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1 Braincomputer interfaces for EEG neurofeedback:
2 Peculiarities and solutions
3 Ren J. Q1 Huster
a,b,
, Zacharais N. Mokom
a
, Stefanie Enriquez-Geppert
a,b,c
, Christoph S. Herrmann
a,b,d
4
a
Experimental Psychology Lab, Carl von Ossietzky University, Oldenburg, Germany
5
b
Research Center Neurosensory Science, Carl von Ossietzky University Oldenburg, Oldenburg, Germany
6
c
Karl-Jaspers Clinic, European Medical School, Oldenburg, Germany
7
d
Center for excellence, Hearing4all, Oldenburg, Germany
8
9
a b s t r a c t a r t i c l e i n f o
10 Article history:
11 Received 13 May 2013
12 Received in revised form 20 August 2013
13 Accepted 26 August 2013
14 Available online xxxx
15 16 17
18 Keywords:
19 Neurofeedback
20 BCI
21 Software
22 EEG
23 Neurofeedback training procedures designed to alter a person's brain activity have been in use for nearly four
24 decades now and represent one of the earliest applications of braincomputer interfaces (BCI). The majority of
25 studies using neurofeedback technology relies on recordings of the electroencephalogram (EEG) and applies
26 neurofeedback in clinical contexts, exploring its potential as treatment for psychopathological syndromes.
27 This clinical focus signicantly affects the technology behind neurofeedback BCIs. For example, in contrast to
28 other BCI applications, neurofeedback BCIs usually rely on EEG-derived features with only a minimum of addi-
29 tional processing steps being employed. Here, we highlight the peculiarities of EEG-based neurofeedback BCIs
30 and consider their relevance for software implementations. Having reviewed already existing packages for the
31 implementation of BCIs, we introduce our own solution which specically considers the relevance of multi-
32 subject handling for experimental and clinical trials, for example by implementing ready-to-use solutions for
33 pseudo-/sham-neurofeedback.
34 2013 Published by Elsevier B.V.
35 36
37
38
39 1. Introduction
40 A braincomputer-interface (BCI) constitutes a processing pipeline
41 originating from recordings of brain activity and producing data that
42 assist human functioning (e.g., Scherer et al., 2013). Consisting of
43 hard and software components, BCIs record brain activity for such dif-
44 ferent purposes as ambulatory monitoring, the control of prostheses,
45 spelling devices, or to establish communication with paralyzed persons
46 (e.g., Birbaumer et al., 2009; Hinterberger et al., 2003). Another applica-
47 tion of BCI research, related to procedures for ambulatory monitoring,
48 is neurofeedback. Whereas in ambulatory monitoring brain activity
49 is recorded to detect and warn of potentially harmful states (e.g., an
50 epileptic seizure), neurofeedback informs a user about its own brain ac-
51 tivity by real-time feedback (which in the visual domain, for example,
52 could be presented as a rectangle whose color depends on changes of
53 the brain feature of interest). Thereby, it provides a learning mecha-
54 nism on how to manipulate one's own brain activity.
55 Neurofeedback procedures are in use already for quite some time and
56 most likely even represent the earliest applications of BCIs. This stems
57 from the notion that many psychiatric disorders are associated with
58 malfunctioning of the brainandthat, consequently, a procedure targeting
59 the self-regularized normalization of brain function is judged benecial
60 for convalescence. Yet, whereas BCIs in other elds continuously ma-
61 tured, methodological and technical progress with neurofeedback
62 seems to be way slower. This may at least partly be caused by the fact
63 that research on BCIs in other elds obtained strong support from ma-
64 chine learning specialists, whereas neurofeedback procedures from
65 the beginning predominantly raised interest in researchers focusing on
66 its application for clinical treatment and cognitive modulation. Here, we
67 will shortly reviewthe current state-of-the-art of neurofeedback technol-
68 ogy and its applications and delineate strategies for further development.
69 Inaddition, we will shortly reviewopensource software packages for BCI,
70 also introducing our own package (NeuroFeedback Suite 1.0) specically
71 designed for controlled, multi-subject neurofeedback training trials. We
72 will focus our examinations on neurofeedback procedures relying on
73 recordings of the electroencephalogram (EEG), because EEG represents
74 the most dominant measurement modality and holds most potential to
75 enable true mobile BCIs in due time. Studies using other modalities will
76 be considered as well whenever of relevance. Please note that this special
77 issue also contains a reviewarticle specically addressing motor imagery
78 in clinical and basic research; therefore, we will leave the discussion of
79 this interesting eld of research to Sterr et al. (add reference).
80 2. Status quo of neurofeedback research
81 Since the earliest reports on EEG-based neurofeedback (Kamiya,
82 1971) the focus in this eld has always been on the application
International Journal of Psychophysiology xxx (2013) xxxxxx
Corresponding author at: Experimental Psychology Lab, Department of Psychology,
European Medical School, Carl von Ossietzky Universitt Oldenburg, Germany. Tel.: +49
441 798 4612; fax: +49 441 798 3865.
E-mail address: rene.huster@uni-oldenburg.de (R.J. Huster).
INTPSY-10717; No of Pages 10
0167-8760/$ see front matter 2013 Published by Elsevier B.V.
http://dx.doi.org/10.1016/j.ijpsycho.2013.08.011
Contents lists available at ScienceDirect
International Journal of Psychophysiology
j our nal homepage: www. el sevi er . com/ l ocat e/ i j psycho
Please cite this article as: Huster, R.J., et al., Braincomputer interfaces for EEG neurofeedback: Peculiarities and solutions, Int. J. Psychophysiol.
(2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.08.011
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83 neurofeedback in clinical settings. Up to now, still the vast majority
84 of studies try to elucidate the efcacy of neurofeedback trainings as ad-
85 ditional tool for the treatment of epilepsy (Egner and Sterman, 2006;
86 Sterman and Egner, 2006), substance use disorder (Sokhadze et al.,
87 2008), affective disorders (Hammond, 2005), tinnitus (Dohrmann
88 et al., 2007a, 2007b), or pain (Jensen et al., 2008). Yet, without doubt at-
89 tention decit/hyperactivity disorder (ADHD) has been the major focus
90 of relevant clinical investigations. Taking ADHD as an example, Arns
91 et al. (2009) conducted a meta-analysis of 15 studies and concluded
92 that EEG neurofeedback for ADHD can be considered efcacious and
93 specic, showing overall medium to large effect sizes in pre-/post-
94 treatment assessments regarding measures of inattention, impulsivity,
95 and hyperactivity. Recently, Lofthouse et al. (2012) reassessed the
96 literature specically focusing on studies relying on designs including
97 randomized-control assignments, blinding and pseudo-neurofeedback
98 procedures. Overall, data also indicated medium to large treatment
99 effects, although the authors recommended to further investigate the
100 specicity of effects via more rigorously controlled double-blindstudies.
101 It is important to note, though, that the application of neurofeedback
102 for basic experimental research on cognition is of special interest. Here,
103 neurofeedback serves as an intervention that opens the possibility to
104 transfer from mere correlational to causal inferences about the manipu-
105 lated brain states and their cognitive contributions. Such basic research
106 on cognitive modulations by means of EEG neurofeedback draws a sim-
107 ilar picture as the previously mentioned clinical studies. Neurofeedback
108 procedures have, for example, successfully been used to alter partici-
109 pants' alpha or gamma activity and thereby increase cognitive capabili-
110 ties in mental rotation and memory (e.g., Hanslmayr et al., 2005; Zoefel
111 et al., 2011; Keizer et al., 2010) or visual detection (Salari et al., 2012).
112 Furthermore, it has been shownthat these operant learning mechanisms
113 can induce long lasting changes in EEG activity ( Q2 Cihan Gani, 2008)
114 and network connectivity (Ros et al., 2013). However, some studies
115 also indicate that the evoked effects are not always frequency-specic,
116 i.e. changes do not exclusively occur in the targeted frequency-band
117 (e.g., Enriquez-Geppert et al., in press, 2013b), suggesting either decits
118 in the specicity of the training regimen or the existence of unspecic
119 outcome effects (e.g., placebo or other expectancy effects).
120 Hence, data frombothclinical studies and basic researchsupport the
121 efcacy of neurofeedback trainings, though unspecic effects seem to
122 exist that potentially threaten the internal validity of studies without
123 appropriate control conditions.
