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A comprehensive review of EEG-based brain-computer interface paradigms

Article in Journal of Neural Engineering · November 2018

DOI: 10.1088/1741-2552/aaf12e

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A Comprehensive Review of EEG-based Brain-Computer Interface
Paradigms
Reza Abiri1, 2, a, Soheil Borhani2, b, Eric W Sellers3, c, Yang Jiang4, d, Xiaopeng Zhao2, e, *
1
Department of Neurology, University of California, San Francisco/Berkeley, CA 94158, USA
2
Department of Mechanical, Aerospace, and Biomedical Engineering, University of Tennessee,
Knoxville, TN 37996, USA
3
Department of Psychology, East Tennessee State University, Johnson City, TN 37614, USA
4
Department of Behavioral Science, College of Medicine, University of Kentucky, Lexington,
KY 40356, USA

Emails: [email protected]; [email protected], [email protected],

c
[email protected], [email protected], [email protected]

*Corresponding author: 313 Perkins Hall, University of Tennessee, Knoxville, TN 37996 USA,
E-mail: [email protected]

Abstract
Advances in brain science and computer technology in the past decade have led to exciting
developments in Brain-Computer Interface (BCI), thereby making BCI a top research area in
applied science. The renaissance of BCI opens new methods of neurorehabilitation for physically
disabled people (e.g., paralyzed patients and amputees) and patients with brain injuries (e.g.,
stroke patients). Recent technological advances such as wireless recording, machine learning
analysis, and real-time temporal resolution have increased interest in electroencephalographic
(EEG) based BCI approaches. Many BCI studies have focused on decoding EEG signals
associated with whole-body kinematics/kinetics, motor imagery, and various senses. Thus, there
is a need to understand the various experimental paradigms used in EEG-based BCI systems.
Moreover, given that there are many available options, it is essential to choose the most
appropriate BCI application to properly manipulate a neuroprosthetic or neurorehabilitation
device. The current review evaluates EEG-based BCI paradigms regarding their advantages and
disadvantages from a variety of perspectives. For each paradigm, various EEG decoding
algorithms and classification methods are evaluated. The applications of these paradigms with
targeted patients are summarized. Finally, potential problems with EEG-based BCI systems are
discussed, and possible solutions are proposed.

1
1 Introduction
The concept of using brain signals to control prosthetic arms was developed in 1971 [1]. Since
that time, researchers have been attempting to interpret brain waveforms to establish a more
accurate and convenient control over external devices. Later, this research area was termed
brain-computer interface (BCI), and its applications spread rapidly [2].
BCI systems utilize recorded brain activity to communicate between the brain and computers to
control the environment in a manner that is compatible with the intentions of humans [3]. There
are two primary directions in which BCI systems have been applied. The first is studying brain
activity to investigate a feedforward pathway used to control the external devices without the aim
of rehabilitation [4]. The other dominant direction is closed-loop BCI systems during
neurorehabilitation with the feedback loop playing a vital role in recovering the neural plasticity
training or regulating brain activities [4].
Brain activity can be recorded through various neuroimaging methods [3, 5]. The methods can be
categorized into two groups: invasive and noninvasive. Electrocorticography (ECoG) and
electroencephalography (EEG) have become the most common invasive and noninvasive
technologies, respectively [3]. ECoG, also known as intracranial EEG, is recorded from the
cortical surface. Other invasive technologies record signals from within the brain using single-
neuron action potentials (single units), multi-unit activity (MUA), local field potentials (LFPs)
[6, 7]. The high quality spatial and temporal characteristics of these signals lead to successful
decoding of biomechanic parameters [8-12]. These decoding achievements for upper limb
kinematics using invasive electrodes in monkeys and humans have resulted in accurate control of
prosthetic devices in 3D space [13-17]. However, the invasive electrodes have significant
drawbacks due to the risk of performing surgery and the gradual degradation of the recorded
signals. Therefore, noninvasive approaches such as functional magnetic resonance imaging
(fMRI), magnetoencephalography (MEG), near-infrared spectroscopy (NIRS), and EEG have
become more widespread in human participants.
Although some noninvasive technologies provide a higher spatial resolution (e.g., fMRI), the
EEG has proved to be the most popular method due to direct measures of neural activity,
inexpensiveness, and portability for clinical use [3]. EEG measures electrical brain activity
caused by the flow of electric currents during synaptic excitations of neuronal dendrites,
especially in the cortex, but also in the deep brain structures. The electric signals are recorded by
placing electrodes on the scalp [3]. EEG signals have been used to control devices such as
wheelchairs [18] and communication aid systems [19]. During the past decade, EEG methods
have also become a promising approach in controlling assistive and rehabilitation devices [20].
EEG signals could provide a pathway from the brain to various external devices resulting in
brain-controlled assistive devices for disabled people and brain-controlled rehabilitation devices
for patients with strokes and other neurological deficits [21-25]. One of the most challenging
topics in BCI is finding and analyzing the relationships between recorded brain activity and
underlying models of the human body, biomechanics, and cognitive processing. As a result,

2
investigation of relationships between EEG signals and upper limb movement, real and
imaginary, has become a fascinating area of research in recent years [26, 27].
To implement an EEG-based BCI system for a particular application, a specific protocol and
paradigm has to be chosen for all phases of the experiment. First, the subject performs a
particular task (e.g., imagery task, visual task) in order to learn how to modulate their brain
activity while EEG signals are recorded from the scalp. Using the recorded EEG as training
data, a neural decoder for the paradigm is generated. Afterward, the subject performs the task
again and the neural decoder is used for BCI control.
Many EEG-based BCI review papers have been published [18, 23, 24, 28-32]; however, there is
a lack of review or guidance in comparing EEG-based BCI paradigms. Here we aim to review
the most commonly employed EEG-based BCI paradigms. A guideline on deployed algorithms
and classification methods in generating control signals from these paradigms are summarized.
Each of these paradigms has their advantages and disadvantages depending on a patient’s
physical condition and user-friendliness. The current and future potential applications of these
paradigms in the manipulation of an external object, rehabilitation, restoration, enhancement, and
entertainment are investigated. Finally, present issues and limitations in EEG-based BCI systems
are examined, and future possibilities for developing new paradigms are discussed.
2 Motor Imagery Paradigms
Motor imagery is described as imagining a movement rather than executing a real movement (for
more detail on motor imagery see [27]). Previous studies have confirmed that imagination
activates areas of the brain that are responsible for generating actual movement [33]. The most
common motor imagery paradigms reported in literature are sensorimotor rhythms (SMR) and
imagined body kinematics (IBK). In the following sections, the paradigms are described in
detail.
2.1 Sensorimotor Rhythms (SMR) Paradigms
2.1.1 Overview
The sensorimotor rhythms paradigm is one of the most popular motor imagery paradigms (e.g.,
[34], [35]). In this paradigm, the imagined movement is defined as the imagination of kinesthetic
movements of large body parts such as hands, feet, and tongue, which could result in
modulations of brain activity [36].
Imagined movement in sensorimotor rhythm paradigms causes event-related desynchronization
(ERD) in mu (8-12 Hz) and beta rhythms (18-26 Hz). In contrast, relaxation results in event-
related synchronization (ERS), (for an in-depth review see [37]). The ERD and ERS modulations
are most prominent in EEG signals acquired from electrode locations C3 and C4 (10/20
international system); these electrode locations are above the sensorimotor cortex. These
modulated EEG signals in the aforementioned frequency domains (mu/beta) can be employed to
control prosthetic devices. Wolpaw et al. [38] controlled a one-dimensional cursor using mu

