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Abstract
Objective: To test a common assumption underlying the clinical use of electroencephalographic (EEG) biofeedback training
(neurofeedback), that the modulation of discreet frequency bands is associated with frequency-specific effects. Specifically, the proposal was
assessed that enhancement of the low beta components sensorimotor rhythm (SMR: 12 15 Hz) and beta1 (15 18 Hz) affect different aspects
of attentional processing.
Methods: Subjects (n 25) were randomly allocated to training with either an SMR or beta1 protocol, or to a non-neurofeedback control
group. Subjects were assessed prior and subsequent to the training process on two tests of sustained attention. The neurofeedback participants
were also assessed on target P300 event-related potential (ERP) amplitudes in a traditional auditory oddball paradigm.
Results: Protocol-specific effects were obtained in that SMR training was associated with increased perceptual sensitivity d prime (d0 ),
and reduced omission errors and reaction time variability. Beta1 training was associated with faster reaction times and increased target P300
amplitudes, whereas no changes were evident in the control group.
Conclusions: Neurofeedback training of SMR and beta1 band components led to significant and protocol-specific effects in healthy
subjects. The data can be interpreted as indicating a general attention-enhancing effect of SMR training, and an arousal-enhancing effect of
beta1 training.
q 2004 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
Keywords: EEG biofeedback; Neurofeedback; Beta1 activity; Sensorimotor rhythm; Attention; P300
1. Introduction
Various parameters of the human electroencephalogram
(EEG) can be brought under operant control by means of a
training process involving the real-time display of ongoing
changes in the EEG via an EEG biofeedback loop. The
principal feasibility of learned self-regulation has been
demonstrated for evoked potentials (EPs) (Rosenfeld et al.,
1969), event-related potentials (ERPs) (Birbaumer et al.,
1981), slow cortical potentials (SCPs) (Birbaumer, 1984;
Hardman et al., 1997), and EEG frequency components
(Kamiya, 1968), with the latter two being of particular
interest due to their reported intrinsic clinical benefits. For
instance, the operant modulation of positive and negative
SCP shifts has been found to facilitate control over epileptic
seizures (Birbaumer et al., 1991; Rockstroh et al., 1993),
* Corresponding author. Tel.: 1-212-342-0121; fax: 1-212-342-0855.
E-mail address: te2111@columbia.edu (T. Egner).
and has been employed to spectacular effect as a braincomputer communication device for totally paralysed
patients (Birbaumer et al., 1999).
Arguably the best established clinical application of AC
EEG frequency component training consists of the treatment of epilepsy through learned self-regulation of the
12 15 Hz sensorimotor rhythm (SMR) recorded from
central scalp regions over sensorimotor cortex (for review
see Sterman, 2000). While the term SMR originally referred
exclusively to the occurrence of phasic EEG spindles,
the term will here be used to cover both phasic and tonic
12 15 Hz activity over the sensorimotor strip. Trained
enhancement of the SMR has been demonstrated to result in
increased seizure thresholds in response to exposure to
eliptogenic agents in monkeys (Sterman et al., 1978), and to
lead to reduced seizure incidence in human epileptics
(Sterman and Friar, 1972; Sterman et al., 1974; Sterman and
MacDonald, 1978; Sterman and Shouse, 1980). SMR
activity over sensorimotor cortex is probably generated
1388-2457/$30.00 q 2004 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/S1388-2457(03)00353-5
132
2. Methods
2.1. Subjects
Participants were 25 students (7 males, 18 females; mean
age 21.7 years, SD 2.24) from the Royal College of Music
(London). The subjects volunteered for participation, gave
their informed consent, and the investigation received
ethical approval from the Riverside Research Ethics
Committee (ref. RREC 2224). The subjects did not receive
monetary reward for participation. Participants were
screened with a health-related questionnaire in order to
exclude subjects with a history of mental or neurological
illness, or currently receiving psychoactive medication. No
volunteers had to be excluded.
2.2. Design
The subjects were randomly allocated to one of 3 training
groups: beta1 neurofeedback (n 8), SMR neurofeedback
(n 9), or a group that engaged in Alexander technique
training (n 8). For the purpose of testing hypotheses
concerning protocol-specific effects on target P300 ERPs,
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3. Results
3.1. TOVA
The hypothesized commission error changes in the beta1
and SMR groups, and d0 increase in the SMR group, were
assessed by planned comparisons (paired t tests) at onetailed P , 0:05 levels. In order to determine differential
effects of the neurofeedback protocols on variables for
which no a priori hypotheses existed, 3 2 (group time)
mixed-subjects analyses of variance (ANOVAs) were
applied, followed by post hoc comparisons assessing
within-group changes for each group (paired t tests), and
between-group differences in change scores (independent
t tests). Descriptive statistics of all TOVA measures are
presented in Table 1.
135
Table 1
Means and standard deviations on all TOVA measures in each group before
and after training
Group
SMR
Beta1
Alexander
Variables
Omission errors
Commission errors
d0
RT (ms)
RTV (ms)
Omission errors
Commission errors
d0
RT (ms)
RTV (ms)
Omission errors
Commission errors
d0
RT (ms)
RTV (ms)
Time 1
Time 2
Mean
SD
Mean
SD
1.00
5.67
6.18
320
84
0.00
3.38
6.86
366
75
0.25
4.25
6.40
343
74
3.00
3.04
0.90
37
20
0.00
3.54
0.73
33
17
0.46
3.69
1.23
58
14
0.11
4.67
6.55
319
70
0.00
4.25
6.85
329
68
0.63
2.38
6.49
341
76
0.33
3.91
0.89
51
27
0.00
5.95
0.78
29
12
1.41
1.60
1.21
54
17
SMR
Beta1
Alexander
Variables
Omission errors
Commission errors
d0
RT (ms)
RTV (ms)
Omission errors
Commission errors
d0
RT (ms)
RTV (ms)
Omission errors
Commission errors
d0
RT (ms)
RTV (ms)
Time 1
Time 2
Mean
SD
Mean
SD
14.00
4.00
5.69
503
147
10.11
5.67
5.86
526
146
8.38
3.63
6.50
494
118
3.33
0.85
0.51
25
11
3.34
1.64
0.52
14
11
3.01
1.02
0.49
15
6
7.75
3.25
6.56
489
128
11.33
4.11
6.35
502
141
8.50
3.88
6.44
483
115
1.88
0.70
0.58
25
12
3.67
1.29
0.71
23
9
3.55
0.81
0.64
14
69
136
4. Discussion
Of the hypothesized cognitive-behavioural effects of the
SMR and beta1 neurofeedback protocols, the expected
commission error decrease in the SMR group and commission error increase in the beta1 group were not confirmed by
the current data. The expected d0 improvements in the SMR
group on the other hand were confirmed in both the TOVA
and the divided attention task. The expected target P300
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Acknowledgements
This research was funded by the Leverhulme Trust and
generously supported by the Royal College of Music.
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