Psychiatry Research: Neuroimaging 335 (2023) 111723

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Psychiatry Research: Neuroimaging

journal homepage: www.elsevier.com/locate/psychresns

Review article

Clinical efficacy of neurofeedback protocols in treatment of Attention

Deficit/Hyperactivity Disorder (ADHD): A systematic review
Mohammed Gamil Mohammed Saif *, Lyudmila Sushkova
Vladimir State University named after Alexander and Nikolay Stoletovs, Department of Electronics, Instrumentation and Biotechnical Systems, Vladimir, Russia

A R T I C L E I N F O A B S T R A C T

Keywords: Attention Deficit/Hyperactivity Disorder (ADHD) is a common neurodevelopmental disorder of childhood and its
Neurofeedback effects mostly continue to adulthood. Neurofeedback training has shown promising results in the treatment of
EEG ADHD. However, there is no yet consensus as to the efficacy of neurofeedback in comparison to stimulant
ADHD
medication. Despite a large number of meta-analyses and comparative reviews on the effects of neurofeedback in
Review
the treatment of ADHD, there is a lack of comparative reviews on the efficacy of neurofeedback protocols. This
SMR
TBR review aims at examining the effect of different training protocols on the efficacy of neurofeedback in the
SCP treatment of ADHD across specific research studies published between 2017 and 2022. Altogether, a total of 916
records were identified and 18 articles met the inclusion criteria. Findings show that the efficacy of different
neurofeedback protocols has been comparable to the efficacy of stimulant medications. Nevertheless, there is still
room for more clinical trials on neurofeedback protocols for ADHD since some studies suggest not using neu­
rofeedback as a stand-alone treatment for ADHD. To my knowledge, this systematic review is the first to review
neurofeedback protocols for ADHD. This study provides significant implications and directions for researchers to
conduct research, on alternatives to stimulant medications for ADHD, in the future.

1. Introduction is associated with a reduction in weight and height in children and ad­
olescents (Carucci et al., 2021). Additionally, stimulants can be inap­
Attention deficit/ hyperactivity disorder (ADHD) is considered a propriate for people with heart conditions as stimulant medications can
childhood common neurodevelopmental and psychiatric disorder lead to an increase in heart rate and blood pressure (Liang et al., 2018).
characterized by inappropriate levels of inattention, hyperactivity, and In recent years, neurofeedback has received considerable attention as an
impulsiveness (Lambez et al., 2020; Wang et al., 2021b). Effects of alternative therapy technique that can result in altering brain activation
ADHD experienced in childhood usually continue to adulthood and without applying electrical potentials or magnetic fields, or pharma­
result in educational failure, academic difficulties, and occupational and ceutical drugs (Carucci et al., 2021). There has been an increasing in­
social skills problems (Mayer et al., 2016). The global rate of prevalence terest in applying neurofeedback as an alternative or combination
of ADHD is reported around 3% for girls, and 9% for boys at school age treatment for ADHD as stimulant medications show limited effectiveness
(Arns et al., 2014a; Lambez et al., 2020). ADHD is commonly comorbid (Swanson et al., 2011). Nonetheless, there is no consensus yet, among
with other disorders, such as anxiety and depression, which make it clinicians and researchers, as to the efficacy of neurofeedback in com­
challenging for clinicians to assess and treat ADHD as the symptoms of parison to stimulant medication. In a systematic review, Moreno-García
ADHD overlap with its comorbidities (Drechsler et al., 2020). The most et al. investigated the efficacy of neurofeedback training in the treat­
common treatments for ADHD are stimulant medications, such as ment of patients with ADHD and concluded that neurofeedback pro­
methylphenidate (Krinzinger et al., 2019), behavioral therapy, and duces significant long-term improvement in symptoms of ADHD
neurofeedback training (Mayer et al., 2016). Stimulant medications seek (Moreno-García et al., 2022). On the other hand, Rahmani et al. re­
to increase tonic dopamine levels between neural cells as ADHD is ported, in a systematic review and meta-analysis, that neurofeedback
associated with a lower level of tonic dopamine (Quintero et al., 2022). has no significant impact on the core symptoms of ADHD (Rahmani
However, long-term stimulant medication, especially methylphenidate, et al., 2022a). In one of the most recent systematic reviews on the

* Correspondent author.
E-mail address: [email protected] (M.G.M. Saif).