124 3. Basic setup of neurofeedback BCIs
125 In general, a neurofeedback system consists of ve elements or pro-
126 cessing steps (Fig. 1): 1) brainsignal acquisition, 2) signal preprocessing,
127 3) feature extraction, 4) generation of a feedback signal, and 5) an adap-
128 tive learner. Of course, all necessary steps are subjected to a real-time
129 constraint. The extracted features usually quantify the strength of activ-
130 ity of a specic brain region or network and the feedback signal conveys
131 information about relevant changes in brain states. Participants are
132 supposed to nd and adapt strategies to purposefully alter their brain
133 states in accordance with prior instructions. Provided an appropriate
134 learning signal and a responding participant, these steps altogether con-
135 stitute a feedback loop whose elements change their states in a quasi-
136 continuous manner based on the timing of the feedback signal. Because
137 a positive learning signal immediately follows once the desired brain
138 state is achieved, neurofeedback training is considered an operant or in-
139 strumental conditioning procedure (see Sherlin et al., 2011, for details).
140 3.1. Acquisition of brain signals
141 Without a doubt, the most common recording method used for
142 neurofeedback is EEG (Birbaumer et al., 2009). At electrodes placed on
143 the scalp, EEG measures voltage uctuations caused by the spatio-
144 temporally summed activity of large populations of neurons. It is gener-
145 ally assumed that excitatory postsynaptic activity at pyramidal neurons
146 represents the most dominant source of EEG. This notion is fostered be-
147 cause of the pyramidal neurons' geometrical organization and the ne-
148 cessity for a strong temporal overlap of currents, most easily achieved
149 with rather slow-changing synaptic events. Hence, EEG mainly reects
150 synaptic input and intracortical processing, in extracellular recordings
151 manifested as local eld potentials (LFP), rather than the output of
152 pyramidal cells (but see Buzski et al., 2012). EEG represents a rather
Fig. 1. Basic setup of a braincomputer interface for neurofeedback. After recording of EEG, data undergo preprocessing (e.g., artifact detection and rejection or correction), feature
generation and extraction, computation and presentation of the feedback signal. The latter step closes the feedback loop, with the participant trying to learn to use the feedback signal
to alter the brain activity in accordance with the instructions.
2 R.J. Huster et al. / International Journal of Psychophysiology xxx (2013) xxxxxx
Please cite this article as: Huster, R.J., et al., Braincomputer interfaces for EEG neurofeedback: Peculiarities and solutions, Int. J. Psychophysiol.
(2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.08.011
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153 low-cost, robust, and potentially mobile measurement modality. In ad-
154 dition, its high temporal resolution, which usually is in the range of only
155 few milliseconds, makes it ideal for real-time BCI applications.
156 Similar in terms of the physiological processes driving signal gener-
157 ation is magnetoencephalography (MEG). Yet, the underlying technol-
158 ogy is different, because MEG does not directly measure the electrical
159 signals resulting from neural events but rather registers the changes of
160 magnetic elds caused by electric currents. Although MEG recordings
161 are less affected by global characteristics of the head (e.g., by the resis-
162 tive properties of the skull) than EEG is, it is not widely used for BCI
163 because MEG is very sensitive to noise of environmental magnetic
164 elds and its hardware needs to be installed xedly. The acquisition
165 and maintenance of MEG systems are Q3 also very expensive, which is
166 the reason why MEG is available only in rather few specialized imaging
167 centers. Still, MEG-based neurofeedback procedures have been well
168 reported in the BCI literature (Sudre et al., 2011).
169 Turning to measurement modalities that rely on hemodynamic
170 rather than electric processes, over the last two decades both functional
171 magnetic resonance imaging (fMRI) and near infrared spectroscopy
172 (NIRS) have become increasingly popular for neurofeedback procedures
173 (e.g., Linden et al., 2012; Mihara et al., 2012). FMRI exploits the fact that
174 neuronal activity and certain parameters of cerebral blood ow are
175 coupled. Relyingonthe blood-oxygen-level-dependent (BOLD) contrast,
176 the change in magnetization between oxygen-rich and oxygen-poor
177 blood is assessed, with lower signal values in the latter case. Put simply,
178 increased neural activity is associated with regional metabolization of
179 glucose and oxygen, whose consumption usually is overcompensated
180 by regional increases in the ow of oxygenated blood. As it stands,
181 BOLD responses seem to be triggered by and to best reect LFPs. The
182 so-called hemodynamic response, which is the change in the MR signal
183 induced by the aforementioned mechanisms, usually is triggered within
184 a radius of fewmillimeters around the center of neural activity, but tem-
185 porally lags it by several seconds, the time ascribed to neurovascular
186 coupling mechanisms. In addition, due to the temporal properties of
187 the hemodynamic response as well as fMRI technology, the temporal
188 resolution also is rather low, usually in the order of seconds.
189 Conceptually related to fMRI, NIRS also assesses uctuations in
190 cerebral blood ow coupled to regional metabolism. However, this
191 method does not rely on changes of magnetic properties but rather
192 uses infrared-emitting diodes and light detectors to record changes in
193 the attenuation of the emitted light. These uctuations reect variations
194 in the local oxygenation of blood hemoglobin. As is the case with fMRI
195 BOLD measurements, the recorded events lag neural activity by several
196 seconds, but the temporal resolution of NIRS is higher and usually is in
197 the order of 100 ms. Then again, it shows limited spatial resolution,
198 roughly 1 cm, and its depth sensitivity also is constrained to 23 cm
199 within the cortex. Since NIRS also represents a comparably mobile and
200 cost effective measurement modality it recently has more often been
201 used for neurofeedback (Mihara et al., 2012).
202 Of course, these different technologies all require specic settings
203 and procedures for appropriate recordings already before digitization
204 of the signals. These, however, do not strongly change the basic charac-
205 teristics outlined above and they may well change between different
206 applications or experimental settings even when the same measure-
207 ment modality is in use. For the remainder of this article, though, we
208 will focus on EEG-based neurofeedback BCIs that clearly represent the
209 most dominant approach in this eld.
210 3.2. Preprocessing of recorded signals
211 Any recording of brain signals inevitably has to deal with artifacts,
212 whose origin usually is either technical or physiological in nature. Most
213 common technical artifacts in EEG recordings are caused by other elec-
214 trical equipment or changing electrode impedances. In general, online
215 lters are well suited to address the effects these sources have on signal
216 quality. Line-noise, for example, can easily be suppressed by applying
217 band-stop lters at 50 or 60 Hz. Inaddition, most current neurofeedback
218 trainings still are conducted in experimental or clinical laboratories,
219 which further open the opportunity to take recordings in electrically
220 shielded rooms. Changes in electrode impedances constitute a greater
221 challenge because frequency characteristics of resulting noise exhibit
222 broadband effects. Recent years, however, saw a strong improvement
223 in low-cost and mobile electrode systems, which provide sufcient
224 signal quality with only a minimum of time needed for subject prep-
225 aration (Debener et al., 2012; De Vos et al., Jung et al., Q4 Tangermann
226 et al., this issue). This development may also advance the application
227 of neurofeedback, and BCIs in general, outside of protected laboratory
228 environments.
229 More problematic are artifacts of physiological origin, such as those
230 from cardiac, muscle, or eye activity. When apparent in the signal,
231 these artifacts can either be corrected or rejected. Pronounced cardiac
232 artifacts can often be avoided by careful electrode placement. Also,
233 most of the signal power associated with muscle artifacts is found in
234 higher frequency bands usually not targeted by current neurofeedback
235 applications (N30 Hz, but see Salari et al., 2012) and instructing subjects
236 not to clench teeth or move the heads effectively avoids the generation
237 of myographic activity at rst hand. However, eye-related artifacts
238 such as blinks or eye movements are not that easily treated. Because
239 neurofeedback relies on continuous measurements over the course
240 of several minutes, eye artifacts cannot easily be avoided by, for exam-
241 ple, simply instructing the participants not to blink. Also, their power
242 unfolds in frequency bands often used for neurofeedback training,
243 which makes them even more problematic in this than in other BCI
244 contexts because, depending on the exact signal feature extracted for
245 feedback, participants might wrongly (and involuntarily) learn not to
246 modulate their brain activity but to manipulate the feedback signal via
247 eye activity.
