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 PMC9120321
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Cogn Neurodyn. 2022 Jun; 16(3): 531–544.

Published online 2021 Dec 2. doi: 10.1007/s11571-021-09732-8
PMCID: PMC9120321
PMID: 35603045

Sensorimotor rhythm neurofeedback training relieves

anxiety in healthy people
Shuang Liu,1 Xinyu Hao,1 Xiaoya Liu,1 Yuchen He,1 Ludan
Zhang,1 Xingwei An,1 Xizi Song,1 and Dong Ming 1,2

Author information Article notes Copyright and License

information PMC Disclaimer

Associated Data
Supplementary Materials

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Abstract
Timely relief of anxiety in healthy people is important, but there is
little research on this topic at present. Neurofeedback training
allows subjects to regulate their specific brain activities
autonomously and thus alter their corresponding cognitive
functions. Inattention is a significant cognitive deficit in patients
with anxiety. Sensorimotor rhythm (SMR) was reported to be
closely related to attention. In this study, trainability, frequency
specificity, and brain-behavior relationships were utilized to
verify the validity of a relative SMR power protocol. An EEG
neurofeedback training system was developed for alleviating
anxiety levels in healthy people. The EEG data were collected from
33 subjects during SMR up-training sessions. Subjects attended six
times neurofeedback training for about 2 weeks. The feedback
value of the neurofeedback group was the relative SMR power at
the feedback electrode (electrode C3), while the feedback values
for the control group were pseudorandom numbers. The
trainability index revealed that the learning trend showed an
increase in SMR power activity at the C3 electrode, confirming
effects across training. The frequency specificity index revealed
only that SMR band activity increased significantly in the
neurofeedback group. The brain-behavior relationships index
revealed that increased SMR activity correlated negatively with
the severity of anxiety. This study indicates that neurofeedback
training using a relative SMR power protocol, based on activity at
the C3 electrode, could relieve anxiety levels for healthy people
and increase the SMR power. Preliminary studies support the
feasibility and efficacy of the relative SMR power protocol for
healthy people with anxiety.

Supplementary Information

The online version contains supplementary material available at

10.1007/s11571-021-09732-8.
Keywords: Neurofeedback, Sensorimotor rhythm, EEG, Anxiety
 Go to:

Introduction

Anxiety disorders are the most prevalent mental disorders and

are associated with immense healthcare costs and a high burden
of disease (Lu et al. 2017). Continued excessive worry, difficulty
concentrating, sleep abnormalities, emotional lability, fatigue, and
restlessness are significant clinical manifestations in patients with
anxiety (Blaskovits et al. 2017). In the light of large population-
based surveys, up to 33.7% of the population are affected by
anxiety disorders during their lifetime in the twenty-first century
(Bandelow and Michaelis 2015). Only one out of six (16%)
patients with anxiety received effective treatment, owing to the
limitations of maladaptive cognitive and behavioral therapy
(Jonge et al. 2017; Weerdmeester et al. 2019). Thus, a better
understanding of interventions clinically that ameliorate anxiety
and stress is urgently needed, given their negative consequences
on human health (Danielsson et al. 2012). Healthy people who are
in a high level of stress and anxiety for a long time may lead to
anxiety disorders or other symptoms (Wells and Matthews 2006;
Wiseman et al. 2015). Hence, timely intervention to treat anxiety
in healthy people is a promising and possible way to reduce the
prevalence of anxiety disorders.

There are two conventional treatment modalities in clinical

psychiatry: pharmacological treatment and psychotherapy.
Pharmacological treatment employs drugs to reduce psychiatric
symptoms, and its effectiveness varies across disorders and
medications with adverse outcomes, such as dry mouth, headache,
or nausea, which can hamper the quality of life (Cheon et al. 2015;
Damsker et al. 2009). Another conventional treatment modality is
psychotherapy, which shows empirical effectiveness, although
there is some difficulty in verifying the effectiveness through
experimental studies (Schueller et al. 2017; Cuijpers et al. 2008).
However, the era of the ‘quantified self’ is upon us (Lupton 2016).
In the field of medicine and mental health treatment, people have
become increasingly interested in self-monitoring technology in
recent years. (Piwek et al. 2016; Schueller et al. 2017;
Weerdmeester et al. 2019; Yetisen et al. 2018). To enhance
treatment effectiveness and address the limitations of
conventional treatment modalities, many complementary
treatments have been proposed, of which neurofeedback is one of
the most sophisticated methods (Cheon et al. 2015).