https://doi.org/10.1016/j.pscychresns.2023.111723
Received 23 February 2023; Received in revised form 7 August 2023; Accepted 9 October 2023
Available online 11 October 2023
0925-4927/© 2023 Elsevier B.V. All rights reserved.
M.G.M. Saif and L. Sushkova Psychiatry Research: Neuroimaging 335 (2023) 111723

efficacy of neurofeedback in the treatment of ADHD patients, Lou­ as a measure for distinguishing ADHD patients (Arns et al., 2014a).
threnoo et al. suggested that future studies should focus on standard Event-related alpha, beta, and theta power are potential biomarkers of
neurofeedback protocols (Louthrenoo et al., 2022); however, no direct ADHD (Michelini et al., 2022).
comparison of different neurofeedback protocols has yet been made for
ADHD. Thus, this review synthesized research that used EEG-based 1.2. Biofeedback
neurofeedback protocols for the treatment of ADHD patients. The aim
of this review was to ascertain whether there is a possibility that Biofeedback is an approach aiming at improving the ability to self-
different protocols of neurofeedback may exhibit different levels of regulate on the basis of providing simultaneous evaluation of physio­
clinical efficacy and to examine the rationale behind the controversy logical signals during training. Neurofeedback training, which is a type
over the efficacy of neurofeedback training for the treatment of ADHD. of biofeedback, is an operant conditioning procedure based on the brain-
computer interface (BCI) (Arns et al., 2020). Neurofeedback is often
1.1. Evaluation of adhd conducted by simultaneously measuring electroencephalography (EEG),
performing online EEG analysis with the extraction of the parameters of
The diagnosis of ADHD using neurophysiological signals is still interest, assessing the current state of the brain, and then providing
challenging, as ADHD symptoms overlap with the symptoms of other real-time auditory or visual feedback to the participant (Enri­
psychiatric disorders (Weibel et al., 2020). The most common diagnostic quez-Geppert et al., 2019b; Saif et al., 2021). Mental tasks, performed to
criteria for ADHD are designed by the American Psychiatric Association voluntarily control brain activity, are usually defined based on the
(Edition, 2013). Clinical interviews and assessment of childhood and feedback information.
family history are common procedures in the diagnosis of ADHD (Jain Historically, neurofeedback can be dated back to the early 1930s
et al., 2017). Electroencephalography (EEG), which shows the func­ when it was first reported, by two French researchers, that EEG alpha
tioning of a human brain at high temporal resolution, has a controversial rhythm could be classically conditioned (Durup and Fessard, 1935). The
history as a diagnostic measure of ADHD (Drechsler et al., 2020). The first application of neurofeedback training based on sensorimotor
EEG embraces a spectrum of frequency bands such as delta (1–4 Hz), rhythm (SMR) was reported by Sterman in the 1960s (Sterman et al.,
theta (4–8 Hz), alpha (8–12 Hz), sensorimotor (SMR) frequency (12–15 1972); it was applied for the suppression of epileptic seizures. The first
Hz), beta (13–30 Hz) and gamma (30–100 Hz) (Omejc et al., 2019). EEG demonstration of the clinical effects of neurofeedback training in ADHD
of many patients with ADHD shows increased power of the theta fre­ was described in 1976 and reaffirmed in 1979 by Shouse and Lubar who
quency band and/or decreased power of the beta frequency band successfully applied neurofeedback in a child with hyperkinetic syn­
(Lenartowicz and Loo, 2014). Theta over beta ratio (TBR) has been used drome and found improvements in distractibility and hyperactivity

Fig. 1. The preferred reporting items for systematic review and meta-analysis (PRISMA) flow diagram for selected studies involving EEG-NF to treat ADHD.

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M.G.M. Saif and L. Sushkova Psychiatry Research: Neuroimaging 335 (2023) 111723