3
rhythms. Figure 1 shows examples of change in frequency spectra of SMR during imagination of
hands.
The main drawback of the SMR paradigm is that the training time for 2D and 3D cursor control
can take weeks or months. The training for this system requires subjects to learn how to
modulate specific frequency bands of neural activity to move a cursor in different directions to
select desired targets.

Figure 1. An example of a change in frequency spectra for EEG recorded from C3 and C4. The top row
(a, b) shows spectral power changes in C3 and C4 electrodes while performing imagined movement of
right hand versus left hand. The middle row (c, d) shows spectral power change in C3 and C4 electrodes
while performing imagined movement of both hands versus rest. The bottom row (e, f) shows spectral
power change in C3 and C4 electrodes for imagined movement of right hand versus rest and left hand
versus rest, respectively (Figure copied from [39] with permission of a Creative Commons Attribution
(CC BY) license).

2.1.2 Analysis & Classification Methods

SMR paradigms have been employed by many researcher groups. For example, Wolpaw and
McFarland introduced the first two-dimensional cursor control strategy [40]. The subjects’ task
was a center-out cursor task, where the cursor was guided to one of eight targets located around
the perimeter of a computer monitor. In this work, each dimension of cursor movement was

4
controlled by a linear equation in which the independent variable was a weighted combination of
the amplitudes in a mu or beta rhythm frequency band recorded from the right and left
sensorimotor cortices. These changes were generated as the result of right and left-hand
imaginary movements.
Bhattacharyya et al. [41] compared the performance of different classification methods for left/
right hand imagery in EEG features. They found that the accuracy of kernelized SVM
outperforms the other classifiers. Murguialday et al. [42] designed a hierarchical linear
classification scheme using the peak mu power band to differentiate between relaxation, left-
hand movement, and right-hand movement. For movement prediction of the right hand, left
hand, tongue, and right foot, Morash et al. [36] showed that time-frequency features could better
depict the non-stationary nature of EEG SMR. Using a parametric modeling approach, they
divided time into bins of 256ms and frequency into bins of 3.9 Hz and applied Naïve Bayesian
classification. However, parametric classification methods require a priori knowledge of
subjects’ EEG pattern that is not always applicable for BCI control. Nonetheless, Chen at al. [43]
used a three-layer neural network non-parametric approach, and they investigated an adaptive
classifier for controlling an orthotic hand by motor imagery. A summary of previous SMR work
is shown in Table 1.

Table 1. Previous SMR paradigms. DWT: Discrete wavelet transform, LMS: Least mean square, STFT:
short-time Fourier transform, CSP: Common spatial pattern, N/A: Not Applicable
Reference Task Feature Classification method
[38] Cursor control in 1D Mu rhythm (8-12Hz) N/A
amplitude from
[44] Cursor control in 2D FFT + Mu rhythm amplitude Linear regression
(7.5-16Hz)
[45] Grasping and object DWT over 12-14Hz and 18- LDA
manipulation 22Hz
[40] Cursor control in 2D Mu (8-12Hz) and Beta (18- Linear regression + LMS to
26Hz) rhythm amplitude optimize weights
[42] Control of a prosthetic hand Peak Mu (8-12Hz) band A logistic regression
power (relaxation and motor
imagery) + a logistic
regression (right hand and
left hand)
[43] Control of a hand orthosis STFT over Mu band (8- 3-layer feedforward NN
14Hz) classified three classes (right
hand, left hand, no
imagination)
[46] Control of a rehabilitation Using CSP algorithm to N/A
robot select features

5
 [47] Control of a robotic am Time-frequency power of N/A
EEG over the recorded
locations on [10.5,13.5] Hz
frequency range
[48] Control of a rehabilitation Time-Frequency power in LDA
robot EEG alpha [8,13] Hz, sigma
[14,18] Hz and beta [18-30]
Hz bands over C3, C4, and
Cz

2.1.3 Applications and Targeted Patients’ Populations

The SMR paradigm has been one of the most promising paradigms used by patients with
tetraplegia, spinal cord injury, and Amyotrophic Lateral Sclerosis (ALS). The paradigm was first
employed in a one-dimensional computer cursor control task by Wolpaw et al. [38]. A drawback
of the method is a relatively lengthy training period of up to several weeks. Wolpaw and
McFarland [44] used mu rhythms from four channels across left and right central sulci to move a
cursor in 2D space to targets located in the four corners of a computer monitor. Subsequently,
they used the same paradigm with people who had spinal cord injuries to guide the cursor to
eight different targets on the sides of a monitor by imagining right and left-hand movement [40].
Finally, they expanded their work and controlled a cursor to hit targets located in 3-dimensional
space [49]. In all of these studies the subjects learned to modulate their SMR based on imagery
of large body parts such as hands and legs.
Applications other than cursor control have also been employed using SMR. Guger et al. [50]
used SMR to open and close a prosthetic hand with imagined right or left-hand movement.
Pfurtscheller et al. [51] employed foot imagery to restore hand grasp in a patient with tetraplegia.
Muller-Putz et al. [45] developed an EEG-based SMR system using imagined foot and hand
movements to help a paralyzed patient do simple tasks such as grasping a cylinder and moving
an object by controlling a functional electrical stimulation (FES) device. Sun et al. [52] and Roy
et al. [53] used motor imagery to control an artificial upper limb. Murguialday et al. [42] also
used an SMR design to open and close a prosthetic hand. In recent years, SMR control signals
have been applied to control objects such as quadcopters [39], virtual helicopters [54], and
robotic manipulators [20, 47, 55]. SMR is also employed in rehabilitation robots [46, 48] and
hand orthosis [43]. The paradigm has also been tested with healthy and stroke patients [56-61].
2.2 Imagined Body Kinematics Paradigms
2.2.1 Overview
Efforts to extract motor imagery commands from EEG signals has been progressing for years
[49]. However, the time-consuming process of training and model calibration limits the efficacy
of BCI utilization for many potential users. Furthermore, the first critique in controlling
prosthetics for amputees via SMR is the lack of natural and intuitive control [62]. In other words,
6
SMR lacks the ability of direct extraction of kinematic parameters. Although the technique can
distinguish motor activities corresponding to large body parts, the decoded motor information
does not contain magnitude or direction of kinematics parameters (e.g., position, velocity, or
acceleration).
Imagined body kinematics (IBK) is a motor imagery paradigm that originated from invasive BCI
technology [9, 10]. However, noninvasive work has noted that the information for this paradigm
is extracted from low-frequency SMR signals (less than 2Hz) [34]. IBK is classified as an
independent paradigm from SMR because the training protocols and analysis methods are
fundamentally different from SMR paradigms. In IBK, the subject is asked to imagine the
continuous movement of only one body part in multi-dimensional space. The recorded signals
are then decoded in the time domain. This paradigm is sometimes referred to as a natural
imaginary movement. In noninvasive devices, Bradberry et al. [63] investigated 2D cursor
control with a natural imaginary movement paradigm and analyzed the data in time-domain
frequencies of less than 1 Hz. Their subjects were instructed to use the natural imaginary
movement of the right-hand index finger, thereby reducing training time to a level similar to
invasive devices [10, 16].
In addition to Bradberry et al.’s work in noninvasive EEG technology, Ofner et al. [64] studied
the continuous and natural imaginary movements of the right hand in a 2D plane. They estimated
the imagined continuous velocities from EEG signals. Kim et al. [65] decoded the three-
dimensional trajectory of imagined right-hand movement in space and also examined the effects
of eye movements on linear and nonlinear decoding models. Andres et al. [66] conducted a
similar study in 2D space using linear models. Gu et al. [67] decoded two types of imaginary
movements of the right wrist at two different speeds and later [68] considered the imagined
speed of wrist movements in paralyzed ALS patients. Others have studied the imaginary
movement of the shoulder, elbow, wrist, and finger [69-71]. Although most of this recent work
could be classified as decoding of IBK, their application for BCI is limited and is still under
investigation.