248 This leaves us with the question of how to process these especially
249 problematical contents of our signal. The most common procedure is
250 to detect and reject data epochs contaminated with artifacts such as
251 an eye blink. Most rejection procedures simply monitor signal ampli-
252 tudes for suspiciously high values (e.g., those higher than 75 V), be-
253 cause blinks and horizontal eye movements generate signal shifts
254 much larger than the normal EEG. Alternatively (or additionally), one
255 may look for steep gradients occurring from one sample to the next,
256 caused by the rather fast amplitude jumps often associated with eye
257 and muscle artifacts. However, amplitudes of eye artifacts vary substan-
258 tially across subjects causing any xed threshold to miss a substantial
259 number of contaminated epochs especially on participants with low
260 amplitude artifacts. On the other hand, a threshold too low may cause
261 a signicant number of clean epochs to be rejected erroneously. This
262 indeed is a severe problem which we tried to address with a semi-
263 adaptive algorithm based on an initial calibration phase in the time-
264 but a monitoring phase relying onthe frequency-domainrepresentation
265 of the signal (for details see Section 5.2).
266 Alternatively, one may choose to correct for artifacts in order to
267 not unnecessarily disrupt the neurofeedback training. Many procedures
268 have been suggested and are applied for ofine analyses of EEG data.
269 Basic ltering can be thought of as a correction procedure too, but it
270 will not always produce satisfying results for the reasons outlined
271 above. A procedure that has been in use for some time for ofine correc-
272 tionof EEGdata is basedonlinear regression(Grattonet al., 1983). Here,
273 a regression between ocular channels on the one hand and the EEG
274 channels on the other hand is used to predict and subtract those parts
275 of the EEG caused by eye artifacts. Although several variants of such
276 regression-based procedures exist (see Croft et al., 2005), it seems that
277 none of these procedures has been applied for real-time analyses yet.
278 A method relying on the covariance structure of these multi-channel
279 data as well is principal component analysis (PCA), which would help
280 to identify artifact-related components uncorrelated with the actual
281 brain activity that then simply could be partialized out from the data
282 (e.g., Lins et al., 1993a, 1993b). However, both linear regression and
3 R.J. Huster et al. / International Journal of Psychophysiology xxx (2013) xxxxxx
Please cite this article as: Huster, R.J., et al., Braincomputer interfaces for EEG neurofeedback: Peculiarities and solutions, Int. J. Psychophysiol.
(2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.08.011
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283 PCA for artifact correction have been criticized because proper brain ac-
284 tivity and eye artifacts may not always be uncorrelated. A more recent
285 approach is independent component analysis (ICA) that overall seems
286 to capture artifactual activity of the EEG very well (Mennes et al.,
287 2010). ICA decomposes the EEG into sources (or independent compo-
288 nents) whose temporal proles show maximal statistical indepen-
289 dence. Again, artifactual components can simply be subtracted from
290 the EEG. All these correction procedures can be thought of as spatial
291 lters. Their parameters need to be estimated from EEG data whose
292 latent structure is representative for the EEG on which the actual cor-
293 rection has to be applied. Whether this generalizability indeed is given,
294 however, would have to be determined for each specic application.
295 Beyond, less commonmethods have beenproposedwhichaimespecially
296 at the detection and removal of artifacts in real-time contexts. Noureddin
297 et al. (2012) used an algorithm based on concurrent recordings from an
298 eye-tracking system, whereas others explored neural networks or blind
299 source separation algorithms and their combination with classication
300 procedures such as support vector machines (e.g., Bartels et al., 2010;
301 Erfanian and Mahmoudi, 2005; Gao et al., 2010; Javidi et al., 2011). Not
302 least, spatial lters may as well be constructed based on constrained
303 ICA, whose feasibility for EEG measurements has already been shown
304 (De Vos et al., 2011).
305 Athorough comparison and evaluation of methods for detection and
306 correction of artifacts in EEG recordings under real-time constraints
307 has not yet been published. Screening the literature reveals that most
308 studies rely on rejection procedures based on amplitude thresholds
309 for artifact detection (usually focusing on eye artifacts) and try to
310 minimize muscular artifacts by a combination of appropriate instruc-
311 tions and data ltering. However, the exact algorithms for artifact detec-
312 tion and rejection exhibit considerable variance. Whereas some studies
313 rely on amplitude thresholds in the time-domain applied to EOG chan-
314 nel recordings (e.g., Salari et al., 2012), others apply thresholds to an
315 individually determined frequency band (e.g., Zoefel et al., 2011) or a
316 combination of multiple but xed frequency bands (de Zambotti et al.,
317 2012). Unfortunately one has to note that a number of studies do not
318 at all specify the exact procedure applied to minimize the impact of
319 artifacts. It has to be concluded that studies addressing and comparing
320 procedures for real-time processing of artifacts are urgently needed.
321 This is true for BCI research in general, but is of special importance for
322 neurofeedback, because contaminated feedback signals may strongly
323 inuence and invalidate the learning outcome.
324 3.3. Feature generation and selection
325 With most BCIs this is the most critical step: given multidimensional
326 data and various procedures for data transformations, the crucial ques-
327 tion is how to best generate and select a specic feature that optimizes
328 the interface's performance. EEGrepresents high-dimensional recordings
329 of spatio-temporally overlapping activity from different brain sources.
330 Because of this, data reduction and decomposition, e.g. my means of
331 procedures such as ICA or PCA on the one hand, and Fourier or Wavelet
332 transforms on the other hand, are very common. Specic methods
333 for feature selection have been identied as well, such as sequential
334 forward or backward selection. Importantly, because most BCIs aim at
335 event-classication, such as the detection of a selected letter embedded
336 in a serial or parallel presentation of non-selected ones (as with a
337 word-speller), feature generation and selection can be approached in
338 a data-driven manner with the BCIs performance being the criterion
339 to be optimized.
340 With neurofeedback training, on the other hand, the procedure
341 underlying the identication of an optimal feature is much slower.
342 Potential features are usually not determined based on data provided
343 for a training procedure, but rather are selected based on theories
344 derived from years of extensive neuroscientic research. Taking ADHD
345 as an example, this means that rst a neurocognitive process has
346 to be isolated strongly (if not even causally) related to behavioral
347 symptomatology. Only then can be determined whether this specic
348 process can sufciently be captured with EEG or any other of the previ-
349 ously introduced methods. Furthermore, the assessment of whether
350 this feature and the complementary training procedure are actually
351 successful relies on careful evaluation of the behavioral and cognitive
352 outcome of neurofeedback training studies. Thus, it becomes obvious
353 that the basic approach (data- vs. hypothesis driven) to and the timing
354 (weeks or months vs. years) of development cycles for neurofeedback
355 differ strongly from BCI applications in most other elds.
356 Because neurofeedback applications depend on input from basic
357 neuroscience, it is not surprising that relevant studies still nearly exclu-
358 sively rely on features with only a minimumof data transformation. The
359 vast majority of studies simply extract the power of a specic frequency
360 band after computation of a Fourier transform on the preprocessed and
361 segmented data. Then, for each segment the rawpower value usually is
362 compared to the baseline power of the same frequency estimated from
363 a separate measurement taken prior to a feedback session. Such relative
364 power values have been used for training of the alpha (e.g., Ros et al.,
365 2013; Zoefel et al., 2011), theta (Enriquez-Geppert et al., 2013b), or
366 gamma (e.g., Salari et al., 2012) frequency bands. However, it has been
367 argued that this rather simple feature may not always be frequency-
368 specic, given that alterations in neighboring frequencies may as well
369 affect the feature of interest, albeit to a smaller degree. Hence, some
370 studies rather quantify the frequency of interest relative to other fre-
371 quency bands, comparing this relative feature during feedback to a
372 similar computation taken from a baseline measurement. Just recently,
373 for example, de Zambotti et al. (2012) used the ratio of 1215 Hz
374 and 47 Hz activity over the somato-motor region for neurofeedback.
375 Irrespective of whether one relies on values of a single frequency
376 band or one computes the ratio relative to other frequencies, the target
377 frequency can furthermore be individually determined in some cases.
378 An individual's dominant frequency in a given band seems to be deter-
379 mined by morphological characteristics of relevant ber tracts and
380 neural connectivity. Q5 Zaehle and Herrmann (2011), for example, found
381 that participants' individual gamma frequency was highly correlated
382 with the white matter volume of the posterior corpus callosum. Corre-
383 spondingly, especially neurofeedbacktrainings of occipital alpha activity
384 often rely on individually determined rather than globally dened
385 frequency bands (e.g., Nan et al., 2012; Zoefel et al., 2011).