The ability for training to control brain electrical activity has been
demonstrated since 1960 (Kamiya 1968, 1969). Owing to its
excellent temporal resolution (milliseconds or less) (Sitaram et
al. 2016; Thibault et al. 2015), electroencephalography (EEG)
biofeedback, known as EEG neurofeedback has been utilized to
make some improvements in some disorders (Bonnet et al. 2017;
Coben et al. 2010; Micoulaud-Franchi et al. 2015; Nigro 2019; Yan
et al. 2019); it is a therapeutic technique in which subjects are
tasked with regulating their brain activity autonomously
(Johnston et al. 2010; Maurizio et al. 2014; Nazari et al. 2011;
Thibault et al. 2015). In clinical, EEG neurofeedback has been used
in attention deficit and hyperactivity disorders (Arns et
al. 2009, 2014; Gevensleben et al. 2009), depressive disorders
(Choi et al. 2011; Hammond 2005a), anxiety disorders
(Hammond 2005b), and sleep disorders (Arns and
Kenemans 2012; Cortoos et al. 2010).

The sensorimotor rhythm (SMR) training protocol is known to

enhance attention which emerges when one is motionless yet
remains attentive and is suppressed by movement in the human
brain recorded over central scalp regions. (Lubar and Lubar 1984;
Pfurtscheller 1981; Reichert et al. 2016; Sterman et al. 1970). It
has a frequency range of 12–15 Hz and it has also been proven to
be an effective frequency with benefit for anxiety but not widely in
clinical due to its long duration, slower effects, and individual
difference (Gadea et al. 2020; Gomes et al. 2016; Gruzelier 2014b;
Reichert et al. 2016; Ros et al. 2009). A large body of literature
showed that the SMR neurofeedback training reduces inattentive
and hyperactive/impulsive symptoms in attention-deficit
hyperactivity disorder (ADHD) children clinically (Enriquez-
Geppert et al. 2019). Studies suggest that increasing SMR activity
voluntarily employing neurofeedback training (NFT) has also
positive effects on the attentional performance of healthy subjects
(Egner and Gruzelier 2004; Vernon et al. 2003). One possible
reason is that the circuitry of SMR is a thalami-cortical, bottom-up
mechanism, and the SMR neurofeedback training acts within the
inhibitory mechanism of the thalamic circuitry. Driven by the
increase in SMR, it improves the body's inhibition ability and
reduces the interference of somatosensory information (Egner
and Gruzelier 2004; Reichert et al. 2016). There is another reason
that the improvements in ADHD symptoms following the SMR
training might be the result of the vigilance stabilization mediated
by the regulation of the locus coeruleus noradrenergic system of
which activation has been shown to impact the sleep spindle
circuitry (Sinha and Saurabh 2011). The SMR training increases
sleep spindle density and improve sleep quality in healthy adults
and ADHD patients trained with the SMR protocol showed
decreased sleep onset latency and improved sleep quality
responsible for the improved inattention (Arns et al. 2014;
Enriquez-Geppert et al. 2019; Schabus et al. 2014; Veen et
al. 2010).

Studies have shown that training aspects of attention can relieve

anxiety (e.g., yoga, meditation) (Kiken et al. 2015; Shreve et
al. 2020; Simon et al. 2020; Wuthrich et al. 2021). Besides,
inattention is one of the clinical manifestations of anxiety
(Blaskovits et al. 2017). It was hypothesized that improving
attention-related SMR activity alleviates anxiety. In most cases,
the SMR training protocol clinically used as feedback value to
relieve anxiety is absolute power (Gomes et al. 2016;
Gruzelier 2014a, 2014b; Ros et al. 2009). However, absolute
power is affected confounded by scalp thickness and electrical
resistance (Allen et al. 2004; Knyazev et al. 2004). To decrease
data variability and better reflect cortical activity (Allen et
al. 2004; Cook et al. 1998; Knyazev et al. 2004), the relative power
value was proposed and used as the feedback value aim to
increase SMR power designed to ease anxiety in a healthy
population.

Concerning the reliability of NFT effects, trainability,

independence, and interpretability first proposed by Zoefel in
2011 were three parameters for optimal research by which to
validate the efficacy of NFT (Zoefel et al. 2011). In that case, these
three parameters include effects concerning the EEG observed at
all and expectations as well as significant behavioral impact. A
change in the targeted band caused by NFT was defined as
trainability. If the trainability is successful, the frequency
specificity as we called independence in this study, which is to
reflect the target frequency band, not other frequency bands of
the neurofeedback group has to be assessed. Finally,
interpretability namely brain-behavior relationships indicating
that the targeted band was generated and was related to reliable
behavioral effects need to be determined.