2.2.2 Analysis & Classification Methods

A number of seminal works have suggested that the low-frequency components of EEG signals
(< 2Hz) located over motor cortex carry kinematic information [63-65, 67-69, 72, 73]. Although
many studies have shown kinematic data is present in low frequencies, Gu et al. [67] were the
first to use this information for classification. They decoded wrist rotation and extension at fast
and slow speeds. They found that discrete imagined movement is encoded in the movement-
related cortical potential (MRCP). In their study, EEG signals were low-pass filtered at 2 Hz and
the negative slope 2s before the movement onset known as Bereitschaftspotential (BP) was
examined. The BP has two parts, the NS1 (Negative Slope of early BP) and the NS2 (steeper
Negative Slope of late BP). The NS1, NS2, and the mu (8-12 Hz) and beta rhythms (18-26 Hz)
constituted the feature space in their study. In another study, Yuan et al. [74] decoded seven

7
different hand clenching speeds using spatial-temporal characteristics of alpha (8-12 Hz) and
beta (18-26 Hz) bands. To translate multiple discrete speeds of hand imagery they developed
multiple linear regression models and smoothed the output with a low-pass 1 Hz filter. Although
they found a correlation between higher frequency bands and the speed of imagery, they did not
successfully find movement trajectory information. Bradberry et al. [63] conducted a prominent
study on IBK; they were able to extract two-dimensional hand imagery [63] and actual three-
dimensional hand movement trajectory [72] using low-frequency EEG signals (<1 Hz). A linear
decoding model with first-order temporal differences of EEG data was developed, and they
successfully modeled continuous cursor velocity, which was correlated with the defined
trajectory. They also showed that EEG data from 100ms before movement imagination onset is
correlated with the movement. The linear model was as follows:
𝑁 𝐿

𝑥[𝑡] − 𝑥[𝑡 − 1] = 𝑎𝑥 + ∑ ∑ 𝑏𝑛𝑘𝑥 𝑆𝑛 [𝑡 − 𝑘]

𝑛=1 𝑘=0

The same equation was used for horizontal and vertical velocities. In this equation 𝑥[𝑡] −
𝑥[𝑡 − 1] is cursor velocity along one axis, 𝑁 is the number of EEG channels, 𝐿 is the number of
time lags, 𝑆𝑛 [𝑡 − 𝑘] is the temporal lagged version of EEG at EEG channel n at time lag 𝑘, and 𝑎
and 𝑏 are the weights that result from the linear regression.
Using partial least squares (PLS) regression, Ofner and Müller-Putz [73] were able to reduce
EEG artifacts And also eliminate highly correlated variables. They were also able to identify
relationships between latent predictors and desired response variables. By using different
electrode locations and different time lags as latent variables, the algorithm captured the user’s
source space contribution to the latent variables. Finally, Kim et al. [65] explored a nonlinear
decoding model called kernel ridge regression (KRR). They showed that KRR algorithm
significantly reduced eye movement contamination, which is common in linear models. Andres
et al. [66] and Kim et al. [65] examined the role of eye movement in the linear decoding of IBK.
By comparing the decoding performance with and without EOG contaminated brain signals, they
found that eye movement plays a significant role in IBK tasks. Additionally, in contrast to a
report published by Korik et al. [75], Kim et al. [65] confirmed that the SMR bands do not
contain kinematic parameter information.

2.2.3 Applications and Targeted Patient Population

The IBK paradigm is new to noninvasive devices. Thus far, it has been applied to a limited
number of applications. The reason for this is likely due to the poor decoding of EEG signals
[76]. Abiri et al. employed natural imagery movements of one hand to control different gestures
of a social robot [77, 78] and to manipulate a robotic arm [79]. Gu et al. [68] employed the
imagined speed of wrist movements in paralyzed ALS patients. It was shown that employing
natural IBK paradigms can dramatically reduce the training times. A generic model which can be

8
operated with zero-training is also a promising future development. Abiri et al. [80, 81] used the
IBK in a zero-training BCI paradigm to control a quadcopter in 2D space.

3 External Stimulation Paradigms

Brain activity can be affected by external stimulations such as flicking LEDs and sounds. The
altered EEG activity can be collected and decoded to control real or virtual objects or external
prosthetics. This is the basic principle for external stimulation paradigms. External stimulation
can be visual [82, 83], auditory [83, 84], or somatosensory [85]. The following sections discuss
the most common external stimulation paradigms employed by BCI researchers.

