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journal homepage: www.intl.elsevierhealth.com/journals/cmpb

An EEGLAB plugin to analyze individual EEG alpha


rhythms using the “channel reactivity-based
method”

A. Goljahani a , P. Bisiacchi b , G. Sparacino a,∗


a Department of Information Engineering, University of Padova, via Gradenigo 6/B, 35131 Padova, Italy
b Department of General Psychology, University of Padova, via Venezia 8, 35131 Padova, Italy

a r t i c l e i n f o a b s t r a c t

Article history: A recent paper [1] proposed a new technique, termed the channel reactivity-based method
Received 17 August 2012 (CRB), for characterizing EEG alpha rhythms using individual (IAFs) and channel (CAFs) alpha
Received in revised form frequencies. These frequencies were obtained by identifying the frequencies at which the
16 December 2013 power of the alpha rhythms decreases. In the present study, we present a graphical interac-
Accepted 18 December 2013 tive toolbox that can be plugged into the popular open source environment EEGLAB, making
it easy to use CRB. In particular, we illustrate the major functionalities of the software and
Keywords: discuss the advantages of this toolbox for common EEG investigations. The CRB analysis
CRB analysis plugin plugin, along with extended documentation and the sample dataset utilized in this study,
Individual alpha frequency (IAF) is freely available on the web at http://bio.dei.unipd.it/crb/.
Channel alpha frequency (CAF) © 2013 Elsevier Ireland Ltd. All rights reserved.
Reactivity index
Alpha de-synchronization
Event-related de-synchronization

in task demand will have opposite effects on the power of


1. Introduction the alpha and theta band rhythms of an EEG. The power of
the EEG rhythms in the theta band (conventional range of (4,
Individual alpha frequency (IAF) is one of the most commonly 7) Hz) increases (synchronization), whereas the power of the
utilized tools to correlate the variability of EEG rhythms among rhythms in the alpha band (conventional range of (8, 13) Hz)
subjects to anatomic, genetic, and behavioral/cognitive traits decreases (de-synchronization) (e.g., see [9–11]). In particular,
and to individually tune conventional theta and alpha bands for each scalp position, the CRB identifies the frequency inter-
(e.g., see [2–8], and the references quoted therein). Recently, val at which the alpha power decreases; then, using these
the channel reactivity-based method (CRB) [1] was proposed intervals, the CRB computes several channel alpha frequen-
to measure IAFs by identifying the EEG power variations that cies (CAFs) and one IAF for each dataset.
are specific to each subject. The method relies on the evi- Our goal was to facilitate the use of CRB in neuroscien-
dence that, in most cases, a suitable stimulus or an increase tific/clinical investigations, which may benefit from adaptively