(Lubar et al., 1976). (Enriquez-Geppert et al., 2019b). Despite TBR not being a conclusive
marker for ADHD, it is a promising neuro-marker for diagnosing ADHD
2. Material and methods (Bioulac et al., 2019b). A number of TBR-based neurofeedback studies,
whose characteristics shown in Table 1, have shown reductions in ADHD
The review protocol was developed, on the basis of the review ob­ symptoms (Geladé et al., 2017; Sudnawa et al., 2018a; Cueli et al.,
jectives, to guide the literature search according to The Preferred 2019a; Wang et al., 2021a; Ghadamgahi Sani et al., 2022; Rahmani
Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) et al., 2022c; Roy et al., 2022a). Sudnawa, et al. (Sudnawa et al., 2018a)
guidelines (Page et al., 2021) as shown in Fig. 1. have applied TBR neurofeedback for the treatment of ADHD and
concluded that TBR neurofeedback was as effective as stimulant medi­
2.1. Search strategy cation in the treatment of ADHD, can be applied as an alternative
therapy to stimulant medication in ADHD. The improvements in ADHD
The search for relevant articles was performed on the electronic symptoms were assessed by parents and teachers using the Vanderbilt
databases of PubMed and Scopus. The search period was delimited from Attention-Deficit Hyperactivity Disorder Diagnostic Rating Scales. The
2017 to 2023, and the language was limited to English. The search terms 40 participants were randomly organized into a neurofeedback group
and queries were as following: ((((((("EEG neurofeedback") OR ("EEG (N = 20; age=8.4 ± 1.6 years; 2 females) and a methylphenidate group
NF")) OR (TBR)) OR (SMR)) OR (SCP)) AND NOT ("MEG neurofeed­ (N = 20; age=9.0 ± 1.5 years; 2 females). Each participant in the neu­
back")) AND NOT ("fMRI neurofeedback")) AND (ADHD); ((((((("EEG rofeedback group received 30 sessions of TBR-based neurofeedback over
neurofeedback") OR ("EEG NF")) OR (TBR)) OR (SMR)) OR (SCP)) NOT a period of 12 weeks. The methylphenidate group participants received
("MEG neurofeedback")) NOT ("fMRI neurofeedback")) AND (ADHD); doses of 5–20 mg orally twice daily over 12 weeks. The result of the
(("ADHD Neurofeedback") NOT ("MEG neurofeedback")) NOT ("fMRI study showed no significant differences in ADHD symptoms between the
neurofeedback"); (("ADHD Neurofeedback") AND NOT ("MEG neuro­ neurofeedback group and the methylphenidate group. Roy, Sumedha
feedback")) AND NOT ("fMRI neurofeedback"). et al. (Roy et al., 2022a) reported results similar to those of Sudnawa,
et al. through a TBR-based neurofeedback study, which included 30
2.3. Inclusion criteria participants as shown in table 1. On the other hand, Janssen et al.
(Janssen et al., 2020) found no evidence for the long-term specificity of
A study, published in a peer-review journal, was only included if it TBR neurofeedback in treating ADHD through a study in which 67
was an EEG-based neurofeedback intervention applied for the treatment subjects participated (see Table 1).
of ADHD. The other studies including functional magnetic resonance
imaging (fMRI), and magneto-electrography (MEG) based neurofeed­ 3.2. SCPs neurofeedback protocol for treating ADHD
back studies were excluded. Moreover, full-text screening of the studies
was carried out to ensure that they meet the criteria set as follows: (1) SPCs neurofeedback protocol is mainly applied in ADHD (Omejc
were clinical or randomized controlled trials; (2) involved EEG-based et al., 2019). SPCs represent positive or negative direct current shifts in
neurofeedback; (3) involved ADHD; (4) involved reliable assessment EEG, which are commonly recorded over the sensorimotor cortex
instrument of ADHD; (5) were published in English between 2017 and (Gevensleben et al., 2014), lasting from hundreds of milliseconds to
2023. several seconds (Arns et al., 2014b). Negative SCPs are thought to
The search for relevant studies was performed on two electronic indicate increased cortical activation, while positive SCPs may reflect a
databases as mentioned above and any duplication of studies was reduction in the firing probabilities of the underlying neural networks
removed. Following the screening of the titles and abstracts of the ar­ (Omejc et al., 2019; Arns et al., 2020). SCPs training applied for the
ticles, all studies that are not in the scope of the review, despite treatment of ADHD is aimed at increasing cortical negativity as it is
mentioning the search queries, were excluded. The full text of studies thought that patients with ADHD have reduced cortical negativity dur­
that met the inclusion criteria outlined above were then downloaded, ing cognitive preparation (Enriquez-Geppert et al., 2019b; Krepel et al.,
and carefully reviewed to ensure their relevance. If the full text of a 2020a). Mayer, et al. (Mayer et al., 2016) have applied neurofeedback of
study is not retrievable, those studies were excluded as well. This pro­ SCPs for the treatment of adults with ADHD and found that SCPs training
cess is shown in a PRISMA flow diagram in Fig. 1. resulted in symptom improvements in participants with ADHD.
Heinrich et al. (Heinrich et al., 2020) compared the effects of SCPs
3. Results and TBR neurofeedback training in 48 participants with ADHD. The
participants were randomly organized into a neurofeedback group (N =
At first, a total number of 203 records were found with PubMed, and 30; age=8–12 years; 5 females) and a control group (N = 18; 8–12 years;
713 records with Scopus. After removing duplicates, 823 records 6 females). The neurofeedback training consisted of 36 sessions, which
remained, of which only 18 publications fulfilled the set inclusion were organized into two treatment blocks of 18 units each. Half of the
criteria and were included. The 18 included studies were classified into participants began with SCP-based neurofeedback; the other half started
four groups based on the neurofeedback protocol applied for treating with TBR-based neurofeedback. In order to compare the two neuro­
ADHD symptoms. Theta/beta ratio (TBR), slow cortical potentials feedback protocols at the intraindividual level, each half of the partici­
(SCPs), and SMR neurofeedback protocols are most commonly used for pants crossed over from the neurofeedback protocol with which they
treating ADHD symptoms. started in the first block to the other neurofeedback protocol in the
second block. The effects of SCP, and TBR NF were not significantly
3.1. TBR neurofeedback protocol for treating ADHD different in reducing ADHD core symptoms. A recent study by Has­
slinger et al. (Hasslinger et al., 2022a) examined the effects of SCP
TBR neurofeedback is the most common protocol applied in ADHD neurofeedback training on cognitive functions in adolescents and chil­
(Van Doren et al., 2017; Moreno-García et al., 2022). Many research dren with ADHD (See Table 2). As a result, it was concluded that the
studies demonstrate that patients with ADHD show increased power of effect of SCP neurofeedback on cognitive functions associated with
the theta frequency band (4–7 Hz) and/or decreased power of the beta ADHD was limited.
frequency band (13 to 30 Hz) especially in the frontal and central re­
gions (Van Doren et al., 2017; Arns et al., 2020). Therefore, TBR neu­ 3.3. SMR neurofeedback protocol for treating ADHD
rofeedback is basically applied in ADHD for decreasing the power of
theta and/or increasing the power of beta frequency band SMR self-regulation training procedures have proved effective in