386 A strong advantage of features directly derived from EEG-frequency
387 bands is their simplicity, both in terms of their computation but also
388 regarding their interpretation, because they most directly relate to
389 the neuroscientic literature they have been derived from at rst
390 hand. The more complex data transformations are, e.g. including di-
391 mensional reduction and clustering or classication, the harder they
392 may become to interpret in relation to prior research. Again, because
393 in other BCI approaches the major interest is not to foster basic neuro-
394 science knowledge but to optimize BCI performance (often only for
395 a single patient), such complex transformations are much more
396 widespread in other than neurofeedback BCI applications. Neverthe-
397 less, especially procedures acting as combined lters may be benecial
398 in this context. For example, PCA and ICA can be thought of as spatio-
399 temporal lters when the feedback is based on a selected component
400 reecting the main process of interest. Filters based on common spatial
401 patterns or common spatio-spectral patterns may prove useful as well
402 (e.g., Sannelli et al., 2010; Lemm et al., 2005). However, the latter pro-
403 cedures represent classication approaches and thus rely on an exten-
404 sive training period. Hence, in this training phase a rater would have to
405 rst classify a number of trials that are then used for lter optimiza-
406 tion. If successful, such a lter could provide a more specic measure
407 of whether a specic brain state has been reached or not. In the context
408 of neurofeedback, however, this holds the potential of circularity and
409 lter design may suffer from poor rater reliability. Hence, a thorough
410 investigation of procedures that may help to increase the signal-to-
411 noise-ratio by means of further processing steps for feature extraction
412 is urgently needed.
4 R.J. Huster et al. / International Journal of Psychophysiology xxx (2013) xxxxxx
Please cite this article as: Huster, R.J., et al., Braincomputer interfaces for EEG neurofeedback: Peculiarities and solutions, Int. J. Psychophysiol.
(2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.08.011
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413 3.4. Feedback signals
414 Once anappropriate feature potentially suited for neurofeedback has
415 been derived, it needs to be fed back to the participant in order to close
416 the learning loop. While with other BCI applications a change in the
417 participant's brain activity may well be a side effect but is not directly
418 pursued, with neurofeedback the modication of brain processes actu-
419 ally is the ultimate goal of the procedure. Hence, appropriate design of
420 the feedback (or control) signal and its presentation is crucial.
421 Feedback signals of various forms and modalities have been utilized.
422 Most studies refer to rather simple stimulus constellations in the
423 visual or auditory domain. For example, quite common is the binaural
424 presentation of a tone whose frequency changes in congruence with
425 the feature of interest (e.g., higher activity corresponds to higher tone
426 frequency and vice versa; e.g., Becerra et al., 2012) or the visual display
427 of colored squares (here, color saturation or square size represent
428 brain activity; e.g., Enriquez-Geppert et al., 2013b). More complex vi-
429 sual stimuli have been in use as well, including thermometer displays
430 (e.g., Subramanian et al., 2011), ying balloons or rockets (e.g., Gruzelier
431 et al., 1999), or virtual re (e.g., deCharms et al., 2005). Such complex
432 feedback signals are often employed under the assumption that they
433 may lead to a higher commitment of participants, thereby optimizing
434 training outcome. In addition, staged multi-stimulus feedback proce-
435 dures have been suggested as well. Nan et al. (2012), for example,
436 dened two subgoals for feedback to increase their participants' indi-
437 vidual alpha amplitude relative to their broad-band EEG amplitude.
438 Two visual stimuli, a sphere and a cube, indicated goal achievement.
439 The radius of the sphere fed back the amplitude of the feature in real-
440 time, whereas the sphere's color changed when goal 1 was reached,
441 which simply corresponded to a high amplitude threshold. Once goal
442 1 was reached, participants had to address goal 2, which was to stay
443 above the threshold for a period of at least 2 s. Then, every 2 s the
444 cube's height was raised until a maximum was reached; alternatively,
445 given that these goals were not met anymore, the cube's height de-
446 clined again.
447 Feedback designs can also differ across studies with respect to the
448 timing parameters of the feedback signal. Whereas fMRI-based feed-
449 back naturally lags neural activity by several seconds and the sampling
450 rate is signicantly lower, feedback signals relying on EEG can follow
451 neural events with a minimal delay determined by the processing
452 time necessary for feature extraction. Hence, in EEG neurofeedback
453 most studies present feedback stimuli in a quasi-continuous manner
454 with short update periods between 100 and 400 ms. Continuous feed-
455 back is also preferred because it provides more opportunities to assess
456 the effectiveness of a previously applied mental strategy and may as
457 well ensure task engagement. However, intermittent feedback has
458 been used as well, especially in context of fMRI-based feedback training
459 studies (e.g., Yoo and Jolesz, 2002). It has also been argued that a con-
460 tinuous updating of the feedback signal and the thereby introduced
461 cognitive load may eventually interfere with the main task. Johnson
462 et al. (2012) compared a continuous feedback (updated every func-
463 tional MR-volume) and an intermittent, blocked (feedback presented
464 after blocks of 20 s) procedure. Interestingly, they found that intermit-
465 tent feedback presentation was more effective than the continuous
466 procedure.
467 Given the various differences between studies with respect to
468 feedback design and timing it is hard to drawstrong conclusions. Com-
469 parative evaluations are lacking but are urgently needed because it is
470 to be expected that the actual signaling of feedback will be a crucial
471 determinant of learning success. Whether intermittent learning will
472 indeed prove to be superior to continuous feedback across modalities
473 needs to be determined by further assessments. Perhaps this nding
474 might turn out to be specic to fMRI: participants may fail to prot
475 from continuous feedback because of the signicant delay between
476 the mental modulation of neural events and feedback signaling the
477 outcome of their efforts. However, one has to note that these issues
478 have already been extensively studied in context of learning theory.
479 Because neurofeedback is understood as anoperant conditioning proce-
480 dure, principles of learning theory should apply here as well. Studies
481 assessing the effectiveness of reinforcement schedules suggest to utilize
482 continuous reinforcement in the initial stages of a learning paradigm,
483 which guarantees a steep learning curve. Intermittent schedules are
484 used later in the course of a training paradigm, as they support resilien-
485 cy of the previously learned behavior against extinction (e.g., Ferster
486 and Skinner, 1957). Future studies need to more directly relate to and
487 benet fromthe vast literature on learning theory and behavior modi-
488 cation (e.g., Sherlin et al., 2011).
489 3.5. Learner characteristics
490 Nowwe want to turn to the question what experimental factors and
491 learner characteristics facilitate the participants' capabilities to success-
492 fully conclude neurofeedback training. Data across studies suggest
493 that about a third of the participants ultimately can be classied as so-
494 called non-responders: subjects who do not learn to signicantly
495 modulate their brain activity over the course of the training in accor-
496 dance with instructions (e.g., Doehnert et al., 2008; Drechsler et al.,
497 2007; Fuchs et al., 2003; Kotchoubey et al., 1999). Correspondingly,
498 non-responding participants also tend not to show changes in behav-
499 ioral outcome measures (e.g., Hanslmayr et al., 2005; Lubar et al.,
500 1995). Yet, one also has to acknowledge that there is no real consensus
501 on howto actually dene success in a neurofeedback training study. For
502 example, should only the targeted frequency band show the expected
503 effects or are changes in other frequencies acceptable or should they
504 even be expected? How large should alterations in brain activity be
505 (in terms of their effect size) to be considered relevant? Or: given that
506 neurofeedback training ultimately aims at the modication of cognitive
507 capabilities, how could transfer from laboratory to real-life settings be
508 assessed best for determining training success? These are non-trivial
509 issues especially given the strong interest in the clinical application of
510 neurofeedback. Similar to drug trials, it would be important to identify
511 participants who do not respond to neurofeedback treatment as early
512 as possible. A specic denition of training success may furthermore
513 be relevant because once a participant or patient has reached training
514 goals, further training may be superuous and inefcient, the latter
515 aspect being relevant under costbenet considerations.
516 Yet, despite all these urgent issues, it also has to be acknowledged
517 that not muchis knownabout participant-characteristics that determine
518 training outcome. One of the earliest reports on responder characteris-
519 tics was provided by Gruzelier et al. (1999) who found that schizo-
520 phrenic patients were less able to modulate functional asymmetries
521 of slow cortical potentials over the motor cortex indicated problems
522 to thoroughly focus on the task at hand. Similarly, in a recent study
523 (Enriquez-Geppert et al., 2013b) via self-reports assessed whether mo-
524 tivation, commitment, or perceived training difculty was associated
525 with the outcome of a neurofeedback training of fronto-medial theta
526 oscillations. However, responders and non-responders did not differ
527 with respect to these measures. Also, anecdotal evidence from our
528 own work on fronto-medial theta modulation suggests that participants
529 can rely on very diverse strategies such as mental imaginary of colored
530 rectangles and inner singing to modulate their brain activity. Nan et al.