Corresponding author. Tel.: +39 0498277741; fax: +39 0498277699.
E-mail addresses: anahita.goljahani@dei.unipd.it (A. Goljahani), patrizia.bisiacchi@unipd.it (P. Bisiacchi),
gianni@dei.unipd.it (G. Sparacino).
URL: http://www.dei.unipd.it/∼gianni (G. Sparacino).
0169-2607/$ – see front matter © 2013 Elsevier Ireland Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.cmpb.2013.12.010
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identifying the alpha frequency intervals instead of using the activity (e.g., the interval of (7.5, 13) Hz in Fig. 1(b)). As illus-
conventional (8, 13) Hz band. Therefore, in this manuscript trated in Fig. 1(c), (fa ,fb ) is expanded leftward until R(f) and
we present an interactive graphical software toolbox, the CRB T(f) intersect and rightward until R(f) and T(f) are close enough
analysis plugin; this set of MATLAB® (The Mathworks Inc.) to consider the alpha modulation activity to be finished. The
routines was designed to be plugged into the popular open required closeness is regulated by a parameter ε. As ε becomes
source platform EEGLAB [12]. increasingly less than 1, R(f) and T(f) must become closer for
The manuscript is organized as follows. First, in Section 2, the alpha interval to be considered finished. In the example
a brief review of CRB is given. Next, in Section 3, the func- of Fig. 1(c), ε = 0.5, and the initial interval (8, 11) Hz is correctly
tionalities of the CRB analysis plugin (e.g., selecting data for expanded to the interval of (7.5, 13) Hz
analysis, applying the method, and inspecting the results) are
described and then illustrated using a sample EEG dataset.
Step 2. Step 2 selects the channels with the strongest alpha
Lastly, in Section 4, possible applications of the software in
de-synchronizations relative to the subject’s alpha activity.
common neuroscientific investigations are discussed.
A reference maximum de-synchronization intensity max is
obtained by computing the pth percentile of the set of  val-
2. Review of the CRB method ues computed in Step 1. The CRB parameter p (e.g., 80% or
90%) regulates the sensitivity of the subject’s max to isolated
CRB compares the EEG data of a test state to that of a reference high  values. Channels are then selected if their  is suffi-
state by means of a power spectral density (PSD) approach ciently close to max . Specifically, the minimum  required for
[13,14]; any alpha de-synchronization that may occur when a channel to be selected is given by sub = r·max , where r is the
the subject changes from one state to another is identified. CRB parameter that determines the closeness of the threshold
Fig. 1(a) illustrates the CRB for a sample EEG recorded from sub to max . Before computing max , channels can be discarded
N scalp locations. First, for each channel, the CRB computes independent of the alpha activity of the subject by setting the
the power spectral densities relative to the reference and CRB parameter min to a value greater than 0. In this case, the
test states (denoted as R(f) and T(f), respectively). Then, CRB channels with  values smaller than min do not affect the
performs the three steps that are summarized below and determination of max through the percentile operator.
described in detail by Goljahani et al. [1].
Step 3. For all of the selected channels, CAFs are computed
Step 1. For each channel, the alpha de-synchronization as
interval f = (f1 ,f2 ) is identified by applying a “scanning and
expansion” procedure to the corresponding R(f) and T(f). Then,  f2
f1
R(f )fdf
the intensity of the alpha de-synchronization in (f1 ,f2 ) is quan- f˛ =  f2 , (2)
tified using the reactivity index  (␮V2 /Hz) f1
R(f )df

 f2
f1
(R(f ) − T(f ))df where (f1 ,f2 ) are the channel de-synchronization intervals
= (1)
(f2 − f1 ) identified in Step 1. Eq. (2) corresponds to the weighted aver-
age of the frequencies in (f1 ,f2 ), with weights proportional to
which measures the average decrease in power from the ref- the power of those frequencies in the reference state. Lastly,
erence state to the test state for each frequency unit in (f1 ,f2 ). the IAF is computed as the median of the CAFs.