In this study, we proposed the relative power as the feedback

value to increase the subjects’ SMR power and developed an
individual adaptive training system based on EEG neurofeedback
to alleviate anxiety in healthy people. The three parameters
mentioned above were utilized to validate training effects in
treating healthy people with anxiety during the SMR up-training.
Go to:

Materials and methods

Subjects

A total of 33 right-handed adults (sixteen men and seventeen

women, [mean ± standard deviation (SD) age, 22.21 ± 1.60 years]),
without any history of neurological illness or psychiatric
disorders, were recruited from Tianjin University in this study. A
single-blind placebo-controlled design was applied in which
subjects were randomly assigned to the neurofeedback groups
(seven men and ten women, mean age = 23.07 years, SD = 1.77,
range 20–26), who were treated using feedback from electrode C3
(Gruzelier 2014b) in a relative SMR power protocol or the control
group (ten men and six women, mean age = 21.88 years, SD = 1.36,
range 18–24), who were treated using feedback from
pseudorandom numbers. All subjects were informed about the
procedure of the experiment before EEG data recording and
signed a consent form in advance; five of the subjects had had
neurofeedback relaxation training over a year previously (two of
the five subjects were in the neurofeedback group and three in the
control group in this study). They all received a small financial
remuneration after completing the experiment. There were no
significant differences between groups in the Gender, Age, and
Self-Rating Anxiety Scale (SAS). The experimental protocol was
approved by the Ethics Committee of Tianjin Anding Hospital.

Neurofeedback system design

The system is mainly composed of three parts: an EEG acquisition

module, a feature extraction module, and a feedback module. The
neurofeedback system is shown in Fig. 1.
Fig. 1
Visual neurofeedback experimental system based on brain-computer interface

Acquisition module

Each subject was seated comfortably in a chair about 65 cm away

from a 23.5-inch LCD screen; EEG signals were acquired by a 64-
channel SynAmps2 system (Neuroscan, Australia) with standard
Ag/AgCl electrodes placed on the scalp according to the
international 10–20 system. The reference electrode was located
at the right mastoid and the ground electrode was placed on the
forehead. The impedance for all electrodes was kept below 10 kΩ.
The sampling rate was 1000 Hz.
Feature extraction module

For the preprocessing, the EEG raw data were varied with
reference to binaural averaging and downsampled at 500 Hz. To
filter out baseline drift, power line interference, and high-
frequency noise, an online band-pass filter between 0.5 and 50 Hz
and a 50 Hz notch filter were enabled in the amplifier (Wang et
al. 2019). In this study, we implemented an independent
component analysis filter using the EEGLAB toolbox in MATLAB
2016b. The neurofeedback interface was written using MATLAB
2016b and Java Script. The neurofeedback training focused on
increasing the relative SMR power referred to electrode C3 as a
feedback electrode. The power spectrum estimation method used
in this study was Welch algorithm spectral with a 3 s Hamming
window, 50% overlapping, and was zero-padded to 512 points
(Akbar et al. 2016; Feng et al. 2010). We used a Welch algorithm
to decompose EEG data to the following frequency bands: delta
(0.5–4 Hz), theta (4–8 Hz), alpha (8–12 Hz), SMR (12–15 Hz), beta
(15–30 Hz), and gamma (30–45 Hz) (Mirifar et al. 2017). Then we
calculated the power value of each frequency band. The overall
process of Welch spectrum estimation is to segment the EEG data
firstly, then calculate the power spectrum of each data segment,
and finally calculate the average power spectrum of all data
segments in which data segments are allowed to overlap, and
perform windowing operation on each data segment. The data
with a total length of N is divided into K segments (overlapped),
and the length of each segment is L. The calculation formula is as
follows:

Pω=1k∑i=1k⎛⎝1LV∣∣∣∣∑n=1lω(n)xi(n)e−jwn∣∣∣∣2⎞
⎠
1
where the power of the ω(n): V=1L∑Ln=1|ω,(,n,)|2

Feedback module

During online training, EEG data were online filtered from

blinking artifacts (through the independent component analysis
filter) and visual feedback was then displayed every 2 s on the
LCD screen in the form of a sunset video. Linear mapping was
used to convert between the relative SMR power and the sunset
video progress. Subjects were not given any instruction in how to
control the feedback screen but were only told to stay mentally
focused and physically relaxed. They were not given any mental
strategy, nor were they aware of the EEG-trained parameter
(Ioannides 2018). No additional information was displayed during
training. Subjects were instructed to let the sunset video play for
as long as possible. The relative SMR power value was calculated
based on the following formula (Finnigan and Robertson 2011;
Reichert et al. 2015; Wang et al. 2013):

Pr(SMR)=Pa(SMR)Pa(total bandwidth)
2

where Pr = relative power; Pa = absolute power; total bandwidth =

0.5–45 Hz.