3.1 Visual P300 Paradigms

3.1.1 Overview
One of the most popular paradigms in EEG-based BCI systems is visual P300 (for review see
[86, 87]). Farwell and Donchin pioneered the use of the visual P300-BCI in 1988 [88] by
creating what is now referred to as the P300 Speller. The P300 is one of the most studied event-
related potentials (ERP). An ERP is derived by averaging EEG signals of a specific event type.
The P300 component is elicited in response to infrequently presented events using what is known
as an “oddball paradigm.” The P300 is a positive peak in the ERP ranging from 5 to 10
microvolts in size and a latency between 220 to 500ms posterior to the event onset (see Figure
2). This ERP is defined as an averaged increase in the amplitude of time series of brain signals
which is most significant at midline locations (Pz, Cz, and Fz in the 10/20 international system).
When inter-stimulus intervals are less than 250-300ms [89], the definition of P300 becomes
debatable because the P300 response and the presentation of subsequent stimuli overlap in time.
For example, with very short inter-stimulus intervals, like 125ms, 3 to 5 stimuli are delivered in
the range 0-500ms from the onset of first stimulus. Likely, the P300 elicited in this paradigm is
the sum of the P300 and other components that are elicited by other stimuli that are presented
prior to and after any given stimulus presentation.
The most important advantages of the visual P300 BCI are that most subjects can use it with very
high accuracy and it can be calibrated in minutes. Therefore, the user can easily and quickly use
the system to control devices. Disadvantages of this paradigm include fatigue from the high level
of attention and visual focus required to use the system [90], and the inability for people with
visual impairments to use the system [91].

9
 Figure 2. ERP components after the onset of a visual stimulus (figure copied from [92] with
permission) .

3.1.2 Analysis & Classification Methods

A summary of previous studies using P300 is shown in Table 2. The P300 was initially reported
by Sutton et al. [93] in 1967. The P300 speller was initially introduced by Farwell and Donchin
[88] within a row/column paradigm (RCP) comprised of a 6×6 matrix of letters and numbers.
Since collecting subject’s overt behavioral response is not necessary for this paradigm, it can be
used as a motor-free means of communication for severely disabled patients. Additionally, P300
shares very similar inter-subject characteristics which help to diminish the subjects’ training time
[94]. However, the subject is required to maintain attention throughout the experiment. The P300
amplitude is subjective to a number of elements such as the probability of target appearance, the
inter-trial duration, difficulty of the experiment, attentional state of the participant and the
habitual effects [92]. Faster P300 responses are indicative of better cognitive performance in
attentional and immediate memory task [92]. Latency jitter can make it difficult to extract the
P300 deflection; thus, presenting multiple trials and averaging the EEG response is required to
increase the signal-to-noise ratio and, thereby, improve decoding accuracy. However, when more
trials are presented the rate of communication is slower, which leads to a speed/accuracy trade-
off.
In [88] and [94], the authors addressed the relationship between the number of trials and
decoding accuracy using stepwise discriminant analysis (SWDA) and reported that more trials
significantly improved performance. Piccione et al. [95] extract P300 by using the fuzzy method
to combine decomposed components of ICA over EEG. Krusienski et al. [96] compared various
classification techniques including Pearson’s correlation method (PCM); Fisher Linear
Discriminant (FLD); Stepwise Linear Discriminant Analysis (SWLDA); and, Linear and
Nonlinear Support Vector Machines (SVMs). They illustrated that FLD and SWLDA performed

10
significantly better than other classification methods. Moreover, their analysis indicated that the
P300 was stable across sessions and subjects.
Citi et al. [97] introduced a 2D cursor control P300-based BCI. They were able to extract an
analog control signal with a single-trial approach using a genetic algorithm. Also, there are other
single-trial classification approaches using P300 signals [98-101]. Most of the early P300 Speller
research had focused on EEG locations along the midline (e.g., Fz, Cz, and Pz). In [102]
information from posterior locations such as PO7, PO8, and Oz were added to an SWLDA
classifier. They showed that adding additional electrode locations significantly improved the
discriminability of data samples. Bell et al. [103] increased the information transfer rate (ITR) to
24 bits/min for a four-choice classification problem relying on the fact that P300 has a robust
response to multiple trials. They elicited P300-based control analyzing only five trials of P300
responses with 95% accuracy using SVMs. Edlinger et al. [104] and Chen et al. [105] applied the
paradigm in a virtual environment (VE) as an actuator for a smart building scenario and to
control a virtual hand, respectively. By dividing the screen into seven different regions Fazel-
Rezai and Abhari [106] were able to reduce distraction caused by adjacent items and, at the same
time, were able to lower the stimulus probability. These changes resulted in larger P300
amplitudes, which resulted in higher detection accuracy and higher ITR [92].
An innovative checkerboard paradigm (CBP) was introduced in [107]. The CBP showed
significantly higher mean accuracy than the row-column paradigm (RCP) (i.e., 92% compared to
77%) and mean ITR was increased to 23 bits/min from 17 bits/min. The CBP is able to avoid
stimulus adjacency-distraction error addressed in [106] and also increases P300 detection
accuracy by lowering the probability of target-occurrence. In [108], a language model to enhance
typing speed was utilized. They examined P300 BCI paradigms including single-character
presentation (SCP), RCP, and they also tested a rapid serial visual presentation (RSVP)
paradigm. They applied PCA over a band-pass [1.5-42] Hz filtered EEG to extract a one-
dimensional feature vector from multiple locations over frontal, central, and parietal regions.

Table 2. A summary of studies with P300 paradigm

Reference Task Feature Classification method
[88] 6×6 row/column (RC) speller Data from Pz, channel were SWLDA
extracted, and band-pass
filtered [0.02, 35] Hz and
downsampled to 50Hz
[95] Control a virtual ball in 2D Data from Cz, Pz, Oz, and Fz A three-layer ANN
channels were extracted, and
ICA was applied to extract
features
[96, 102] 6×6 row/column (RC) speller Moving average and SWLDA
decimation with factor of 12
[97] Computer cursor control in Low-pass filter with cut-off Continuous wavelet
2D frequency of 34 Hz and transform (CWT) and
decimation to 128 Hz Genetic Algorithm (GA)

11
 [103] Control of a humanoid robot Band-pass filter [0.5, 30] Hz SVM
and downsampling to 100 Hz
[104] Single Character (SC) speller Band-pass filter [0.5, 30] Hz LDA
and downsampling to 60 Hz
[106] Region-based (RB) speller C1, C2, Cz, Pz, and Fz Averaged Mexican-hat
channels were used wavelet coefficients used as
feature set
[107] 8×9 Checkerboard (CB) Cz, Pz, PO7, and PO8 channels SWLDA
speller were used
[2, 109] Single Character (SC) speller Scaling data samples into [-1, Bayesian Linear
1] and downsampling to Discriminant Analysis
32Hz (BLDA) and Fisher’s Linear
Discriminant Analysis
(FLDA)
[110] Target selection in 3 D space Channel selection and SWLDA
downsampling to16 Hz

3.1.3 Applications of Visual P300 and Targeted Patient Population

The most common application of visual P300 has been in developing prosthetic keyboards to
provide a pathway of communication for disabled patients. Usually, speller devices in BCI
consist of a matrix of letters, numbers, and symbols [94]. The rows and columns of this matrix
are flashed in sequence, and the subject has to focus attention on the intended character. The
intended character is then determined by the speller based on its row and column. These devices
use a statistical model based on the P300 ERP to identify the correct symbol during flashing. The
main advantage of P300 spellers has been their usefulness to people with ALS [92, 111, 112] and
brainstem stroke [113]. P300 has also been investigated as a way for a subject to control some
specific tasks in the environment [114]. It has also been used to control a humanoid robot [103],
and to navigate a wheelchair [110, 115]. This paradigm was also employed to control a computer
cursor in 2D space [97] by paralyzed patients [95]. Additionally, it has been used to control a
virtual hand [105] in a virtual reality smart apartment [104].