531 (2012) had subjects report and rate the effectiveness of strategies
532 to alter their individual alpha activity. Again, although data suggested
533 that some kind of positive thinking (e.g. about friends, love, or nature)
534 was most effective, still about 39 percent of the participants relied on
535 neutral (e.g. mental calculation) or even negatively valent (e.g. evoking
536 anger) strategies. Therefore, it is occasionally discussed whether a more
537 appropriate and effective study design would explicitly instruct subjects
538 to use a specic strategy. We are not aware, though, of published work
539 that really brought this notion to test.
540 On the other hand, it was also reported that the outcome of earlier
541 training sessions may be used to predict overall training success.
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542 Weber et al. (2011), for example, foundthat the achieved augmentation
543 of sensori-motor activity (1215 Hz) of a training incorporating a total
544 of 25 sessions could be predicted based on the outcome of the rst
545 11 sessions. The prediction model furthermore generalized across inde-
546 pendent samples. In a recent study we conceptually replicated this
547 observation: already fronto-medial theta training achievements of the
548 rst training day were highly correlated with total training outcome.
549 Furthermore, we found that training success was associated with
550 gray and white matter morphology of the midcingulate cortex, a region
551 shown to be one of the main generators of the targeted oscillatory activ-
552 ity (Enriquez-Geppert et al., in press). Similarly, Halder et al. (2013) also
553 reported that microstructural characteristics of white matter tracts such
554 as the corpus callosum, cingulate bundle, and superior fronto-occipital
555 fasciculus were associated with individual BCI-performance.
556 In conclusion, remarkably few studies addressed learner charac-
557 teristics that determine training outcome, although in neurofeedback
558 training studies the participant's ability to adapt to the training environ-
559 ment constitutes a much more critical factor than in most other BCI
560 applications. A serious adaptation of relevant procedures for clinical
561 treatment strongly relies ona thoroughinvestigationof the patients' de-
562 terminants for training success, as well as a more stringent denition
563 training goals and necessary transfer effects.
564 4. Specic characteristics and requirements of neurofeedback BCIs
565 As has become clear from previous sections, neurofeedback BCIs
566 come with some peculiarities that differentiate them from applications
567 in related elds. Their strong association with clinical research has a
568 dominant impact on this subgroup of BCIs. Indeed, it is currently being
569 discussed whether or not neurofeedback trainings for treatment of
570 mental disorders should undergo assessment under regulations manda-
571 tory for clinical trials (Lofthouse et al., 2012). Altogether, this makes
572 research on and the development of neurofeedback BCIs much more
573 costly in terms of both time and interdisciplinary staff. Although the im-
574 pact on basic research may be less pronounced, an adaptation of the re-
575 search agenda seems necessary. Our earlier discussions suggest that the
576 participant as anactively engaged learner may need to become a clearer
577 focus of further study.
578 On the other hand, differences should as well be found regarding
579 specications for implementations of neurofeedback BCIs. Given that
580 the majority of researchers on neurofeedback does not have a back-
581 groundincomputer science or machine learning, relevant BCIs optimally
582 should be distributed as ready-to-use software packages with adequate
583 procedures for artifact handling and feature generation/extraction. With
584 respect to the latter, features should still provide meaningful informa-
585 tion to the user of the software. At last, one also has to consider that ap-
586 propriate control conditions are an essential specic of neurofeedback
587 studies. Hence, an implementation of a neurofeedback BCI should
588 not only be suited to process the data of a single subject, but also to han-
589 dle multi-subject data, optimally including routines for pseudo-/sham-
590 feedback and appropriate experimenter blinding.
591 5. Software for neurofeedback training
592 In this section we shortly address software systems potentially suit-
593 ed to implement neurofeedback BCIs. We will start with a discussion of
594 open-source software packages that have already beeninuse andwhich
595 had some impact on the eld. Then, we introduce our own software sys-
596 tem, NeuroFeedback Suite (version 1.0), which we will make freely
597 available alongside this article.
598 5.1. Open source software packages
599 The most inuential software specically tailored towards BCI re-
600 search is BCI2000, which represents a joint project of the Wadsworth
601 Center of the New York State Department of Health in Albany, New
602 York, USA, and the University of Tbingen, Germany (http://www.
603 bci2000.org). BCI2000 is written in C++ and applies object-oriented
604 programming techniques. This enables high modularity and reusability
605 of the code. It has been designed as a general purpose systemfor BCI re-
606 search and supplies implementations of routines for all processing steps
607 specied above. For example, the software out-of-the-box supports sev-
608 eral data acquisition systems for EEG and MEG recordings and provides
609 interfaces for external programming environments such as MATLAB.
610 A general limitation of such multi-purpose packages is that usually the
611 setup of a given BCI design needs further self-made implementations
612 on the user side. This, for example, is the case with routines for the pre-
613 sentation of the feedback signal. Here, BCI2000 provides a base class
614 (the FeedbackTask class) from which the user has to derive and build
615 and Q6 own pipeline for stimulus presentation.
616 A similar approach was taken by the Graz BCI Lab, Austria, which
617 also provides a number of C++ libraries to be used to build a user-
618 designed BCI, potentially also for neurofeedback purposes (http://bci.
619 tugraz.at/software). Again, modules are built from classes and imple-
620 ment basic functions for data acquisition from several EEG systems,
621 real-time visualization of biosignals, as well as data processing via clas-
622 siers. These libraries also provide ample opportunities to engage exter-
623 nal programming environments (e.g., MATLAB). The implementation of
624 these libraries is sparser though and aims at lower-level access when
625 compared to BCI2000.
626 Both software packages, BCI2000 and the Graz BCI libraries, are
627 well documented and come with worked examples that signicantly
628 decrease the time needed to prepare an implementation of a user-
629 designed BCI. However, a potential user interested in a neurofeedback
630 application will need intermediate programming skills in order to
631 bind module functionality, adapt already existing routines, and imple-
632 ment those elements not yet included in the packages (e.g. for the
633 visualization of the feedback signal). Both packages aim at the research
634 community and are free to use.
635 Another general purpose software package for BCI introduced in
636 its full only a few years ago is OpenViBE (http://openvibe.inria.fr). This
637 software package is comparably user-friendly because it not only is
638 distributed via windows executables but the source code is provided
639 as well, thereby guaranteeing high cross-platform compatibility. More
640 importantly though, it provides a graphical programming interface.
641 That is, potential users can build the core of their BCI system in a drag-
642 and-drop manner. OpenViBE comes with a high number of modules
643 supporting all processing steps discussed above, although the visualiza-
644 tion of an appropriate neurofeedback signal again might necessitate
645 additional implementations by the user.
646 The latest free software release aiming at general BCI research
647 applications that already received quite some attention is BCILAB
648 (http://sccn.ucsd.edu/wiki/BCILAB). It is developed at the Swartz Center
649 for Computational Neuroscience, University of California San Diego,
650 USA. It is a MATLAB-based toolbox that offers strong integrability with
651 other software packages developed in the same lab, of which EEGLAB
652 is the most widely known one.
653 Note, that none of the software packages just introduced specically
654 aimat neurofeedback trainings, but rather provide a general framework
655 for designing BCIs. Whereas this maximizes the usability and exibility
656 of the solutions provided, it comes at the disadvantage that potential
657 users less adept inprogramming will encounter problems implementing
658 their own neurofeedback BCI. This might be especially problematic
659 since a substantial part of the target group will be comprised of clinical
660 and psychological practitioners. Note, however, that more recently
661 some companies, specialized in providing equipment for clinical use,
662 also complemented their product list with software packages more
663 directly aiming at bio- or neurofeedback applications. Nevertheless, all
664 software packages known to us focus on the design and optimization
665 of BCIs for single participants. Yet, neurofeedback training studies and
666 clinical trials come with the need for multi-subject management, be-
667 cause they require conditions featuring pseudo- or sham-training and
6 R.J. Huster et al. / International Journal of Psychophysiology xxx (2013) xxxxxx
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(2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.08.011
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668 potential experimenter blinding. This is one of the specications met
669 with our own software system that will be introduced next.