Experimental design

Figure 2a illustrates the experimental paradigm procedure. The

severity of anxiety was evaluated using the SAS at the beginning
and the end of the experiment (about 10 days apart) (Olatunji et
al. 2006). The neurofeedback group underwent six times
neurofeedback training (a single training every other day) for
about 2 weeks (Quaedflieg et al. 2016), all in the same period
(Fig. 2b). Figure 2c illustrates a single neurofeedback training. The
duration of a single training was 42 min, comprising an 8-min
resting-state period, a 2-min baseline trial, six 4-min feedback
trials, and a second 8-min resting-state period.
Fig. 2
Experimental design. a The SAS was used at the beginning and the end of the
experiment (which intervened about 2 weeks). b , c The neurofeedback group
underwent a total of six times neurofeedback training (one every other day), which
were composed of two resting-state periods (8 min each), a baseline, and six
training trials (4 min each) namely a session. d Resting-state was recorded as a
block of eight one-minute periods following an ‘OCCOCOOC’ sequence of eyes-open
and eyes-closed states (where ‘O’ = eyes-open and ‘C’ = eyes-closed).

Neurofeedback procedure
Resting-state
The resting-state measurement in this study used an “OCCOCOOC”
sequence (“O” = “open eyes”; “C” = “closed eyes”) for a total of
8 min since the EEG signals are more affected by blinking when
the eyes are open and more stable when the eyes are closed and
resting (Adolph and Margraf 2017). During the resting-state, the
subjects wore headphones; they kept their eyes open when a
prompt tone was played to indicate “Please open your eyes,” and
closed their eyes when the prompt tone indicated “Please close
your eyes.” The details are shown in Fig. 2d.
Baseline and trial

A 2-min baseline and six 4-min trials are under the online
feedback module. A 2-min baseline was recorded, in which the
subjects saw the screen and were instructed to relax without
trying to control the feedback screen voluntarily. The baseline
data recorded was used to calculate an individual threshold. There
are 60 relative SMR values in the 2 min baseline as 2 s is a sample.
The minimum value of relative SMR power at baseline was the
individual threshold of that day. The individual threshold did not
adjust at the beginning of each trial. The sunset video started
playing when the feedback value exceeded the individual
threshold. Otherwise, the screen displayed the initial image of the
sunset video. During each trial, when the feedback value exceeded
80% of the previous one, the current threshold was increased by
one. By contrast, when the feedback value was less than 20% of
the former, the current threshold was reduced by one. The sunset
video was presented on an LCD screen: the progress of the video
linearly corresponds to the relative SMR power. Subjects were
instructed to try their best to let the sun sink as low as possible.

Offline EEG processing

The EEG data were cleaned of artifacts using a three-step

procedure. Initially, the reference was varied and downsampling
was conducted in the same way as in online EEG processing. A
Butterworth filter was used to filter the EEG data between 0.5 and
50 Hz. Then the EEG data were carefully inspected for the
presence of artifacts, such as eye blinks, eye movements, and body
movements. We applied an independent component analysis filter
in MATLAB 2016b to remove the eye blinking component. Finally,
we computed the power values for each epoch in the bands 4 to
30 Hz, which were commonly not affected by ocular and muscular
artifacts (Delorme et al. 2007).

Self-rating anxiety scale

The SAS is a self-reported questionnaire that contains 20 items to

assess the intensity of anxiety. Each question gives a choice of four
answers (each scoring 1 to 4 points). The SAS score is used to
determine whether a subject has minimal (20–39 points), mild
(40–49 points), moderate (50–59 points), or severe (60–80
points) anxiety (Tao and Gao 1994). The test–retest-reliability in
the SAS score (r = 0.760, p < 0.01) has also been examined.

Statistical analysis

Tiredness is a largely unrecognized feature of neurofeedback

learning. Gruzelier et al. (2014) mentioned that subjects reported
tiredness after a 15-min SMR protocol session (Gruzelier 2014b).
In this study, as a result of the 24-min SMR training, the second
resting-state period in a single training did not reflect the training
effect well; therefore, we only analyzed the first resting-state
period. The first resting-state period of the six times
neurofeedback training was defined as resting 1 to resting 6.
Baseline, trial, and session are all defined in the same way. For
each subject, the SMR power at the feedback electrode (C3) was
calculated for the first resting-state, baseline, trial, session of each
training. Moreover, the power values were processed by the min–
max normalization, and outliers at any electrode were removed
(White and Thomas 2005). All data were analyzed and eliminated
 by the Kolmogorov–Smirnov test and triple standard difference
method using SPSS (Version 20.0. Armonk, NY: IBM Corp.2011)
and MATLAB 2016b.