The “scanning and expansion” procedure operates as fol-


The reader is referred to [1] for more details, particularly
lows. During the scanning phase (illustrated in Fig. 1(b) for
about the meaning of the seven CRB parameters (i.e., wsize ,
a representative channel), an initial frequency interval (fa ,fb )
wshift , , and ε in Step 1 and p, r, and min in Step 2) and for
is found within the alpha de-synchronization interval of the
general guidelines for setting these parameters.
channel. To do so, the frequency axis is divided into a series of
Goljahani et al. [1] demonstrated that the parameterized
overlapping frequency intervals, which are obtained by shif-
procedures of the CRB successfully adapted to the quite dif-
ting a window whose size and shift are determined by the CRB
ferent individual characteristics of the EEG rhythms of the 19
parameters wsize and wshift . For all intervals, the correspond-
studied subjects, even in cases without unique clear peaks in
ing de-synchronization intensities ’s are computed using Eq.
the reference PSD. Moreover, the CRB proved to be effective
(1). The intensities relative to the intervals above the conven-
both in flexibly identifying the frequency intervals at which
tional (8, 13) Hz band are then multiplied by a weight that
the alpha rhythms actually became de-synchronized and in
decreases as the distance between the frequency interval and
selecting the channels with the largest modulations.
the conventional (8, 13) Hz band increases. Lastly, the interval
(fa ,fb ) is identified by selecting the interval with the maximum
weighted de-synchronization intensity. The rate at which the Remark. Although CRB was designed for use with EEG data,
weights decrease with the distance is governed by a parame- CRB may be applied to any signal that shows suitable power
ter . In the case of Fig. 1(b), setting wsize = 3 Hz, wshift = 0.5 Hz, variation patterns, including independent components (ICs)
and  = 0.7 results in an (fa ,fb ) that is equal to the (8, 11) Hz that are identified by ICA. In the latter case, the ith channel in
range. In the expansion phase, (fa ,fb ) is expanded to encom- Fig. 1(a) corresponds to the ith IC, and the acronym CAF may
pass all of the frequencies involved in the channel’s alpha be read as component (instead of channel) alpha frequency.
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Fig. 1 – Panel (a): block diagram illustrating the three steps of the CRB method. For each channel i, R(f) and T(f) are the resting
and test spectra, respectively. f = (f1 ,f2 ), where f1 and f2 are the boundaries of the alpha modulation interval.  is the
reactivity index relative to f. L is the set of channels selected by CRB, and f̂˛ is the estimated IAF. Panels (b) and (c): “scanning
and expansion” procedure illustrated utilizing representative reference (red) and test (blue) EEG spectra. In panel (b), the
sliding windows are represented by rectangles superimposed to the spectra, and the frequency interval selected by the
scanning procedure is highlighted by the thick rectangle. The thin red rectangle is drawn around the frequency interval that
would have been selected in the case of no regularization mechanism. In panel (c), the initial and expanded intervals are
highlighted in dark and light gray, respectively. (For interpretation of the references to color in this figure legend, the reader
is referred to the web version of this article.)
Adapted from Figs. 2, B.1, and B.3 of [1].
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statistical software to analyze the results from different