3.2 Steady State Visual Evoked Potential Paradigms

3.2.1 Overview
The Steady State Visual Evoked Potential (SSVEP) is another popular visual component used in
BCI ([116, 117]). SSVEP is also called photic driving since the generators of this response are
located in visual cortex. Rather than either motor execution or imagined motor action, subjects
have to shift gaze and as well as their attention to flickering stimuli, which requires highly
accurate eye control.
In the SSVEP paradigm, a constant frequency flickering stimulus on the central retina results in
an EEG pattern consistent with the flickering rate. The frequencies of stimulation can be varied
from low (1~3.5 Hz) to high frequency (75~100 Hz) [118]. The stimulus can be produced using

12
a light-emitting diode (LED) or a cathode ray tube (CRT). Multiple flickering targets with
distinct flickering frequencies are typically presented to the user. There is a strong correlation
between flicker frequency and the observed frequency of the EEG. The user’s intended target is
determined by matching the pattern of EEG activity to the command associated with the
particular frequency.
There are advantages associated with the SSVEP paradigm. Because the stimuli are exogenous,
it is a no-training paradigm that can be used by many subjects. The stimuli flash at many
different frequencies, thereby resulting in many commands and more degrees of freedom to
control prosthetic devices. In addition, the SSVEP frequencies can be more reliably classified
than event-related potentials. However, the use of flickering stimuli could lead to fatigue for the
subject, mainly when using low flickering frequency [119-122]. This paradigm is also not well
suited for people with visual impairments due to the required gaze shifts during use. However,
Min et al. [123] have recently proposed a new SSVEP paradigm that uses a grid-shaped line
array. They suggested that this novel presentation is gaze-independent. There are also steady-
state somatosensory evoked potentials (SSSEP) [124] and hybrid SSSEP and P300 applications
[125].

3.2.2 SSVEP Analysis & Classification Methods

As opposed to transient VEP which is used to measure the travel time of a visual stimulus from
the eye to the occipital cortex [117], SSVEP depicts a stable characteristic of the spectral content
of EEG signals. Among various EEG paradigms, SSVEP is less vulnerable to artifacts and has
higher ITR. BCIs based on P300 or SMR paradigms reach ITR of 4-60 bits/min, SSVEP-based
BCIs yield ITR of 100 bits/min and higher. Since information in SSVEP paradigms is located in
narrow-band frequency ranges, a narrow-band band-pass filter is typically part of the signal
preprocessing of SSVEP. However, the amplitude and phase characteristics of SSVEP depend on
the intensity and frequency of the stimulus.
Herrmann [118] investigated the correlation between frequency of stimulus presentation and the
firing rates of neurons. The results exhibited resonance phenomena at 40Hz, subharmonics at
10Hz and 20Hz, and weaker intensity integer multiples of the stimulus (e.g., 80Hz). Muller-Putz
and Pfurtscheller [126] applied SSVEP in a hand prosthesis using four-class classification with
LED flicker at 6, 7, 8 and 13Hz. Harmonic sums at each of the stimulation frequency yielded the
feature set for classification of SSVEP. They achieved online accuracy between 44% and 88%. A
drawback of the SSVEP paradigm is that low-frequency stimulation can lead to fatigue or
epileptic seizure. Therefore, a high-frequency flicker (60-100 Hz) is preferred [127]. Bryan et al.
[128] used an estimated signal’s power spectrum generated by the Fast Fourier Transform (FFT)
as an input to control a humanoid robot with a single electrode (Oz). Li and Zhang [129] applied
an LDA classifier and an optimization algorithm to improve SSVEP online accuracy. A
minimum energy combination (MEC) was utilized in [130] to detect principle and harmonic
frequencies in spatially filtered signals. They also conducted an extensive study including 61

13
subjects in order to investigate the scope of applicability of SSVEP-based BCIs. In addition to
performance, they examined a number of covariates including age, gender, and level of tiredness.
Chen et al. [131] examined the correlation coefficients between stimulus frequency and subject’s
EEG frequency using canonical correlation analysis (CCA). Considering accuracy and ITR
simultaneously, they determined a user-specific optimal stimulation duration and phase interval.
In a text input application, Chen et al. [132] attempted to enhance ITR by employing entropy
coding algorithms such as Huffman coding. An advantage of the SSVEP paradigm is that it is
less susceptible to motion artifacts. Thus, it is a suitable choice for a mobile subject. Pfurtscheller
at al. [133], showed that a gait-assistance exoskeleton could be accurately controlled. They
evaluated online and offline performance of CCA and k nearest neighbors (kNN) classifiers.
Most studies conducted with the SSVEP paradigm are based on decoding bottom-up visual
information. Thus, these systems are gaze-shift dependent. Min et al. [123] examined a top-down
visual condition within the paradigm. The results in the top-down condition showed a different
pattern over the occipital lobe than the pattern produced by the bottom-up condition. Moreover, a
randomly-shuffled LDA (rLDA) classifier performed more accurately in the top-down condition
than the more commonly used CCA classifier. An overview of previous SSVEP studies with
accuracy and ITR is shown in Table 3.
Bio-inspired intelligent information processing techniques can also help to understand the human
perceptual systems and to incorporate the biological models and features of human perceptual
systems into the bioinspired information processing techniques to process the physiological
signals for BCI. For instance, entropy can be used to measure the dynamic complexity of EEG
signals. Cao et al. [134] proposed using inherent fuzzy entropy for the improvement of EEG
complexity evaluation, which can apply to SSVEP.

Table 3. An overview of SSVEP paradigms.