Concerning this study on healthy people with anxiety, data

analysis excluded those pre-SAS values above 40, including one in
the neurofeedback group and one in the control group. We also
excluded subjects who may have an impact on the results due to
events or physical conditions during training, including three in
the neurofeedback group and two in the control group. Thus, the
final sample for the EEG analysis and SAS scale consisted of 26
subjects (i.e. the neurofeedback group: 13, the control group: 13).

1. Trainability is reflected by the trend of the SMR power over

training days. SMR power at the C3 electrode in resting-state was
tested. To assess trainability, repeated measures analysis of
variance (ANOVA) was performed, with two within-subject factors
of Group (neurofeedback group and control group) and Time
(resting 1 to resting 6), which used Greenhouse–Geisser’s degrees
of freedom correction for violations of the sphericity assumption
(as indicated by significant Mauchly s test of sphericity) and Least
—Significant Difference (LSD)'s corrected probability values (p-
values) for post-hoc comparisons. If trainability was successful,
the frequency specificity, as well as the effect on the behavioral
level of the neurofeedback training, were assessed.
2. In the neurofeedback group, we determined whether only the
SMR frequency band was significantly increased. To assess
frequency specificity, resting 1 and resting 6 were collapsed
within four frequency bands (theta (4–8 Hz), alpha (8–12 Hz),
SMR (12–15 Hz), beta (15–30 Hz)) across subjects and compared
using a paired t-test. Statistical significance was assumed at the
0.05 alpha level (two-tailed).
3. To judge whether the intervention training affects the emotional
experience, the raw scores of the SAS scale were utilized before
and after training in two groups, respectively, using a paired t-
test. Then, we assessed brain-behavior relationships, and the
Spearman correlation was calculated between the change in SMR
power and the change in symptoms of anxiety (SAS score).

Go to:

Results

Demographics for both groups are given in Table Table1.1. There

were no significant differences between groups in sex and age (p
> 0.05). Repeated measures ANOVA did not reveal significant main
effects of Group (neurofeedback group and control group) and
Time (baseline 1 to baseline 6) on SMR power or relative SMR
power at C3 (SMR power (Group: F(1, 24) = 1.794, p > 0.05; Time:
F(5, 20) = 0.446, p > 0.05); Relative SMR power (Group: F(1, 24) =
0.727, p > 0.05; Time: F(5, 20) = 0.437, p > 0.05). Furthermore,
there was no significant interaction between Time and Week
(SMR power: F(5, 20) = 0.946, p > 0.05; Relative SMR power: F(5,
20) = 1.003, p > 0.05). Note that preliminary analysis (independent
samples t-tests and repeated measures ANOVA) revealed no
differences in behavioral parameters and electrophysiological
parameters between the neurofeedback group and the control
group.

Table 1
Demographic variables of the subjects in this study

Neurofeedback Control
Neurofeedback vs.
group group
control, p
n = 13 n = 13
Sex (male:female) 4:9 7:6 0.234
Age, years (mean ±
22.38 ± 1.71 22.08 ± 2.15 0.917
SD)
SAS scale (mean ±
28.85 ± 4.22 29.23 ± 5.18 0.837
SD)
Open in a separate window
Trainability

As depicted in Fig. 5, the averaged SMR power across all subjects

during six times neurofeedback training at the C3 electrode in the
resting-state was calculated, demonstrating that the SMR power
increased in the neurofeedback group but that there was no
upward trend in the control group. Repeated measures ANOVA
revealed a significant interaction between Group (neurofeedback
group and control group) and Time (resting 1 to resting 6) on
SMR power at C3. Furthermore, a significant simple effect of Time
by Group in the neurofeedback group was found. Also, the results
revealed a significant simple effect of Group by Time. LSD post-
hoc comparisons revealed the SMR power at C3 in resting 6 was
higher than resting 1, resting 2, and resting 4 of the
neurofeedback group and the control group is higher than the
neurofeedback group in resting 3. (Table (Table22 and Fig. 3).