3. Description of the CRB analysis plugin groups or experimental events.

3.1. Availability and overview 3.2. Demonstrative run

3.2.1. Sample dataset


The CRB analysis plugin for EEGLAB, along with some tech- The sample dataset is a representative EEG dataset taken from
nical documentation and the representative dataset used [1]. The EEG was continuously recorded from 29 Ag/AgCl elec-
below, is freely available at http://bio.dei.unipd.it/crb/. EEGLAB trodes mounted according to the international 10/20 system
(http://sccn.ucsd.edu/eeglab/) is a popular open source envi- (Fpz used as a ground, reference given by the link of the right
ronment for performing several EEG signal analyses. One of and left mastoid electrodes) during a letter-matching task. For
the main strengths of EEGLAB is the possibility to rapidly details about the dataset, the reader is referred to [1]. Horizon-
integrate new analysis techniques and make them available tal and vertical electrooculograms (EOGs) were also measured
to the community using straightforward plugins. Examples in parallel. The EEG and EOGs were digitalized at a frequency of
of the plugins that have been released include plugins 512 Hz and a conversion resolution of 0.19 ␮V/digit. Offline, the
that perform the following tasks: automatically [15] and signals were digitally filtered between 0.4 and 100 Hz, resam-
semi-automatically [16] detecting common EEG artifacts, sta- pled at 256 Hz, epoched with respect to the stimulus onset (i.e.,
tistically analyzing scalp evoked responses by accounting for the presentation of a five-letter string), and, lastly, pruned for
single trial variability [17], studying source information flows, artifacts using the infomax-based ICA [19] that is implemented
building realistic electrical head models from available data in EEGLAB [20].
and building online brain–computer interface (BCI) models
[18]. 3.2.2. Definition of initial settings
The most straightforward application of the CRB analysis When the CRB analysis toolbox is launched, the window shown
plugin is analysis of the alpha rhythm de-synchronization in Fig. 2 opens. The top panel of the window (A in the fig-
in response to an event (e.g., the movement of a finger or ure) presents some information about the dataset (e.g., the
a cognitive event). For this application, the reference and epochs’ time reference with respect to the event onset and
test states are the time intervals preceding and following the whether channel locations or ICs are available). The data that
event, respectively. Typically, an EEG is continuously recorded will be analyzed, i.e., the input of Fig. 1(a), are selected in the
from several electrodes that are placed on the entire scalp or panel labeled B in the figure. By default, all EEG channels in the
a functionally relevant part of the scalp during an experiment dataset are selected, but the user can focus on a specific scalp
in which the event is repeated several times. Subsequently, area by selecting the desired channels based on their location.
the recordings are imported into EEGLAB. After possible pre- Instead of EEG data, IC activations (i.e., time courses of ICs)
processing and ICs computation, the data are epoched with may be analyzed as well, and a subset of ICs can be selected
respect to the investigated event (i.e., the data are divided into (e.g., specific projection maps), if necessary. Reference and test
slices that surround the repetitions of the event). Once the intervals are defined in the left side of the panel labeled C in
epoched dataset is available, the CRB analysis can be launched the figure. As soon as the intervals are defined, the default val-
by clicking on Analyze alpha frequencies by CRB from the EEGLAB ues for estimating the reference and test PSDs appear on the
Tools menu. The first configuration window is displayed and right side of the same panel. For each channel, the reference
allows interactive definitions of the following: the data to and test PSDs are computed by averaging the single-trial PSDs
be analyzed (i.e., the input of the algorithm); the reference over all epochs. The settings in the right side of panel C deter-
and test time intervals with respect to the event onset; sett- mine how the reference and test PSDs are estimated for each
ings for the computation of the reference and test PSDs; and epoch before averaging. Specifically, for each epoch, the PSDs
the values of the seven CRB parameters. Default values are are estimated using Welch’s method, and the values of win-
provided for all settings, except for reference and test time dows length (ms) and overlap (%) in the panel determine how the
intervals; the user must supply the desired values of these reference and test intervals are split into consecutive overlap-
intervals before running the analysis. Besides IAF, the follow- ping windows (e.g., see [21] for a classic textbook overview of
ing results are produced by the toolbox for all channels for the PSD estimation topic). Here, it is worthwhile to recall that
which an alpha activity is detected: de-synchronization fre- as the windows become shorter, the estimated PSDs become
quency intervals, intensity of de-synchronizations, CAFs, and smoother, and details of the true PSDs are lost. The reader can
reference and test alpha powers. Moreover, the indexes of easily assess how the PSDs estimates vary for several values of
the channels selected by CRB in Step 2 (i.e., the indexes of windows length by previewing the spectra directly from panel
the channels showing the strongest de-synchronizations) are C. A practical rule is that the details finer than the reciprocal of
returned as well. The numerical results are accompanied by the window length (measured in seconds) cannot be resolved
graphical representations of the results. For each channel, the (e.g., 1 Hz for the settings of Fig. 2). As shown in the figure,
corresponding CAF and de-synchronization interval are drawn by default, the software maximizes the resolution by setting
along with the reference and test PSDs. After inspecting the the reference and test windows lengths equal to the duration
numerical or graphical results, the user can easily refine the of the reference and test time intervals, respectively; thus, the
settings before re-launching the analysis. Once the user is sat- single-trial PSDs are estimated using a unique window. This
isfied with his/her settings, the results can finally be saved setting is recommended when approximately tens of epochs
(e.g., .txt or .mat files) and easily imported into specialized are available because the averaging of single-trial PSDs over all
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Fig. 2 – Screenshot of the GUI for the initial settings of the CRB analysis toolbox. The GUI contains the initial settings needed
to run the CRB analysis on the sample dataset. Details about the components of the GUI can be found in Section 3.2.2. For
ease of reading, labels A–E were added to the screenshot.