Reference Task Feature Classification method
[132] Spelling using a multi-level (6-10) Hz over Oz, A1 and Bayesian model enhanced by
selection criterion grounded by A2 language entropy model
[133] Lower limb exoskeleton (9-17) Hz with eight CCA and kNN
electrodes over occipital and
parietal lobes referenced by
FCz and grounded by Fpz
[135] Checkerboard as visual (6-10) Hz over Oz, O1, and Maximum Likelihood
stimuli O2
[123] Spelling using a grid-shaped (5-10) over 3 electrodes of CCA and rLDA
flicking structure occipital lobe
[136] Navigation in 2-dimensional 15, 30, 45Hz and their 900 CCA
computer game phase shift over occipital and
parietal lobes
[131] Spelling characters (7-70) Hz with 9 electrodes CCA
over parietal and occipital
lobe

14
 [126] Control of an electrical (6-13) Hz with four Maximum Likelihood
prosthesis electrodes over occipital lobe
[129] A brain-to-brain motion (6-13) Hz with four LDA
control system electrodes over occipital lobe
[130] Spelling (7-10) Hz with eight MEC
electrodes over occipital lobe

3.2.3 SSVEP Applications and Targeted Patients Population

Due to a large number of discrete control commands and high reliability of SSVEP, the paradigm
has been studied by many BCI researchers. Recently, a high-speed SSVEP speller was used to
enable the subject to choose among 40 characters including letters of English alphabet, numbers,
and some symbols [131]. In addition, an user-dependent SSVEP based on determining the
prominent key-parameter for each user was developed by [130] to spell only one phrase.
According to the appearance frequency of letters, a multilevel SSVEP-based BCI was designed
in [132] to type text. Bryan et al. [128] used SSVEP signals to control a humanoid robot. Other
applications include an electrical prosthesis [126], an orthosis [137], and a lower limb
exoskeleton [133]. Recently [135] demonstrated the feasibility of an SSVEP paradigm in locked-
in syndrome. SSVEPs have even been used to allow a cockroach to navigate the desired path
[129] and to navigate in a 2-dimensional BCI game [136].

4 Error-Related Potential
4.1 Overview
The error-related potential (ErrP) recently been used as an ERP component that can be used to
correct BCI errors [138]. The ErrP occurs when there is a mismatch between a subject’s intention
to perform a given task and the response provided by the BCI. For example, assume a user
wishes to move a cursor from the middle of a monitor to the left side of the monitor. If the cursor
erroneously moves to the right, an error-related potential will be generated. The ErrP is mostly
pronounced at frontal and central lobes and has a latency of 200-700ms. Figure 3 shows a
schematic of how an ErrP is generated and how it can be used to teach an intelligent agent to
control a BCI. The paradigm no longer relies on an average number of trials like in P300, but it
uses a short window in a single trial basis. Ferrez and Millan [139] decoded errors followed the
occurrence of miss recognition of user intent by the BCI system. Subsequently, Chavarriaga and
Millan [140] utilized the ErrP to control an external autonomous device within the concept of
shared autonomy. The shared autonomy describes the situation where the user has only a
supervisory control over the action of a system upon which he/she has no control. Consistent
with the previous reports, they reported an ERP response located over the medial-frontal cortex
with a negative amplitude around 260ms after an error was detected by the subject. Moreover,
the amplitude of the ERP is inversely [140] modulated by the frequency of the autonomous
system error.

15
Figure 3. A schematic of how an ErrP paradigm can be used in a BCI system (figure copied from [138]
with permission). Left: Detecting the existence of error and correct the last movement. Right: Using ErrP
in a learning process to update a BCI classifier.

A real-time and closed-loop BCI system can be regarded as a control problem. The ErrP can be
used to adjust the input control signals to the device. While in a traditional control system, the
adjustment is performed by the using linear or nonlinear controllers, in a BCI system where the
brain plays the role of controller, the adjustment can be automatically performed by the power of
brain signals (for more information see review [141]). Finding a suitable controller in a
traditional control system has become a solvable problem; however, understanding brain-
controlled signals and translating them into logical and stable commands for usage in an external
device remains challenging. This investigation is further discussed in a study by Artusi et al.
[142].
The process of using ErrP in a closed-loop BCI system could be considered as analogous to
“learn from your mistake.” In contrast to a traditional control system, in which error signal can
be sensed in milliseconds, the brain does not produce an ErrP until 200ms-700ms after the
subject receives feedback [139, 142]. The feedback is the relevant event whose onset engages the
brain circuits to process error-related information. The delay and non-stationarity of the signal
slows the system and makes real-time implementation difficult. Additionally, since the ErrP does
not contain any information about direction or magnitude, there is still the challenge of how to

16
adjust command signals based on detected ErrP in a multi-degree-of-freedom control system.
Thus, most BCI systems are designed using pre-learned algorithms to perform a task in a closed-
loop BCI [140, 143]. Recently, Iturrate et al. [144] developed a BCI system using the ErrP to
autonomously complete a task after a training time of several minutes. In their task, a brain-
controlled robotic arm learned how to reach a specific target based on a pre-learned algorithm
using ErrP paradigm.
4.2 ErrP Analysis & Classification Methods
One approach to extracting the ErrP is to detect the discrepancy of the observed action and the
translated action in the BCI platform. Ferrez and Millan [139] found an interaction between the
subject and the BCI system. They observed positive peaks at 200ms and 450ms after feedback
and negative peaks 250ms and 450ms after feedback. They also observed that ErrP amplitude is
higher as the error rate decreases. Chavarriaga and Millan [140] investigated the consequences of
the subject monitoring an external agent that the subject does not have control over. They used a
cursor movement paradigm and estimated the posterior probability of moving the cursor in the
wrong direction as 𝑃𝑒𝑟𝑟 by classifying the EEG signal using a Gaussian classifier. They found
that electrode locations FCz and Cz were most closely correlated to the ErrP response.
Itturate et al. [145] designed a study where a subject observed a virtual robot performing a
reaching task. The subject was instructed to judge the robot motion based on prior information of
the correct path. The averaged EEG waveforms at each electrode location were calculated, and
the results showed a significant difference between the correct and incorrect operation of the
robot. On error trials, a sharp positive peak at approximately 300ms was observed and was
followed by a negative peak at approximately 400ms. The averaged EEG waveforms were
derived in two steps: First, bipolar channels in the medial and posterior regions within the range
[150-700ms] were selected, offset components were removed, a bandpass filter of 0.5-10Hz was
applied, and the result was down-sampled to 64Hz; Second, they applied a Functional Decision
Tree in their AdaBoost classification algorithm to the resulting feature vector. Ten-Fold cross-
validation suggested that the resulting averaged EEG waveforms distinguished between correct
and incorrect motion of a robot.