Table 2
Learning curves for SMR power at C3 during the resting-state

F
Group × Time
Group (p) Time (p) LSD's post-hoc comparisons
(p)
3.833 1.620
C3 2.538* (0.032) Group: Con > NF in resting 3
(0.062) (0.160)
Time: resting 6 > resting 1, resting 2
and resting 4 in NF
Open in a separate window

Bold number indicates repeated measures ANOVA revealed a significant

interaction between Group (neurofeedback group and control group) and Time
(resting 1 to resting 6) on SMR power at C3

Bold words indicate a significant simple effect of Time by Group in the

neurofeedback group was found. Also, the results revealed a significant simple
effect of Group by Time. LSD post- hoc comparisons revealed the SMR power at C3
in resting 6 was higher than resting 1, resting2, and resting 4 of the neurofeedback
group and the control group is higher than the neurofeedback group in resting 3

Con: Control Group; NF: Neurofeedback Group; *p < 0.05

Fig. 3
The learning curve for averaged SMR power at feedback electrode (C3) in resting-
state across all subjects during six times training in the neurofeedback group and
control group. The x-axis shows the resting-state range, whereas the y-axis shows
averaged SMR power: *p < 0.05. All data have been min–max normalized
individually. Error bars indicate SD. The black dotted line indicates zero
Fig. 5
EEG changes between resting 1 and resting 6 at the C3 electrode in the
neurofeedback group: *p < 0.05. Error bars indicate SD

Furthermore, it is necessary to report on changes in SMR power

within- and between- neurofeedback training. Figure 5b
illustrates the time course of SMR power over the training trials
for both groups. The regression analysis of absolute SMR power
(predictor variable = trial; dependent variable = SMR power)
revealed a significant positive slope across trials only in the
neurofeedback group. In terms of within-training, repeated
measures ANOVA revealed no significant main effects of Group
(neurofeedback group and control group) and Time (trial 1 to trial
6) on SMR power at C3, but there was a significant interaction
between Group and Time. In addition, a significant simple effect of
Time by Group in the neurofeedback group was found. Besides,
the results revealed a significant simple effect of Group by Time.
LSD post-hoc comparisons revealed higher SMR power at C3 in
trial 6 than trial 1 and trial 4, trial 3 than trial 1 of the
neurofeedback group, and the neurofeedback group is higher than
the control group in trial 6. (Table (Table33 and Fig. 4). In terms
of between-training, repeated measures ANOVA revealed no
significant main effects of Group (neurofeedback group and
control group) and Time (session 1 to session 6) on SMR power at
C3(Group: F(1, 24) = 0.545, p > 0.05; Time: (F(5, 20) = 0.916, p >
0.05)), and there was no significant interaction between Group
and Time (F(5, 20) = 0.959, p > 0.05).

Table 3
Learning curves for SMR power at C3 within-session

F
Group × Time
Group (p) Time (p) LSD's post-hoc comparisons
(p)
5.202
C3 0.762(0.391) 1.240(0.328) Group: NF > Con in Trial 6
**(0.003)
Time: Trial 6 > Trial 1 and Trial 4
in NF Trial 3 > Trial 1 in NF
Open in a separate window

Bold number indicates there was a significant interaction between Group and Time

Bold words indicate a significant simple effect of Time by Group in the

neurofeedback group was found. LSD post- hoc comparisons revealed higher SMR
power at C3 in trial 6 than trial 1 and trial 4, trial 3 than trial 1 of the
neurofeedback group. Besides, the results revealed a significant simple effect of
Group by Time. LSD post- hoc comparisons revealed higher SMR power at C3 in the
neurofeedback group than the control group in trial 6

Con Control Group, NF Neurofeedback Group

**p < 0.01

Fig. 4
Time course of SMR power over the neurofeedback training trials, averaged over
all 6 neurofeedback training sessions, presented separately for the neurofeedback
and control groups. The x-axis shows the trial range, whereas the y-axis shows
averaged SMR power: *p < 0.05; **p < 0.01. The black dashed line represents the
regression line. All data have been min–max normalized individually

Frequency specificity

As the trainability analyses revealed that the trained frequency

changed significantly in the neurofeedback group, frequency
specificity was subsequently assessed in the neurofeedback
group. A paired t-test revealed that there was a significant
increase in SMR power between resting 1 and resting 6 at the C3
electrode (SMR: t(12) = -2.701, p < 0.05,), while other frequency
bands (theta: t(12) = -2.062, p > 0.05, alpha: (t(12) = -0.069, p >
0.05, beta: (t(12) = -0.986, p > 0.05) were not significantly affected.
These results indicate that using the relative SMR power protocol,
the neurofeedback training increased SMR power independent of
the other frequency bands in the neurofeedback group (Fig. 5).