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M.G.M. Saif and L. Sushkova Psychiatry Research: Neuroimaging 335 (2023) 111723

Table 1
Summary of the eligible TBR-based neurofeedback studies identified during the systematic review.
Source Protocol Sample Groups (if any) NF Training NF ADHD Behavioral Results Conclusion
Duration Electrodes Assessments

(Roy et al., ↓TBR = N = 30 NF group (N = 10; age= 24 sessions of Cz Conners 3-P Significant improvements in NF can be a stand-
2022) (↓Theta / 6–12 years) 40 mins; 2 Short Scale core ADHD symptoms were alone or combined
↑Beta) B.P.T group (N = 10; sessions a observed with all 3 groups; intervention tool for
age=6–12 years) week MPH group has shown the children with ADHD
Medication group (N = greatest improvement; NF has
10; age=6–12 years; been superior for learning
meds=MPH) problems
(Rahmani ↓TBR N= First group (N ¼ 29; 30-mins Cz ADHD-RS-IV; Improvements in core ADHD NF Combined with
et al., 2022) 112 age=6–17 years; sessions over DSM-5 symptoms were observed with vitamin D3 was more
treatment=vitamin D3) 12 weeks; 2 all 3 groups. effective than each
Second group (N = 29; days a week treatment alone.
age=6–17 years;
treatment=NF+ vitamin
D3)
Third group (N = 29;
age=6–17 years;
treatment=NF)
Control group (N = 29;
age=6–17 years;
treatment=N/A)
(Ghadamgahi ↓TBR N = 40 NF group (N = 20; 20 sessions of C3/C4 DSM-5; Improvements in ADHD P-M exercises are
Sani et al., age=5–12 years) 40–45 mins; point WISC-IV symptoms were observed in more appropriate
2022) P-M exercises group (N three sessions Both NF and PM exercises option for reducing
= 20; age=5–12 years) a week. symptoms of ADHD
(Wang et al., ↓TBR N = 36 NF group (N = 22; 60 sessions of Cz DSM-IV; NF resulted in significant Children with ADHD
2021) age=8.23 ± 1.59 years) 32 mins; 2–3 SWAN improvement of ADHD differed from healthy
Control group (N = 15; times a week symptoms children in phase-
age= 8.80 ± 2.43 years) based effective
connectivity
(Janssen et al., ↓TBR N = 67 NF group (N = 24; 3 sessions of Cz DSM-IV-TR; N/A No support was found
2020) age=7–13 years) 45 mins a DBDRS; for the long-term
MPH group (N = 23; week over a WISC-III specificity of TBR
age=7–13 years); period of neurofeedback in
PA group (N = 20; 10–12 treating ADHD
age=7–13 years) months
(Cueli et al., ↓TBR N= ADHD-I group (N = 15; 36 sessions of Cz; EDAH- ADHD-C and ADHD-HI TBR NF produces
2019) 64; age=9.667±1.128 15 mins over Fp1 assessment; demonstrated greater significant
years) 3 months QEEG; TOVA improvements in ADHD improvements in
ADHD-HI group (N = symptoms than ADHD-I ADHD symptoms
11; age=9.883±1.456
years)
ADHD-C group (N = 38;
age=9.458±1.005
years)
(Sudnawa ↓TBR N = 40 NF group (N = 20; 30 sessions of Fz DSM − 5; No differences in ADHD NF is a promising
et al., 2018) age=8.4 ± 1.6 years) 30 mins over Vanderbilt baseline symptoms between alternative treatment
Medication group (N = a period of 12 assessment groups were found for ADHD in children
20; age=9.0 ± 1.5 years weeks scale
meds=MPH)
(Geladé et al., ↓TBR N= NF group (N = 39; 10–12 week, Cz DSM-IV-TR; MPH more effective than TBR TBR NF can’t be
2017) 112 age=7–13 years) 3 sessions of DBDRS; NF in improving standalone
Medication group (N = 20 mins per WISC-III neurocognitive functioning treatment in ADHD
36; age=7–13 years; week
meds=MPH)
PA group (N = 37;
age=7–13 years)