4.3 ErrP Applications and Targeted Patients

The use of ErrP in BCI systems was initially investigated by Ferrez and Millan [139].
Chavarriaga and Millan [140] employed the ErrP to allow a user to control and correct the
behavior of an external autonomous system. In their approach, the user watched and maintained
supervisory control over the autonomous system in order to correct behavior of a system without
any direct or continuous control.
ErrP has been employed for robot reinforcement learning [145], 1D cursor control, [139, 140,
146-150] and 2D cursor control [144, 151]. Iturrate et al. [143] used ErrP with shared control for
a 2D reaching task. ErrP has also been used in BMI systems to control artificial [152] and robotic

17
arms, [149, 153], and it has been used to teach a robotic BMI system how to reach a particular
target in a 2D plane [144].
The ErrP can provide additional information to improve closed-loop BCI systems. It is likely
that, in the future, the ErrP will allow a user to observe and spontaneously make the desired
change in a BCI system without the need for directly performing a control task [154, 155].

5 Hybrid Paradigms
5.1 Overview
A hybrid paradigm refers to a combination of two or more physiological measures in which at
least one is EEG (for review see [156-158]). The other physiological measures could be other
bio-signals such as heart rate (ECG), eye movements (EOG) or hemodynamic signal recorded by
fNIRS [159]. In hybrid paradigms, sequential or simultaneous processing structures can be used
to output control commands to the BCI system [157]. Figure 4 shows a schematic of each
system. In the simultaneous processing configuration, bio-signals concurrently enter two (or
more) parallel decoding systems while in a sequential setting one decoding paradigm acts as a
gating function for another decoding system. Visual P300, SSVEP, and SMR paradigms are the
most prevalent paradigms in the development of hybrid BCI systems [82, 116].

User Application
Paradigm Type 1 Paradigm Type 2
Interface Interface

(a)

Paradigm Type 1

User Application
Interface Interface

Paradigm Type 2

(b)

Figure 4. A schematic of two employed structures in hybrid BCI systems; a) Sequential form, b)
Simultaneous form.
In recent BCI studies, combining various mentioned paradigms or combining a BCI paradigm
with another interface has shown to enhanced BCI performance. For example, Luth et al. [160]
paired P300 and SSVEP in controlling an assistive robotic arm. In a 2D cursor task, Li et al.
[161] used Mu and Beta rhythms for controlling horizontal movement and P300 for vertical
movement. Bi et al. [162] also used a combination of SSVEP and P300. The SSVEP paradigm

18
was used to extract directional information (clockwise/counterclockwise), and the P300 was used
to decode the speed of the cursor. To minimize false positive rates of the user’s resting state,
Pfurtscheller et al. [137] introduced a hybrid BCI that combined of event-related synchronization
(ERS) and SSVEP collected from an EEG channel located above motor cortex and another
electrode located above visual cortex. Allison et al. [163] developed a 2D cursor control BCI
incorporating SSVEP for decoding horizontal and event-related desynchronization (ERD) for
vertical movements.

5.2 Analysis & Classification Methods

Duan et al. [164] developed a hybrid BCI platform to control a robot to execute the grasp motion
using SSVEP, Mu rhythm, and feet motor imagery. A comparison between a single-paradigm
versus hybrid neurofeedback real-time BCI consisting of motor imagery and SSVEP were
reported by Yu et al. [165]. They used the Common Spatial Pattern (CSP) method to extract
maximally different mu and beta band powers for distinct classes of motor imagery and utilized
the CCA to decode flickering frequency. Hyung Kim et al. [166] combined EEG and eye
tracking for controlling a quadcopter. They discriminated two mental states of intentional
concentration and non-concentration using EEG signals. They applied CSP to filter EEG and
then utilized the Autoregressive (AR) model to estimate the spectral power of EEG from 11 Hz
to 19 Hz. The classification between two states of the model was performed by SVM, and it
worked as a gating function to switch on the quadcopter. Afterwards, eye tracker was exploited
to control the direction of the drone. Kim et al. [167] utilized the same BCI platform in a
pointing and selection task. A summary of previous studies on hybrid BCI is shown in Table 4.
Further information in regard to hybrid BCIs can be seen in recent review articles [116, 156-158,
168, 169].

Table 4. An overview of previously published BCI hybrid paradigms.

Reference Task Feature Classification method
[160] Control Rehabilitation Sequential P300 and SSVEP Matched filter, FFT
robotic devices
[161] 2D cursor control Simultaneous mu/Beta SVM
rhythm and P300
[137] Control an orthosis Sequential ERS and SSVEP FLDA

[170] Control an artificial upper Simultaneous motor imagery CCA, FLDA

limb with 2 (Degree of and SSVEP
Freedom) DoF
[163] 2D cursor control Simultaneous ERD and LDA
SSVEP
[166] Quadcopter flight control Sequential motor imagery SVM
and eye tracking

19
 [162] 2D cursor control Simultaneous SSVEP and RBF SVM, FLDA
P300
[164] Robotic grasp control Sequential SSVEP and Mu CCA, STFT
rhythm
[171] Robotic control Sequential EOG and ERP LDA

[172] Quadcopter flight control Simultaneous EEG and NIRS LDA

[165] Neurofeedback training Simultaneous motor imagery CCA, CSP+FFT

and SSVEP

5.3 Applications and Targeted Patients Population

Hybrid paradigms have been developed and applied to many BCI applications. Some studies
have used a combination of two EEG signals to control virtual objects and prosthetic devices.
For example, Bi et al. [162] used P300 and SSVEP paradigms to control a 2D computer cursor.
Allison et al. [163] used SMR and SSVEP paradigms to control a computer cursor in 2D space.
Li et al. [161] used SMR and P300 paradigms to control a 2D computer cursor. Horik et al. [170]
combined SMR and SSVEP to control a 2-DOF artificial upper limb. Also using SMR and
SSVEP, Duan et al. [164] controlled a humanoid robot to perform simple tasks. Pfurtscheller et
al. [137] evaluated the feasibility of orthosis control using a combination of SSVEP and motor
imagery paradigms. Yu et al. [165] also used a combination of SSEVP and motor imagery to
enhance training performance for a motor imagery paradigm. Luth et al. [160] employed a hybrid
P300 and SSVEP for a low-level application of a semi-autonomous robotic rehabilitation system.
In other hybrid BCI systems, EEG is combined with other bio-signals such as EOG. For
example, Kim et al. [167] and Malechka et al. [173] developed wearable hybrid BCI systems
using EEG and an eye-tracking device. Kim et al. [166] employed their system with a motor
imagery paradigm to control a quadcopter in three-dimensional space. Ma et al. [171] developed
a novel hybrid BCI using eye movements and the P300 ERP to control devices such as mobile
robots and humanoid robots. Other studies have combined EEG paradigms with other
neuroimaging techniques (e.g., fNIRS) for communication purposes in ALS and monitoring of
patients vigilance state [159] and to control external devices such as quadcopters [172].

6 Other Paradigms
In addition to the most common BCI paradigms detailed above, other paradigms have been
examined in a limited number of studies. Table 5 shows a number of previously generated EEG-
based BCI paradigms and a brief description of each system. Among the paradigms shown in
Table 5, the “covert and overt attention,” “discrete movement intention” and “auditory
paradigm” paradigms have shown promise as BCI devices.