670 5.2. NeuroFeedback Suite 1.0
671 To address some of the issues discussed above, we designed our own
672 BCI software specically aiming at its applicationfor neurofeedback train-
673 ing studies. This software, developed under the name NeuroFeedback
674 Suite (NFS, version 1.0) and running under MATLAB, has evolved from
675 applications used for our own neurofeedback training studies (see
676 Fig. 2). NFS will be made freely available in parallel to this article
677 here: http://sourceforge.net/p/nfsuite/(available from May, 20th, 2013,
678 at latest). NFS specically intends to provide researchers direct and un-
679 complicated access to a ready-to-use neurofeedback software without
680 further need for implementing any modules. Although in its rst and
681 current version the individualization of the system is somewhat limited,
682 we plan to integrate many new options in due time. We will shortly go
683 through the single processing steps highlighting some features, in the
684 end furthermore discussing truly unique characteristics of this package.
685 Inthis initial release NFS natively supports real-time recordings of EEG
686 ampliers of BrainProducts' BrainAmp family (www.brainproducts.com)
687 using the Transmission Control Protocol. Beyond online lters already
688 applied during data recording, additional processing steps further en-
689 sure signal quality. These optional steps comprise FFT-based ltering
690 as well as a procedure for the detection and rejection of eye artifacts.
691 The latter is implemented as a two stage procedure. First, during a cali-
692 bration phase (usually about three minutes long) EEG as well as ocular
693 activity is recorded. Initially, a simple amplitude threshold for the detec-
694 tion of blinks is used; this threshold can be adjusted individually
695 to optimize detection performance. Then, epochs of a total width of
696 two seconds centered around a blink's peak activity are extracted
697 automatically and an average amplitude spectrum is computed. The
698 peak within this amplitude spectrum denes a center-frequency and a
699 frequency band is dened by cut-off frequencies three Hz. Subse-
700 quently, mean amplitude and standard deviation for this frequency
701 band are derived. During the actual neurofeedback, the activity in
702 this subject-specic, artifact-associated frequency band is monitored.
703 Segments with mean amplitudes higher than the initial mean activity
704 minus one standard deviation are rejected. However, given the substan-
705 tial amount of inter-individual variability of artifact-induced time-
706 courses, all of these settings can be adjusted individually to optimize
707 performance. In this initial release of NFS, feature extraction follows
708 the predominant paradigm in the literature in that the amplitude or
709 power of a specied frequency band can be extracted and fed back.
710 The feedback signal consists of a visually presented colored square
711 with graded color intensity ranging from blue (lower than reference)
712 over gray to red (higher than reference). The reference value for this
713 comparison, for example, is the mean amplitude in the specied fre-
714 quency band computed from artifact-free segments of a baseline mea-
715 surement taken before the training sessions.
716 During study setup, one can dene the order of training stages in-
717 cluding artifact calibration, start/end baseline measurements, as well
718 as the number and duration of the actual training blocks and training
719 sessions/days. Also, study defaults canbe set for a number of parameters
720 (e.g. initial amplitude thresholds or feedback frequency band), which
721 are automatically adopted for the subjects assigned to the study. Later,
722 these values can be modied individually for each subject and parame-
723 ter values are stored andmanagedacross training sessions. For example,
724 individual center frequencies and frequency bands can be dened for
725 each subject enabling highly individualized trainings.
726 A truly unique feature of this software is its capability to manage
727 multi-subject data within a single study (Fig. 3), thereby supporting an
728 easy application of pseudo-/sham-neurofeedback. When incorporating
729 a subject in the study, it is possible to simply enlist it for pseudo-
730 feedback by matching it with another subject of the proper feedback
731 condition. This way, the subject receives a replay of the corresponding
732 training block of the matched subject. However, actual EEG and eye ac-
733 tivity of this subject are still recorded and feedback is suspended upon
734 the detection of a blink as in a real recording, thereby substantially
735 increasing the credibility of the pseudo feedback. This design is ideally
Fig. 2. Main interface of NeuroFeedback Suite. The main user interface provides panels with subject information (A), a copy of the screen presented to the subjects overlayed with the
current experimental stage and the session history (B and C, respectively), as well as signal displays for time-series data and their spectral composition (D and E, respectively). Note,
that panel A indicates that the current subject undergoes proper neurofeedback training (Normal User). A participant of the pseudo group would receive sham neurofeedback based
on the replay of the recorded signal of a matched participant (Linked Subject).
7 R.J. Huster et al. / International Journal of Psychophysiology xxx (2013) xxxxxx
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(2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.08.011
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736 suited to implement double blind trials by blocking the experimenter's
737 access to the subject matching necessary for pseudo-feedback. The
738 latter information then has to and can only be managed by a study-
739 administrator but not the actual experimenter. The implementation of
740 such procedures is necessary, because potential treatment procedures
741 have to undergo stringent assessment including blinding of both partic-
742 ipants and experimenters. The architecture for full double-blinding will
743 be available with an upcoming update.
744 Additional features planned for the next release are ICA for artifact
745 correction, features based on FFT-derived frequency-band ratios and
746 independent component activity proles, as well as the support of addi-
747 tional EEG systems. Potential users with special requirements of course
748 may still modify the freely available source code.
749 6. Discussion
750 Looking back at this synopsis a number of interesting conclu-
751 sions can be drawn. Since its advance in the early nineteen-seventies
752 neurofeedback has triggered a large number of seminal studies, with
753 clinically-oriented evaluations prevailing. Hence, despite reviews and
754 meta-analyses clearly attesting to the efcacy of neurofeedback training
755 procedures, much of our basic knowledge on the mechanisms of action
756 and their potential optimization is still unknown. Similarly, whereas BCI
757 applications inother elds technically matureddue to strong input from
758 specialists incomputer and engineering sciences, the basic methodology
759 of interfaces for neurofeedback has not changed much. It is obvious that
760 current neurofeedback training procedures could undergo signicant
761 advancement given an adjustment of relevant research agendas. This
762 is even more the case since the technology for mobile BCIs matured
763 noticeably, opening the possibility for neurofeedback trainings as ambu-
764 latory and at-home treatment procedures.
765 It is interesting to note that, despite the many successful studies,
766 some undeniable skepticism still surrounds neurofeedback trainings.
767 This is, in our opinion, due to methodological shortcomings of early
768 studies that often did not implement appropriate control conditions.
769 Yet, as recent reviews and meta-analyses unquestionably showed,
770 mediumto large effects can regularly be observed with respect to alter-
771 ations in brain activity that often even occur concurrently with changes
772 in behavior and cognitive performance (e.g., Arns et al., 2009; Keizer
773 et al., 2010; Lofthouse et al., 2012). However, the specicity of the ob-
774 served training effects is somewhat unclear. In terms of changes in the
775 EEG, many studies show that effects are not exclusively found in the
776 targeted frequency range, but also with respect to other EEG oscilla-
777 tions. We assume that training specicity will to a large degree depend
778 on the feature extracted. Thus, directly relaying the raw activity of the
779 target frequency might produce less specic outcome than a relative
780 measure that relies on the ratio of the target and surrounding frequen-
781 cies. Ona related issue, optimal characteristics for the designof the feed-
782 back signal still need to be determined. Would an optimal feedback rely
783 on a single signal, or might a multi-component learning signal with in-
784 structions to increase brain activity indexed by the one but to decrease
785 that indexed by the second signal be more efcient? Is there an optimal
786 delay betweenbrainrecording andfeedback presentation? Does one ac-
787 tually benet from continuous feedback or would a blocked feedback
788 (e.g., every minute) be even more efcient? These are only some of
789 the questions that urgently need to be examined. Much may be gained,
790 however, from assessing the literature on learning theory principles.
791 In a recent review, for example, Sherlin et al. (2011) directly relate
792 neurofeedback research to operant conditioning studies in other elds,
793 thereby providing a comparison which may well guide the design of fu-
794 ture neurofeedback studies. Beyondthat, too muchis unknown on what
795 learner characteristics are benecial and predictive for training out-
796 come. It seems that pre-training brain structure and function, as well
797 as early training achievements might turn out as relevant predictors
798 for ultimate training responsivity. All these issues need additional con-
799 sideration before neurofeedback trainings can undergo evaluations
800 in terms of clinical trials. Research agendas in both clinical as well as
801 basic science need to undergo adjustment in order to have a fair chance
802 to ultimately reach this goal.
803 On the other hand, it is somewhat unfortunate that substantial
804 methodological developments in BCI research have not been trans-
805 ferred to neurofeedback applications. This can be seen in procedures
Fig. 3. Graphical user interface for study and subject management. Panel A provides a list of the subjects enrolled in a given study. When selecting a subject, relevant information is
displayed in panels A and B, the latter providing an overview of the already completed sessions and experimental stages. Should a subject be added to the study or information needs
to be edited, a second user interface opens to enter basic information and to assign the user type (Normal User or Pseudo User).