Note: NF: Neurofeedback; B.P.T: Behavioral parent training; TBR: Theta/beta ratio; Cz: Middle central electrode; DSM-5: Diagnostic and statistical manual of mental
disorders; ADHD-RS-IV: Attention deficit and hyperactivity disorder rating scale version IV; WISC-IV: Wechsler intelligence scale for children – fourth edition; P-M:
Perceptual-motor; C4: Right central electrode; C3: Left central electrode; MPH: Methylphenidate; DSM-IV: Diagnostic and statistical manual of mental disorders, 4th
edition; SWAN: Strengths and Weaknesses of ADHD Symptoms and Normal Behavior; DSM-IV-TR: Diagnostic And Statistical Manual, Fourth Edition, Text revision;
DBDRS: Disruptive behavior disorder rating scale; PA: Physical activity; TOVA: Test of variables of attention; EDAH: Experience-dependent hebbian depression; QEEG:
Quantitative electroencephalogram; FP1: Left prefrontal pole; ADHD-I: Inattentive ADHD; ADHD-HI: Hyperactive/impulsive ADHD; ADHD-C: combined ADHD; Fz:
Middle frontal electrode.

decreasing symptoms of ADHD (Omejc et al., 2019). SMR neurofeed­ sessions of 60 mins over 4 weeks. The results of the study indicated that
back targets increase the power of the SMR frequency band (Jeunet SMR neurofeedback improved bimanual coordination tasks in patients
et al., 2019). Norouzi et al. (Norouzi et al., 2018) examined the effects of with ADHD. Bioulac et al. (Bioulac et al., 2019a) compared the effects of
SMR neurofeedback training on bimanual coordination in children with SMR neurofeedback training and stimulant medication (methylpheni­
ADHD. The participants were randomly organized into a neurofeedback date) in 179 children with ADHD (See Table 3); the methylphenidate
group (N = 10; age=7.61 ± 2.1 years) and a control group (N = 10; group showed a significant reduction in ADHD symptoms more than that
age=8.09 ± 2.3 years). The neurofeedback training consisted of 40 in neurofeedback group. Similarly, Purper-Ouakil et al. (Purper-Ouakil

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M.G.M. Saif and L. Sushkova Psychiatry Research: Neuroimaging 335 (2023) 111723

Table 2
Summary of the eligible SCP-based neurofeedback studies identified during the systematic review.
Source Protocol Sample Groups (if any) NF Training NF Electrodes ADHD Behavioral Results Conclusion
Duration Assessments

(Hasslinger Two NF: N= WMT group (N 25 sessions of 60 C3 and C4 for WISC-IV; The effects of WMT on spatial No support for broad
et al., 1. SCP 202 = 51; mins; 5 sessions/ SCP; Fz and Cz WAIS-IV; and verbal working-memory effects of SCP NF and
2022) (↑Neg.) age=12.61 ± week during 5 for LZT CPT-II were superior to SCP NF, LZT, LZT on cognitive
2. LZT 2.74 years) subsequent weeks and pharmacological treatment functions associated
(QEEG) SCP NF group with ADHD
(N = 51; age=
12.35± 2.65
years)
LZT group (N =
50; age= 12.41
±2.30 years)
Phar.
Treatment (N
= 50;
age=12.21 ±
2.41 years)
(Heinrich 1. SCP N = 48 NF group (N = 36 sessions of 50 Cz FBB-HKS; Effects of SCP, and TBR NF are SCP NF was found to
et al., (↑Neg.); 30; age=8–12 min; 2–3sessions SDQ not significantly different in be superior to TBR NF
2020) 2. ↓TBR years) per week reducing ADHD core symptoms. in reducing elevated
AST control Regarding SDQ-DP, SCP NF was DP
group (N = 18; superior to TBR NF and AST
8–12 years)
(Krepel et al., 1. SCP N= SCP group (N = 20 sessions of C3, Cz, or C4 The reduction in ADHD The QEEG-informed
2020) (↑Neg.); 136 9; age= 24.9 ± 20–30 mins; 2–3 for SMR; Fz, ADHD-RS; symptoms was the same for male NF has specificity in
2.↓TBR; 14.9 years) times a week FCz, or Cz for HSDQ; vs. female, and adults vs. treating ADHD
3. ↑SMR SMR group (N TBR; Pz for SCP PSQI children, irrespective of NF symptoms, and a
= 84; age=24.9 protocol used potential to be
± 14.9 years) effectively replicated
TBR group (N
= 27; age=24.9
± 14.9 years)
Another NF
group (N = 16;
age =24.9 ±
14.9 years)