Brain-behavior relationships

On average, subjects in the neurofeedback group decreased their

SAS score from 28.85 ± 4.22 to 26.69 ± 4.27 after training (t(12) =
2.545, p < 0.05). For the control group, the SAS scale after six times
training was decreased slightly but not significantly (t(12) =
2.030, p > 0.05) from 29.23 ± 5.18 to 27.00 ± 6.23. Furthermore,
the correlations between changes in emotional symptoms and
SMR power at electrode C3 in the first and last training of resting-
state were examined. A significant negative correlation was found
between the decrease in SAS score and the increase in SMR power
(r = 0.398, p < 0.05). That is, the greater the SMR power, the
greater the improvement in symptoms of anxiety.
Go to:

Discussion

The objective of this work was to propose the relative SMR power
protocol as the feedback value used to improve absolute SMR
power and develope an individual adaptive training system based
on EEG neurofeedback to alleviate anxiety in healthy people.
Trainability, frequency specificity, and brain-behavior
relationships were used to validate training effects in treating
healthy people with anxiety during the SMR up-training. Anxiety is
associated with inattention in terms of clinical manifestation.
Given the rationale beyond this protocol, the relation between
SMR power and attention performance has been found in a
previous study (Lubar and Lubar 1984). To decrease data
variability and better reflect cortical activity, we hereby proposed
the relative SMR power protocol as the feedback value and
explored the application of a neurofeedback protocol based on
SMR up-regulation in healthy people with anxiety. The results
showed that the subjects who had NFT relieved their anxiety and
increased their SMR power compared with subjects who had
sham training. This suggests that neurofeedback supports the
feasibility and efficacy of the NFT protocol based on relative SMR
power for healthy people with anxiety. Thus, this neurofeedback
protocol has the potential to alleviate anxiety in a healthy
population.

Regarding trainability, we first assessed the effectiveness of the

neurofeedback protocol for all subjects by evaluating the change
in SMR power. The analysis of learning effects during training and
within-session illustrated a gradual enhancement in SMR power.
In addition, we have failed to report significant changes in SMR
power between-session which is consistent with the results of
Kober et al. (2015), Vernon et al. (2003), and Vernon, (2005)
(Kober et al. 2015; Vernon 2005; Vernon et al. 2003). For the
neurofeedback group, a linear increase of SMR power during the
first resting-state overtraining was visible, suggesting the transfer
of the previous learning experience to the next training. The
mechanism could be that subjects accessed their perception to
regulate the EEG signals, mastered techniques to control EEG
signals, and reinforced the techniques by repeated practice of
neurofeedback tasks (Lacroix and Gowen 2010; Schwartz and
Shapiro 1976; Sitaram et al. 2016). This result is significant
because it proves that the training of each stage is based on the
training times and experience of the previous days. As with any
type of experiment, the amount of training is crucial to determine
its effectiveness. Hammond (2011) believes that at least 5–10
times of training are needed to prove the effectiveness of
neurofeedback (Hammond 2011). In this study, we performed
only six times of training, which limited the performance of the
results. If more training times were added, the results of
trainability should have been better. In the recent neurofeedback
literature, it is still highly discussed whether neurofeedback
training should lead to tonic changes in the background EEG (as
assessed during resting measurements) or to phasic changes
(Gruzelier 2014c). Only the analysis of changes in SMR power
within- and between- sessions can reveal the second one. The
neurofeedback group receiving real feedback showed an
increasing trend in absolute SMR power at the C3 electrode
within-session. Subjects showed receiving sham feedback no
changes in SMR power over time within-session. But beyond that,
the change in SMR power between-session was not found. It
shows that the subjects can also improve the SMR power during
short-term training. But each session, that is, the state of each day
is not the same, so there is no trend of SMR growth between
sessions during the training. These results reflect successful NFT
based on the relative SMR feedback value in the neurofeedback
group (Gruzelier et al. 2006; Kerstin et al. 2008; Schabus et
al. 2014; Vernon et al. 2003). Accordingly, our subjects were able
to learn how to adapt and generalize mental alertness, physical
relaxation, which corresponded to increasing SMR activity
(Marzbani et al. 2016; Xiang et al. 2018).

Regarding frequency specificity, only SMR band activity

significantly increased in the neurofeedback group after training;
other frequency bands, namely theta, alpha, and beta were
unaffected. In other words, the neurofeedback group significantly
increased the target frequency band, which is also consistent with
previous research (Chen and Lin 2020; Quaedflieg et al. 2016;
Zoefel et al. 2011). Similarly, we also want to explore the changes
in the control group. A paired t-test revealed that there was a
significant increase in theta power between resting 1 and resting
6 at the C3 electrode (theta: t(12) = 2.184, p < 0.05), while other
frequency bands (alpha: t(12) = 0.194, p > 0.05; SMR: t(12) =
0.057, p > 0.05; beta: t(12) = 0.224, p > 0.05) were not significantly
affected possibly due to theta indexing low arousal, tiredness, and
inattention (Gruzelier 2014b). Besides, the feedback value in this
study was relative power which included theta, alpha, SMR, and
beta bands, and the subjects in the control group felt tired or
scatterbrained because they were unable to control the feedback
interface easily. These results indicate that using the relative SMR
power protocol, the neurofeedback training increased SMR power
independent of the other frequency bands in the neurofeedback
group (Fig. 6).
Fig. 6
EEG changes between resting 1 and resting 6 at the C3 electrode in the control
group: *p < 0.05. Error bars indicate SD