epochs significantly reduces their high single-trial variance. Once all initial settings have been defined, pressing the run
When fewer epochs are available, it may be worthwhile to CRB analysis and show results button computes the results. The
reduce the windows length and increase the overlap values to results are then displayed, as illustrated in the next section.
reduce the variance of the single-trial PSDs at the expense of
a loss in resolution. Accordingly with Welch’s method, data in 3.2.3. Inspection of the results
each window are multiplied by a tapering function. The role The results of the CRB analysis are displayed both numerically,
of the function is to counteract the masking of the lower level as in Fig. 3, and graphically, as in Fig. 4.
components by the sidelobes of the close higher level compo- In addition to the CAFs, s, and boundaries of the de-
nents due to leakage. The default setting of the toolbox is the synchronization intervals (f1 ,f2 ), the numerical results in Fig. 3
Hanning window, but options for the Hamming window or no include a selection flag that is set to 1 for the channels
tapering [21] are also available. Panel D of Fig. 2 defines the that were selected during Step 2 of the algorithm. The CAFs
seven parameters of the CRB algorithm. Although default val- of the selected channels are those that generate the IAF
ues are assigned to the parameters, the user can easily modify reported at the bottom of the window. Analogously, the aver-
these values (several examples that illustrate their role can age modulation interval reported under the IAF is obtained by
be found in Section 5 of the online technical documentation). averaging the boundaries of the de-synchronization intervals
Note that panel D provides two additional options for comput- of the selected channels. The values of the reference, PR , and
ing CAFs in addition to the one defined by Eq. (2). Specifically, test, PT , alpha powers (␮V2 ) in (f1 ,f2 ) are also included in the
CAFs can be computed by utilizing T(f) or |R(f) − T(f)| instead of table of Fig. 3, along with their relative percentage variation
the R(f) from Eq. (2). In the first case, each CAF reflects the fre- (PT − PR )/PR × 100 [3]. NaN values are returned for the chan-
quencies of the de-synchronized alpha-rhythms with highest nels for which the algorithm was not able to detect any alpha
powers during the test condition. In contrast, in the second de-synchronization. After they are inspected, the results can
case, each CAF reflects the frequencies of the alpha-rhythms either be saved by pressing save results or recomputed after
with the largest decrease in power between the reference and changing the values of the CRB parameters in the panel on
state intervals. the right side of the window.
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Fig. 3 – Screenshot of the GUI for numerical values inspection that results from the CRB analysis of the sample dataset. The
GUI contains a table that reports the following information for each channel: from the left, the selection status, the values of
CAF and , the boundaries (f1 and f2 ) of the modulation interval, reference and test powers in the modulation interval, and
their relative power variation percentage. The value of the IAF is reported in text at the bottom of the GUI. Interactive tools
for refining the initial settings, plotting the spectra of the channels and saving the results are available on the right side of
the GUI.