Note: Neg: negativity; LZT: Live z-score training; WMT: Working memory training; CPT-II: Conner’s Continuous Performance Test-II; WAIS-IV: Wechsler Adult In­
telligence Scale-IV; AST: Attention skills training; SDQ: Strengths and difficulties questionnaire; DP: Dysregulation profile; FBB-HKS: Fremdbeurteilungsbogen für
Hyperkinetische Störungen; ADHD-RS: ADHD Rating Scale; HSDQ: Holland Sleep Disorder Questionnaire; PSQI: Pittsburgh Sleep Quality Index; QEEG: Quantitative
Electroencephalogram.

Table 3
Summary of the eligible SMR-based neurofeedback studies identified during the systematic review.
Source Protocol Sample Groups (if any) NF Training NF Electrodes ADHD Behavioral Results Conclusion
Duration Assessments

(Norouzi ↑SMR N = 20 NF group (N = 10; 40 sessions of C3; C4 DSM-V SMR NF improved SMR NF enhances the
et al., age=7.61 ± 2.1 60 mins over 4 bimanual coordination motor control of ADHD
2018) years) weeks tasks in patients with ADHD patients
Control group (N
= 10; age=8.09 ±
2.3 years)
(Bioulac ↑SMR; N= NF group (N = 108; 36 sessions; 4 C3, Cz and C4 for K-SADS; No evidence of non- NF and MPH are no
et al., ↓TBR 179 age= 7 to 13 years) sessions per SMR; F3, Fz, F4 ADHD-RS- IV; inferiority of NF against equivalent in treating
2019) Medication group week and Cz for TBR WISC-IV; SDQ MPH in reduction of ADHD ADHD
(N = 71; age= 7 to symptoms
13 years)
(Purper- ↑SMR; N= NF group (N = 111; 32 to 40 Fpz, Fz, F3, F4, Cz, ADHD-RS-IV; MPH is more effective than NF isn’t supported to be
Ouakil ↓TBR 178 age= 10.3 ± 1.8) sessions; 4 C3, C4 and Pz SDQ; CPT NF in improving core ADHD standalone treatment
et al., Medication group sessions per symptoms for patients with ADHD
2021) (N = 67; age=9.8 ± week
1.8)

Note: K-SADS: Kiddie- Schedule for Affective Disorders and Schizophrenia for School-Age Children; MPH: Methylphenidate; SDQ: Strengths and difficulties
questionnaire.

et al., 2022) found that methylphenidate is more effective than SMR in 3.4. Other EEG-based neurofeedback protocol used in treating ADHD
improving core ADHD symptoms (See Table 3).
TBR, SCP, and SMR are well-established and called standard neu­
rofeedback protocols in treating ADHD (Van Doren et al., 2017; Omejc

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M.G.M. Saif and L. Sushkova Psychiatry Research: Neuroimaging 335 (2023) 111723