8 R.J. Huster et al. / International Journal of Psychophysiology xxx (2013) xxxxxx
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806 for the processing of artifacts, but becomes most obvious when it comes
807 to feature generation and feature extraction. Nearly all studies known to
808 us exclusively rely on frequency-based information, which necessarily
809 represents a spatio-temporal overlap of many simultaneously active
810 brain systems. It is to be expected that machine learning applications
811 suchas ICAmay positively impact neurofeedback trainings by increasing
812 a feature's signal to noise ratio and its specicity. Whereas these issues
813 rather relate to the algorithmic optimization of neurofeedback BCIs,
814 we also pointed out that their design needs more consideration in
815 terms of usability. Whereas BCIs in general are an active eld for
816 computer scientists and engineers, neurofeedback BCIs so far have not
817 much benetted. However, given that a majority of potential users
818 comes from clinical and psychological science, software packages with
819 a low level of abstraction and with support for multi-subject and study
820 handling are urgently needed. Because of the current lack of such soft-
821 ware packages specically aiming at neurofeedback BCIs, we introduced
822 our NeuroFeedback Suite that will undergo continued development in
823 order to address current shortcomings.
824 Summarizing, neurofeedback trainings proved to be efcacious pro-
825 cedures for the modulation of brain activity, cognition and behavior.
826 Much remains to be learned though regarding both underlying learning
827 mechanisms and characteristics for an optimal training outcome. With
828 respect to the implementation of neurofeedback BCIs, much is to be
829 gained by further algorithmic and design optimization, especially
830 when considering the special prerequisites of their users and relevant
831 study designs.
832 7. Q7 Uncited reference
833 Enriquez-Geppert et al., 2013c
834 Acknowledgments
835 This work was partially supported by the Deutsche
836 Forschungsgemeinschaft (DFG grant number: HU1729/2-1, awarded
837 to RJH and CSH).
838 References
839 Arns, M., de Ridder, S., Strehl, U., Breteler, M., Coenen, A., 2009. Efcacy of neurofeedback
840 treatment in ADHD: the effects on inattention, impulsivity and hyperactivity: a meta-
841 analysis. Clin. EEG Neurosci. 40, 180189.
842 Bartels, G., Shi, L.-C., Lu, B.-L., 2010. Automatic artifact removal from EEG a mixed
843 approach based on double blind source separation and support vector machine.
844 Conf. Proc. IEEE Eng. Med. Biol. Soc. 2010, 53835386.
845 Becerra, J., Fernndez, T., Roca-Stappung, M., Daz-Comas, L., Galn, L., Bosch, J., Espino, M.,
846 Moreno, A.J., Harmony, T., 2012. Neurofeedback in healthy elderly human subjects
847 with electroencephalographic risk for cognitive disorder. J. Alzheimers Dis. 28,
848 357367.
849 Birbaumer, N., Ramos Murguialday, A., Weber, C., Montoya, P., 2009. Neurofeedback and
850 braincomputer interface clinical applications. Int. Rev. Neurobiol. 86, 107117.
851 Buzski, G., Anastassiou, C.A., Koch, C., 2012. The origin of extracellular elds and
852 currentsEEG, ECoG, LFP and spikes. Nat. Rev. Neurosci. 13, 407420.
853 Cihan Gani, N.B., 2008. Long term effects after feedback of slow cortical potentials and
854 of thetabeta-amplitudes in children with attentiondecit/hyperactivity disorder
855 (ADHD). Int. J. Bioelectromagn. 10, 209232.
856 Croft, R.J., Chandler, J.S., Barry, R.J., Cooper, N.R., Clarke, A.R., 2005. EOG correction: a com-
857 parison of four methods. Psychophysiology 42, 1624.
858 De Vos, M., De Lathauwer, L., Van Huffel, S., 2011. Spatially constrained ICA algorithm
859 with an application in EEG processing. Signal Process. 91, 19631972.
860 De Zambotti, M., Bianchin, M., Magazzini, L., Gnesato, G., Angrilli, A., 2012. The efcacy of
861 EEG neurofeedback aimed at enhancing sensory-motor rhythmtheta ratio in healthy
862 subjects. Exp. Brain Res. 221, 6974.
863 Debener, S., Minow, F., Emkes, R., Gandras, K., De Vos, M., 2012. How about taking a low-
864 cost, small, and wireless EEG for a walk? Psychophysiology 49, 14491453.
865 deCharms, R.C., Maeda, F., Glover, G.H., Ludlow, D., Pauly, J.M., Soneji, D., Gabrieli, J.D.E.,
866 Mackey, S.C., 2005. Control over brain activation and pain learned by using real-
867 time functional MRI. Proc. Natl. Acad. Sci. U. S. A. 102, 1862618631.
868 Doehnert, M., Brandeis, D., Straub, M., Steinhausen, H.-C., Drechsler, R., 2008. Slowcortical
869 potential neurofeedback in attention decit hyperactivity disorder: is there neuro-
870 physiological evidence for specic effects? J. Neural Transm. 115, 14451456.
871 Dohrmann, K., Elbert, T., Schlee, W., Weisz, N., 2007a. Tuning the tinnitus percept by
872 modication of synchronous brain activity. Restor. Neurol. Neurosci. 25, 371378.
873 Dohrmann, K., Weisz, N., Schlee, W., Hartmann, T., Elbert, T., 2007b. Neurofeedback for
874 treating tinnitus. Prog. Brain Res. 166, 473485.
875 Drechsler, R., Straub, M., Doehnert, M., Heinrich, H., Steinhausen, H.-C., Brandeis, D., 2007.
876 Controlled evaluation of a neurofeedback training of slow cortical potentials in chil-
877 dren with Attention Decit/Hyperactivity Disorder (ADHD). Behav. Brain Funct. 3, 35.
878 Egner, T., Sterman, M.B., 2006. Neurofeedback treatment of epilepsy: from basic rationale
879 to practical application. Expert. Rev. Neurother. 6, 247257.
880 Q8 Enriquez-Geppert, S., Huster, R.J., Scharfenort, R., Mokom, Z.N., Vosskuhl, J., Figge, C.,
881 Zimmermann, J., Herrmann, C.S., 2013. The morphology of the midcingulate cortex
882 redicts frontal-midline theta neurofeedback success. Front. Hum. Neurosci. Q9
883 Enriquez-Geppert, S., Huster, R.J., Herrmann, C.S., 2013b. Boosting brain functions:
884 improving executive functions with behavioral training, neurostimulation, and
885 neurofeedback. Int. J. Psychophysiol. Q10
886 Enriquez-Geppert, S., Huster, R.J., Scharfenort, R., Mokom, Z.N., Zimmermann, J., Herrmann,
887 C.S., 2013c. Modulation of frontal-midline theta by neurofeedback. Biol. Psychol. Q11
888 Erfanian, A., Mahmoudi, B., 2005. Real-time ocular artifact suppression using recurrent
889 neural network for electro-encephalogram based braincomputer interface. Med.
890 Biol. Eng. Comput. 43, 296305 (.f).
891 Ferster, C.B., Skinner, B.F., 1957. Schedules of Reinforcement. Appleton-Century-Crofts,
892 New York.
893 Fuchs, T., Birbaumer, N., Lutzenberger, W., Gruzelier, J.H., Kaiser, J., 2003. Neurofeedback
894 treatment for attention-decit/hyperactivity disorder in children: a comparison
895 with methylphenidate. Appl. Psychophysiol. Biofeedback 28, 112.
896 Gao, J., Zheng, C., Wang, P., 2010. Online removal of muscle artifact from electroencepha-
897 logram signals based on canonical correlation analysis. Clin. EEG Neurosci. 41, 5359.
898 Gratton, G., Coles, M.G., Donchin, E., 1983. A new method for off-line removal of ocular
899 artifact. Electroencephalogr. Clin. Neurophysiol. 55, 468484.
900 Gruzelier, J., Hardman, E., Wild, J., Zaman, R., 1999. Learned control of slow potential
901 interhemispheric asymmetry in schizophrenia. Int. J. Psychophysiol. 34, 341348.
902 Halder, S., Varkuti, B., Bogdan, M., Kbler, A., Rosenstiel, W., Sitaram, R., Birbaumer, N.,
903 2013. Prediction of braincomputer interface aptitude from individual brain struc-
904 ture. Front. Hum. Neurosci. 7, 105.