The de-synchronization intervals, CAFs, selection flags, local average modulation interval are computed using the CAFs
and IAF are also graphically illustrated in the window shown in and the de-synchronization intervals of the selected channels
Fig. 4. For each channel, the reference (red line) and test (blue among those plotted.
line) PSDs are plotted together, and a gray rectangle is drawn
around the de-synchronization interval that was identified by 3.3. Additional interactive tools
the CRB. Moreover, a thin vertical line is drawn along the CAF,
and a check mark in the right upper corner of a plot represents During the inspection of results, the user can easily change
the value of the selection flag for the channel. Lastly, for all the boundaries of (f1 ,f2 ) utilized to compute CAFs, reactiv-
channels, a thick vertical line is drawn at the IAF. The graphical ity indexes and powers. For instance, the user may need
representation of the results allows immediate identification to slightly refine the de-synchronization intervals that were
of the most active scalp regions and frequency intervals of identified by the CRB or may be interested in comparing CRB
the alpha activity. The graphical representation of the results results with those obtained by computing CAFs relative to the
may also reveal the need to refine some of the parameters (e.g., conventional (8, 13) Hz band. New boundaries can be defined
decrease  due to the presence of a strong de-synchronization by typing their values in the table of numerical results or by
in the beta range that the algorithm mistakes for an alpha highlighting the desired intervals with the mouse directly on
de-synchronization). If this is the case, the value of  can be the plots of Fig. 4. Once the new intervals have been defined,
changed in the window that presents the numerical results, results in the table of Fig. 3 can be updated by pressing the
and the analysis may be re-launched with the new parame- recompute with new table values button in the first case and
ter value. The values of local IAF and local average modulation the synchronize with table data button in the second case. Note
interval at the bottom of the window in Fig. 4 are only different that the power modulations in any other band (e.g., the con-
from those reported at the bottom of the window in Fig. 3 if a ventional (4, 7) Hz theta band) can also be assessed from the
subset of all channels is plotted. In this case, the local IAF and windows in Figs. 3 and 4; this use goes beyond the aim of
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Fig. 4 – Screenshot of the GUI for spectra plots inspection that results from the CRB analysis of the sample dataset. Each plot in
the GUI depicts the reference PSD (red line) superimposed to the test PSD (blue line) for the channel in the plot title. In all
plots, a thick vertical black line is drawn at the subject’s IAF, which is reported in text at the bottom of the GUI. For all
streams with a positive  value, the responsiveness regions are shaded in gray, and a thin vertical black line is drawn along
the relative CAF. The red titles correspond to selected channels. The values of local IAF and the average modulation interval
are displayed at the bottom of the GUI. (For interpretation of the references to color in this figure legend, the reader is
referred to the web version of this article.)

analyzing alpha rhythms. The user is also free to include


or discard channels from the computation of the IAF
4. Discussion and conclusions
(e.g., to focus on a specific region). Channels can be
This study describes an open source MATLAB software based
included/discarded by performing one of the following: set-
on the CRB algorithm proposed by Goljahani et al. [1]; this
ting the selection flag to 1 relative to the desired channels
software can be used as an EEGLAB plugin. This plugin esti-
in the table of numerical results and pressing the recom-
mates the CAFs and IAF by identifying the frequency intervals
pute with new table values button; checking/unchecking the
at which the alpha rhythms actually de-synchronize for the
plots in Fig. 4 and pressing the synchronize with table data
subject and the investigated task. The analysis can be per-
button.
formed on either EEG scalp data or ICs. Although command
line options are available, the toolbox provides user-friendly
Remark. The CRB analysis can also be run from the MATLAB interactive windows to easily define the initial settings and to
command line without any graphical support (e.g., to perform display and save the results. The results are displayed both
batch analyses or to integrate functions in custom scripts; numerically and graphically to facilitate tuning of the CRB
details can be found in the online technical documentation). parameters and generation of insights about the phenomenon
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under investigation. Choosing the same setting values allows [6] C.M. Smit, M.J. Wright, N.K. Hansell, G.M. Geffen, N.G.
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additional interactive tools allow the user to easily investigate and alpha power in a large adolescent twin sample,
International Journal of Psychophysiology 61 (2006) 235–243.
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diverse investigations. For instance, in addition to studying between somatosensory painful stimuli and motor
IAFs relative to the entire scalp or a scalp sub-region (e.g., [22]), sequences affects both anticipatory alpha rhythms and
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398–405.
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[8] B.S. Chang, D.L. Schomer, E. Niedermeyer, Normal EEG and
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[10] R.H. Grabner, C. Brunner, R. Leeb, C. Neuper, G. Pfurtscheller,
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Neuper, G. Pfurtscheller, G.L. Romani, C. Babiloni, Is there
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The authors thank the anonymous reviewers for the com- [13] A. Brignol, T. Al-ani, X. Drouot, Phase space and power
spectral approaches for EEG-based automatic sleep–wake
ments and criticisms that helped to greatly improve the
classification in humans: a comparative study using short
quality of the final manuscript. The study was partially
and standard epoch lengths, Computer Methods and
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