et al., 2019). Nevertheless, investigation of other possible protocols, or sessions, and session frequency. Furthermore, technical equipment and
the possibility of enhancing the performance of the standard protocols, reward systems are mostly different for different studies. The one thing
by combining them with other protocols, is of great interest in the all studies, which applied a specific neurofeedback protocol, have in
research community of neurofeedback training (Duric et al., 2017; Lee common is the EEG potentials or frequency bands they seek to reward or
and Jung, 2017; Mohagheghi et al., 2017). Pakdaman et al. (Pakdaman inhibit in ADHD patients.
et al., 2018a) compared the effects of stimulant medication (Ritalin) and
non-standard neurofeedback training in treating ADHD. 14 children 4. Discussion
participated in the study and were randomly divided into two groups:
neurofeedback with Ritalin group (N = 7; age= 7.86 ± 2.410 years; 2 The complex etiology and comorbidities of ADHD have made it
girls); neurofeedback without Ritalin group (N = 7; age=7.29± 2.215 challenging for clinicians to treat ADHD effectively using pharmaceu­
years; 3 girls). Neurofeedback training was applied to decrease the tical drugs (Drechsler et al., 2020). Neurofeedback training has received
power in delta, theta, and beta 2 frequency bands and simultaneously considerable attention as an alternative therapy for ADHD (Arnold et al.,
increase the power in the SMR frequency band. The participants 2021). Nonetheless, the efficacy of neurofeedback, being applied for the
received neurofeedback training 2 sessions of 45–60 mins per week over treatment of ADHD, is controversial in the scientific community (Omejc
6 months. The neurofeedback group showed significant improvements et al., 2019). This systematic review explores the neurofeedback pro­
in ADHD symptoms; however, the combination of Neurofeedback and tocols for ADHD with the aim to reveal the causes behind the contro­
Ritalin was more effective in reducing ADHD symptoms. Table 4 lists the versy over the efficacy of neurofeedback training for the treatment of
neurofeedback studies based on non-standard protocols used in treating ADHD. For this purpose, the selected studies in this review were
ADHD. compared in terms of details of neurofeedback protocol, and clinical
In general, the results of the included studies show that neurofeed­ outcome of the intervention.
back training, especially with standard protocols (TBR, SMR, and SCP), The selection of the appropriate protocol is the main focus of neu­
produced beneficial effects in the reduction of measured core symptoms rofeedback training as the neurofeedback effect on brain functioning
of ADHD. However, those effects of neurofeedback training were not depends mainly on the kind of protocol, and the way of its imple­
consistent across all studies; findings of some studies illustrate that TBR mentation (Enriquez-Geppert et al., 2019b). This review concluded that
neurofeedback has the potential to be a stand-alone therapy for ADHD the most common neurofeedback protocols applied for the treatment of
patients while some other studies in Table 1 do not support the sug­ ADHD include TBR, SMR, and SCP, which is consistent with existing
gestion of using TBR neurofeedback protocol as an alternative therapy literature on neurofeedback for ADHD (Enriquez-Geppert et al., 2019a;
or has no evidence on the long-term specificity of TBR neurofeedback in Arns et al., 2020; Kuznetsova et al., 2023). Arns et al. (Arns et al., 2014a)
treating ADHD. When comparing the protocol details for these studies, it claimed that TBR, SMR, and SCP protocols were well studied and
is clear that there is high heterogeneity in samples, inclusion criteria, described as "standard protocols ". However, the results of this review
electrode placement, control group, number of sessions, duration of demonstrate that each of the "standard neurofeedback protocols" is far

Table 4
Summary of the eligible another-based neurofeedback studies identified during the systematic review.
Source Protocol Sample Groups (if any) NF Training NF Electrodes ADHD Behavioral Results Conclusion
Duration Assessments

(Pakdaman ↓Theta/ N = 14 NFþRitalin 2 sessions of Cz for TBR and DSM-V; NF is efficient in improving Ritalin and NF
et al., 2018) ↑alpha; group (N = 7; 45–60 mins Theta/ SMR; Fz WISC-R; core symptoms of ADHD combination is more
↓Delta; age= 7.86 ± 2.410 per week for Delta; F3 CPT; efficient than
↓Theta/ years) over 6 and F4 for Clinical Q standalone NF in
↑SMR; NF group (N = 7; months Theta/alpha treating ADHD
↓TBR age=7.29± 2.215
years)
(Lee and ↑Beta/ N = 36 NF þMedication 2 sessions of C3; C4 DSM-IV-TR; Significant additive NF may be
Jung, 2017) ↑SMR; group (N = 18; 50 mins per CRS; ARS treatment effect of NF on the considered as a
↓Theta; age=8.72 ± 2.42 week over ADHD symptoms was found possible effective
↓ high beta years) 2.5 months and a reduction of theta treatment for
Medication waves was recorded in NF children with ADHD
group (N = 18; condition participants
age=8.78 ± 1.83
years)
(Mohagheghi ↓Theta/ N = 60; 40 sessions FP1; FP2; F7; CPRS-R; The both NF protocols have Alpha enhancement
et al., 2017) ↑alpha; age= 7 N/A of 45 min; 3 F3; Fz; F4 CPT-II; comparable effect on clinical protocol was more
↓TBR to 10 sessions per K-SADSPL; symptoms of ADHD effective in
years week ARS; DSM-5 suppressing
omission errors
(Duric et al., SMR/beta N = 130 NF group (N = 42; 30 sessions; Cz Barkley Significant ADHD core Combined MPH and
2017) (alpha age=11.4 ± 3.1 3 times a teacher and symptom improvements were NF showed 6-month
stimulatio- years) week parents; DSM- reported 6 months after efficacy in ADHD
n); NFþ Medication IV; WISC-IV; treatment completion in all treatment
↑Beta/ group (N = 44; ICD-10 three groups, with marked
↓theta age=11.2 ± 2.8 improvement in inattention
years) in all groups
Medication
group (N = 44;
age= 10.9 ± 2.4
years)

Note: WISC-R: Wechsler intelligence scale for children-revised; CPT: Conner’s continuous performance task; CRS: Conners behavior rating scale; ARS: ADHD rating
scale; CPRS: Conners’ parent rating scale; CPT-II: Conners’ continuous performance task II; K-SADSPL: Schedule for affective disorders and schizophrenia for school
aged children present and lifetime version; CPRS-R: Revised conners’ parent rating scale; ICD-10: International classification of disease.