905 Hammond, D.C., 2005. Neurofeedback with anxiety and affective disorders. Child Adolesc.
906 Psychiatr. Clin. N. Am. 14, 105123 (vii).
907 Hanslmayr, S., Sauseng, P., Doppelmayr, M., Schabus, M., Klimesch, W., 2005. Increasing
908 individual upper alpha power by neurofeedback improves cognitive performance in
909 human subjects. Appl. Psychophysiol. Biofeedback 30, 110.
910 Hinterberger, T., Kbler, A., Kaiser, J., Neumann, N., Birbaumer, N., 2003. A braincomputer
911 interface (BCI) for the locked-in: comparison of different EEG classications for the
912 thought translation device. Clin. Neurophysiol. 114, 416425.
913 Javidi, S., Mandic, D.P., Took, C.C., Cichocki, A., 2011. Kurtosis-based blind source extrac-
914 tion of complex non-circular signals with application in EEG artifact removal in
915 real-time. Front. Neurosci. 5, 105.
916 Jensen, M.P., Hakimian, S., Sherlin, L.H., Fregni, F., 2008. Newinsights into neuromodulatory
917 approaches for the treatment of pain. J. Pain 9, 193199.
918 Johnson, K.A., Hartwell, K., LeMatty, T., Borckardt, J., Morgan, P.S., Govindarajan, K., Brady,
919 K., George, M.S., 2012. Intermittent real-time fMRI feedback is superior to continu-
920 ous presentation for a motor imagery task: a pilot study. J. Neuroimaging 22, 5866.
921 Kamiya, J., 1971. Biofeedback training in voluntary control of EEG alpha rhythms. Calif.
922 Med. 115, 44.
923 Keizer, A.W., Verment, R.S., Hommel, B., 2010. Enhancing cognitive control through
924 neurofeedback: a role of gamma-band activity in managing episodic retrieval.
925 NeuroImage 49, 34043413.
926 Kotchoubey, B., Busch, S., Strehl, U., Birbaumer, N., 1999. Changes in EEG power spectra
927 during biofeedback of slow cortical potentials in epilepsy. Appl. Psychophysiol.
928 Biofeedback 24, 213233.
929 Lemm, S., Blankertz, B., Curio, G., Mller, K.R., 2005. Spatio-spectral lters for improving
930 the classication of single trial EEG. IEEE Trans. Biomed. Eng. 52, 15411548.
931 Linden, D.E.J., Habes, I., Johnston, S.J., Linden, S., Tatineni, R., Subramanian, L., Sorger, B.,
932 Healy, D., Goebel, R., 2012. Real-time self-regulation of emotion networks in patients
933 with depression. PLoS One 7, e38115.
934 Lins, O.G., Picton, T.W., Berg, P., Scherg, M., 1993a. Ocular artifacts in EEG and event-
935 related potentials. I: scalp topography. Brain Topogr. 6, 5163.
936 Lins, O.G., Picton, T.W., Berg, P., Scherg, M., 1993b. Ocular artifacts in recording EEGs and
937 event-related potentials. II: source dipoles and source components. Brain Topogr. 6,
938 6578.
939 Lofthouse, N., Arnold, L.E., Hurt, E., 2012. Current status of neurofeedback for attention-
940 decit/hyperactivity disorder. Curr. Psychiatry Rep. 14, 536542.
941 Lubar, J.F., Swartwood, M.O., Swartwood, J.N., O'Donnell, P.H., 1995. Evaluation of the
942 effectiveness of EEG neurofeedback training for ADHD in a clinical setting as mea-
943 sured by changes in T.O.V.A. scores, behavioral ratings, and WISC-R performance.
944 Biofeedback Self Regul. 20, 8399.
945 Mennes, M., Wouters, H., Vanrumste, B., Lagae, L., Stiers, P., 2010. Validation of ICA as a tool
946 to remove eye movement artifacts from EEG/ERP. Psychophysiology 47, 11421150.
947 Mihara, M., Miyai, I., Hattori, N., Hatakenaka, M., Yagura, H., Kawano, T., Okibayashi, M.,
948 Danjo, N., Ishikawa, A., Inoue, Y., Kubota, K., 2012. Neurofeedback using real-time
949 near-infrared spectroscopy enhances motor imagery related cortical activation.
950 PLoS One 7, e32234.
951 Nan, W., Rodrigues, J.P., Ma, J., Qu, X., Wan, F., Mak, P.-I., Mak, P.U., Vai, M.I., Rosa, A.,
952 2012. Individual alpha neurofeedback training effect on short term memory. Int.
953 J. Psychophysiol. 86, 8387.
954 Noureddin, B., Lawrence, P.D., Birch, G.E., 2012. Online removal of eye movement and blink
955 EEGartifacts using a high-speed eye tracker. IEEE Trans. Biomed. Eng. 59, 21032110.
956 Ros, T., Thberge, J., Frewen, P.A., Kluetsch, R., Densmore, M., Calhoun, V.D., Lanius, R.A.,
957 2013. Mind over chatter: plastic up-regulation of the fMRI salience network directly
958 after EEG neurofeedback. NeuroImage 65, 324335.
9 R.J. Huster et al. / International Journal of Psychophysiology xxx (2013) xxxxxx
Please cite this article as: Huster, R.J., et al., Braincomputer interfaces for EEG neurofeedback: Peculiarities and solutions, Int. J. Psychophysiol.
(2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.08.011
U
N
C
O
R
R
E
C
T
E
D

P
R
O
O
F
959 Salari, N., Bchel, C., Rose, M., 2012. Functional dissociation of ongoing oscillatory brain
960 states. PLoS One 7, e38090.
961 Sannelli, C., Vidaurre, C., Muller, K.R., Blankertz, B., 2010. Commonspatial patternpatches
962 an optimized lter ensemble for adaptive braincomputer interfaces. Conf. Proc. IEEE
963 Eng. Med. Biol. Soc. 2010, 43514354.
964 Scherer, R., Faller, J., Balderas, D., Friedrich, E.V.C., Prll, M., Allison, B., Mller-Putz, G.,
965 2013. Braincomputer interfacing: more than the sum of its parts. Soft. Comput. 17,
966 317331.
967 Sherlin, L.H., Arns, M., Lubar, J., Heinrich, H., Kerson, C., Strehl, U., Sterman, M.B., 2011.
968 Neurofeedback and basic learning theory: implications for research and practice.
969 J. Neurother. 15, 292304.
970 Sokhadze, T.M., Cannon, R.L., Trudeau, D.L., 2008. EEG biofeedback as a treatment for sub-
971 stance use disorders: review, rating of efcacy, and recommendations for further
972 research. Appl. Psychophysiol. Biofeedback 33, 128.
973 Sterman, M.B., Egner, T., 2006. Foundation and practice of neurofeedback for the treat-
974 ment of epilepsy. Appl. Psychophysiol. Biofeedback 31, 2135.
975 Subramanian, L., Hindle, J.V., Johnston, S., Roberts, M.V., Husain, M., Goebel, R., Linden, D.,
976 2011. Real-time functional magnetic resonance imaging neurofeedback for treatment
977 of Parkinson's disease. J. Neurosci. 31, 1630916317.
978 Sudre, G., Parkkonen, L., Bock, E., Baillet, S., Wang, W., Weber, D.J., 2011. rtMEG: a real-
979 time software interface for magnetoencephalography. Comput. Intell. Neurosci.
980 (2011, 327953). Q12
981 Weber, E., Kberl, A., Frank, S., Doppelmayr, M., 2011. Predicting successful learning of
982 SMR neurofeedback in healthy participants: methodological considerations. Appl.
983 Psychophysiol. Biofeedback 36, 3745.
984 Yoo, S.-S., Jolesz, F.A., 2002. Functional MRI for neurofeedback: feasibility study on a hand
985 motor task. NeuroReport 13, 13771381.
986 Zaehle, T., Herrmann, C.S., 2011. Neural synchrony and white matter variations in the
987 humanbrainrelationbetweenevoked frequency andcorpus callosummorphology.
988 Int. J. Psychophysiol. 79, 4954.
989 Zoefel, B., Huster, R.J., Herrmann, C.S., 2011. Neurofeedback training of the upper alpha
990 frequency band in EEG improves cognitive performance. NeuroImage 54, 14271431.
991
992
10 R.J. Huster et al. / International Journal of Psychophysiology xxx (2013) xxxxxx
Please cite this article as: Huster, R.J., et al., Braincomputer interfaces for EEG neurofeedback: Peculiarities and solutions, Int. J. Psychophysiol.
(2013), http://dx.doi.org/10.1016/j.ijpsycho.2013.08.011