo

S. K.

Makeig

(2012). Clinical utility of EEG in Attention-Deficit/Hyperactivity Disorder: A research update. Neurotherapeutics, 9, 569-587. doi:10.1007/s13311-012-0131-z

18.

Lora

J. A.

Moreno

(2011). Neurofeedback and its contributions to the treatment of Attention Deficit-Hyperactivity Disorder (Case Studies. Libro de Resúmenes IX Congreso Nacional de Psicología Clínica). San Sebastián: Asociación Española de Psicología Conductual.

19.

McCarney

S. B.

Arthaud

T. J.

(2004). Attention Deficit Disorders Evaluation Scale (3rd ed.). Colombia, MO: Hawthorne Educational Services, Inc.

20.

Meisel

Servera

Garcia-Banda

Cardo

Moreno

(2013). Neurofeedback and standard pharmacological intervention in ADHD: A randomized controlled trial with six-month follow-up. Biological Psychology, 94, 12-21. doi: 10.1016/j.biopsycho.2013.04.015

21.

Monastra

V. J.

Lynn

Linden

Lubar

J. F.

Gruzelier

LaVaque

T. J.

(2005). Electroencephalographic biofeedback in the treatment of attention-deficit/hyperactivity disorder. Applied Psychophysiology Biofeedback, 30, 95-114. doi:10.1007/s10484-005-4305-x

22.

Moreno

Delgado

Aires

Meneres

(2013). Administering the CPT/IVA to evaluate the effects of neurofeedback in ADHD. Anuario de Psicología Clínica y de la Salud, 9, 49-50.

23.

Moreno-García

Delgado-Pardo

Roldán-Blasco

(2015). Attention and Response Control in ADHD. Evaluation through Integrated Visual and Auditory Continuous Performance Test. Spanish Journal of Psychology, 18, 1-14. https://dx-doi-org.web.bisu.edu.cn/10.1017/sjp.2015.2

24.

Moreno-García

Delgado-Pardo

Camacho-Vara de Rey Meneres-Sancho

Servera-Barceló

(2015). Neurofeedback, pharmacological treatment and behavioral therapy in hyperactivity: Multilevel analysis of treatments effects on electroencephalography. International Journal of Clinical and Health Psychology, 15, 217-225. doi:10.1016/j.ijchp.2015.04.003

25.

Murray

D. W.

Arnold

Swanson

Wells

Burns

Jensen

. . . Strauss

(2008). A clinical review of outcomes of the multimodal treatment study of children with attention-deficit/hyperactivity disorder. Current Psychiatry Report, 10, 424-431.

26.

National Institute for Health & Clinical Excellence. (2008). Attention deficit hyperactivity disorder (ADHD) (NICE Guideline No. CG72). London, England.

27.

Peterson

McDonagh

M. S.

(2008). Comparative benefits and harms of competing medications for adults with attention-deficit hyperactivity disorder: A systematic review and indirect comparison meta-analysis. Psychopharmacology, 197, 1-11. doi:10.1007/s00213-007-0996-4

28.

Pfiffner

L. J.

Villodas

Kaiser

Rooney

McBurnett

(2013). Educational outcomes of a collaborative school-home behavioral intervention for ADHD. School Psychology Quarterly, 28, 25-36. doi:10.1037/spq0000016

29.

Pigott

H. E.

Cannon

(2014). Neurofeedback in the best available first-line treatment for ADHD: What is the evidence for this claim? NeuroRegulation, 1, 4-23. doi:10.15540/nr.1.1.4

30.

Sandford

J. A.

Turner

(2002). Integrated visual and auditory continuous performance test manual. Richmond, VA: Brain Train.

31.

C. Y.

Leung

P. W.

Hung

S. F.

(2008). Treatment effectiveness of combined medication/behavioural treatment with chinese ADHD children in routine practice. Behaviour Research and Therapy, 46, 983-992. doi: 10.1016/j.brat.2008.06.007

32.

Willis

W. G.

Weyandt

L. L.

Lubiner

A. G.

Schubart

C. D.

(2011). Neurofeedback as a treatment for ADHD: A systematic review of evidence for practice. Journal of Applied School Psychology, 27, 201-227. doi:10.1080/15377903.2011.590746

33.

Yan

Wang

Liu

Zong

Jiao

Yue

. . . Liu

(2008). Designing a brain-computer interface device for neurofeedback using virtual environments. Journal of Medical and Biological Engineering, 28, 167-172.