6
M.G.M. Saif and L. Sushkova Psychiatry Research: Neuroimaging 335 (2023) 111723

away from being standardized; this finding complies with existing behavioral therapy.
literature, indicating that the standard neurofeedback protocols have This review has a number of limitations to be acknowledged. First, all
been applied differently in different studies (Hasslinger et al., 2022b; non-English publications were excluded, which increased the risk of
Moreno-García et al., 2022). The comparison of the protocol details in missing important relevant articles. Second, although the included
this review shows that each "standard protocol" is standardized only in studies were divided into four groups based on the neurofeedback pro­
terms of the targeted EEG potential or frequency band. TBR neuro­ tocol applied as an intervention, the studies in each group were too
feedback protocol is aimed at modulation of theta/beta frequency heterogeneous to perform meta-analysis; they differ in inclusion criteria
bands; SMR targets sensorimotor frequency; SCP is aimed at modulating and characteristics of the participants, equipment used for EEG
slow cortical potentials. The other parameters of the standard protocols recording, duration of neurofeedback training, control group, evalua­
are, non-standardized, often selected by the reasoning of a clinician. tion instruments and measures of statistical analyses. Finally, the au­
Therefore, there is a lack of uniform standards with respect to training thors of the included studies have not been contacted for seeking
courses for neurofeedback. clarification on whether there is a misinterpretation of their studies in
The comparison of the main findings of the studies reviewed in this this review.
review shows that there is no consensus on the efficacy of so-called
"standard neurofeedback protocols" in comparison to stimulant medi­ 5. Conclusion
cation and the other types of control such as cognitive behavioral
therapy. While some studies support applying neurofeedback training as There has been an increasing interest in applying neurofeedback as
a stand-alone treatment for ADHD (Sudnawa et al., 2018b; Roy et al., an alternative or combination treatment for ADHD as medications and
2022b), some other studies suggest combining neurofeedback and behavioral therapy both show limited effectiveness. Despite an
stimulant medications or vitamin D3 (Pakdaman et al., 2018b; Rahmani increasing number of research projects and publications on neurofeed­
et al., 2022b). As it is shown in Table 1, despite some studies applying back training applied for the treatment of ADHD in the last ten years,
the same neurofeedback protocols, their findings are varied and con­ there is still no consensus on the efficacy of the intervention as is
tradictory. Such contradictory findings agree with contradictory find­ demonstrated in this systematic review. The selection of the appropriate
ings of the most recent meta-analyses and reviews, investigating the protocol is the main focus of neurofeedback training as the neurofeed­
efficacy of neurofeedback in ADHD (Lee et al., 2022; Rahmani et al., back effect on brain functioning depends mainly on the kind of protocol
2022a; Kuznetsova et al., 2023). The quality of the studies included in and the way of its implementation. Based on the articles reviewed, the
these meta-analyses and reviews may be the reason for the contradiction most common neurofeedback protocols applied for the treatment of
in their findings. ADHD are TBR, SMR, and SCP. Nonetheless, there is a lack of uniform
The reasons behind contradictory findings of studies of comparable standards with respect to training courses for neurofeedback therapy,
quality can be attributed to a number of factors. First of all, ADHD is not which results in controversy over the efficacy of neurofeedback applied
the same for all patients, and it can be inattentive (ADHD-I), hyperac­ for the treatment of ADHD.
tive/impulsive (ADHD-HI), or combined (ADHD-C); and the effect on
neurofeedback training significantly differs with the type of ADHD Ethics approval
(Cueli et al., 2019b). Consequently, the application of the same neuro­
feedback protocol, which is common practice among researchers and Not applicable.
clinicians as it is shown in Tables 1-4, for all patients with ADHD may
result in the failure of neurofeedback in improving the symptoms of
Funding
ADHD. Therefore, the individualized neurofeedback protocol, which is
adapted to the specific profile of each patient based on their individual
Not applicable.
baseline QEEG, may be more appropriate. QEEG-informed selection of
an appropriate individualized neurofeedback protocol for treating
ADHD was effectively applied by Arns et al. (2012). The clinical effec­ Declaration of Competing Interest
tiveness of QEEG-informed neurofeedback was replicated successfully
by Krepel et al. (2020b). Also, the review study by Garcia Pimenta et al. I confirm that there is no conflict of interest associated with this
(2021) demonstrated that the efficacy of personalized neurofeedback in publication, and there has been no financial support for this work that
ADHD was superior to non-personalized neurofeedback. Furthermore, could have influenced its outcome.
the review by Núñez-Jaramillo et al. (2021) recommended the person­
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