Regarding Brain-behavior relationships, the increase in SMR

power correlated only with the decrease in SAS score. Hence, the
increase in SMR activity was correlated only with the intensity of
anxiety according to the subjects in this study. The SMR training
protocol is known to enhance attention. In this study, attention
has been improved probably from the following two reasons.
Subjects have learned the mental state promoted by SMR power
up-training, namely a peaceful, relaxed state, and remaining
focused leads to improve the body's inhibition ability and reduces
the interference of somatosensory information, possibly a result
of subjects shifting their attention from negative thoughts to the
neurofeedback tasks (Hammond 2011; Pimenta et al. 2018;
Sitaram et al. 2016). Another reason for increased attention may
be due to improved sleep quality. Regarding the SAS, we explored
the items about sleep according to the following phrases: 'I fall
asleep easily and get a good night's rest ', 'I have nightmares'. On
average, subjects in the neurofeedback group decreased their
score from 3.46 ± 0.78 to 3.00 ± 0.91 after training (t(12) =
2.521, p < 0.05). For the control group, the scale after six times
training was decreased slightly but not significantly (t(12) =
0.485, p > 0.05) from 3.08 ± 1.39 to 2.92 ± 1.12. As mentioned
above, training aspects of attention can relieve anxiety (e.g., yoga,
meditation). This training helps to learn focus attention (Kiken et
al. 2015; Simon et al. 2020). Therefore, training with the SMR
protocol improved the body's inhibition ability and sleep quality,
thereby improving attention (Enriquez-Geppert et al. 2019;
Reichert et al. 2016), which may be the reason for the improved
intensity of anxiety.

There are some limitations to this study. The main limitation is

that the sample size should be justified with a power analysis
based on the smallest effect size of interest or another method
(Online Resource 1) (Ros et al. 2020). A further limitation is that
we did not include a cognitive performance test that assessed
attention based only on the SMR power. Without such a cognitive
performance test, we cannot completely exclude the possibility
that subjects gradually became familiar with the experiment
process during the training or daily life. Third, long-term training
could have a better impact than short-lived state changes
(Engelbregt et al. 2016). Therefore, future protocols might require
more training or follow-up studies to ensure more robust effects
of NFT based on EEG.

In future research, we aim to find an appropriate method to

exclude the responder to verify the role of NFT. This would be
beneficial for future trainer selection and treatment outcome
prediction. Additionally, combining other reward protocols with
concurrent relative SMR power up-regulation might generate
more positive outcomes. Neurofeedback based on relative SMR
power could be a time-effective treatment for anxiety and an
interesting new option to consider in anxiety therapy, especially
for clinical applications. However, whether absolute or relative
SMR power is better as a neurofeedback value will be discussed in
the future.
Go to:

Conclusion

Taken together, the relative SMR power protocol we proposed has

been reported as the feedback value to increase SMR power rather
than relative SMR power within healthy subjects who learned self-
regulation based on NFT. Moreover, three parameters—
trainability, frequency specificity, and brain-behavior
relationships—were utilized to validate training effects in treating
healthy people with anxiety during the SMR up-training. Hence,
our results imply that NFT using a feedback protocol based on
relative SMR power at the C3 electrode could significantly
decrease the SAS score and increase SMR power; thus, anxiety
could be relieved for healthy people. This study supports the
potential of neurofeedback as a promising novel experimental
therapy for neurological and psychiatric conditions. This
preliminary study supports the feasibility and efficacy of a relative
SMR power protocol for healthy people with anxiety.
Go to:
Supplementary Information
Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 42 KB)(42K, pdf)

Supplementary file2 (PDF 84 KB)(83K, pdf)
Go to:

Acknowledgements
We thank the 2 anonymous reviewers for their constructive
comments.
Go to:

Abbreviations

NFT Neurofeedback training

SMR Sensorimotor rhythm

SAS Self-rating anxiety scale

Go to:

Author contributions

SL and XH contributed equally to the study conception, literature

search, and writing. All authors contributed to manuscript
revision, read and approved the submitted version.
Go to:
Funding

This research was funded in part by National Natural Science

Foundation of China, Grant Nos. 81925020, 81630051.
Go to:

Declarations
Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by the Ethics Committee of Tianjin

Anding Hospital. (Number: NCT04562324 (Online Resource 2)).
Go to:

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional

claims in published maps and institutional affiliations.

Shuang Liu and Xinyu Hao have contributed equally to this work.

Go to:

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