20
Covert and Overt Attention Paradigm: Hunt and Kingstone [174] were among the first to use a
covert attention BCI paradigm. They discovered the existence of a dissociation between
voluntary shifts in overt and covert attention. In a covert attention paradigm, the subject is
instructed to look at a centrally located fixation point. The subject’s task is to follow another
point (e.g., cursor) without overt eye movement. In contrast to covert attention, an overt attention
task the subject is instructed to use overt eye movements while they attend to a moving object.
Both of these approaches depend on visual attention, and the EEG signals are typically recorded
from the posterior cortex. Additional studies using this paradigm were performed by Kelly et al.
[175, 176]. In [176], they investigated Parieto-occipital alpha band (8-14Hz) EEG activity in a
covert attention paradigm to classify the spatial attention to the right and left. Later, they
confirmed the existence of distinct patterns in overt and covert attention during preparatory
processes [175]. Tonin and colleagues [177, 178] used a covert attention paradigm in a 2-class
classification problem (i.e., attention to right corner target of a monitor vs. attention to left corner
target of a monitor) to control a BCI system in online mode and provide feedback to the subject
by showing the result of classification. Additionally, Treder et al. [179] employed a covert
attention paradigm for a two-dimensional BCI control to covertly choose a target among six
targets which are equally distributed around a circle on a screen.
Discrete Movement Intention Paradigm: In the movement intention paradigm, EEG signals
collected before movement onset are used to detect the intended movement of a BCI user and
manipulate the environment accordingly. In these studies, the subject may or may not be able to
physically execute an actual movement. However, their EEG signals can confirm the intention of
movement before movement occurs [180]. In some studies, the terminology “attempted” [181] or
“planned” [182] movement is used to describe the intention of movement. This paradigm can be
primarily and fruitfully used in motor rehabilitation. By using the movement intention paradigm
in robotic rehabilitation, a patient’s intentions can initiate the movement of a robot. Frisoli et al.
[183] used a gaze-dependent variation of this paradigm for upper limb rehabilitation. EEG
signals were used to adjust jerk, acceleration, and speed of the exoskeleton. As a means of
therapy for post-stroke patients, Muralidharan et al. [181] successfully extracted intention from
EEG signals to open or close a paretic left/right hand. A similar study by Lew et al. [184] was
performed using two able-bodied subjects and two post-stroke patients with an overall success
rate of 80% in detection of movement. Investigation of EEG signals for the intention of the right-
hand and left-hand movements was performed by Bai et al. [185]. Bai et al. [180] predicted wrist
extension movements in seven healthy subjects. Zhou et al. [186] classified the information from
EEG signals during the moment in which the subjects (four healthy, two stroke) intended to
perform shoulder abduction or elbow flexion movements. Also, EEG data were analyzed for a
chronic stroke patient before the onset of hand movement toward a target [187].
Auditory Paradigm: Auditory paradigms have also been investigated by a number of BCI
researchers [83]. Brain signals can be modulated either by using an intention-driven
(endogenous) BCI or stimulus-driven (exogenous) BCI depending on the paradigm. For
example, auditory P300 [188] considered as an exogenous stimulation is used to evoke auditory

21
steady-state responses (ASSR) [189]. ASSR is an auditory evoked potential in response to rapid
auditory stimuli; Picton et al. [189] showed that the ASSR maximum amplitude is recorded from
the vertex of the scalp. Sellers and Donchin [188] compared P300 auditory and visual paradigms
in patients with ALS. Although they showed proof of principle with the auditory P300 BCI,
performance was significantly better in the visual condition. Nijboer et al. [84] also validated the
feasibility of an auditory-based BCI by comparing with visual-based BCI. Ferracuti et al. [190]
used a novel paradigm where five classes of auditory stimuli were presented in five different
locations of space.
Somatosensory (Tactile) paradigm: In recent years, the usage of a somatosensory paradigms for
patients with visual impairment has become popular. In this paradigm, vibrotactile sensors are
located in pre-determined parts of body while stimulations happen at different frequencies [191].
The stimulations of these sensors will be reflected on EEG signals recorded from the scalp.
Muller-Putz et al. [124] investigated the usability of the steady-state somatosensory evoked
potential paradigm. Other researchers employed tactile P300 paradigms in their BCI systems
[192]. Imagined tactile paradigms were also investigated by Yao et al. [85]. The somatosensory
paradigm was utilized in assisting patients with locked-in syndrome [193, 194].
Reflexive Semantic Conditioning Paradigm: BCIs for communication purposes have been
developed since the late eighties; however, it remains a great challenge to provide reliable results
for people with severe motor disabilities, such as completely locked-in syndrome (CLIS). A
paradigm named "reflexive semantic conditioning" (based on Pavlov theory) was developed and
tested in healthy participants as well as in people with diagnosis of ALS. The main goal of the
paradigm is to deal with communication problems in CLIS and ALS patients [195-199].

Table 5. Less Common EEG-based BCI paradigms.

References Paradigm Description
[174], [175], [176], Overt (Covert) attention paradigm: the EEG signals are generated
[177], [178], [179] through overt (eye movement) or covert (eye fixation) attention on
movements of a cursor on a screen.
[180], [181], [182], Discrete movement intention paradigm: using recorded EEG signals,
[183], [184], [185], intention of subject is decoded prior to performing a task. It is a
[186], [187], [200], popular paradigm in Rehabilitative robotics.
[201], [202], [203], [204]
[83], [84], [189], [188], Auditory paradigm: the origin of EEG signals is related to an
[190], [205], [206], [207] external sound stimulus. The potential future application could be for
aural prostheses.
[208] Olfactory paradigm: smelling/remembering an odor could cause
distinguishable changes in EEG signals.
[209], [210], [211] Real movement paradigm: EEG signals are recorded (used for
control) while subject is performing real movement.

22
 [85], [191], [212], [124], Somatosensory (Tactile) paradigm: tactile sensors are used to
[192], [193], [194], [213] stimulate parts of body (in different frequency) while the EEG
signals are recorded for classification and generating control
commands.
[154], [155] Passive paradigm: passive EEG signals without the purpose of
voluntary control, such as the user’s intentions, situational
interpretations, and emotional states, are utilized as a complementary
BCI.
[214] Non-motor mental imagery paradigm: EEG signals origin from non-
motor imaginary tasks such as math calculation.
[215], [19], [216], [217], Slow cortical potentials paradigm: low frequency EEG signals
[218] recorded from prefrontal cortex are modulated through a long
training time of a cognitive task while receiving neurofeedback, as
well.
[219], [220], [221] Observation-based paradigm: EEG signals are collected while the
subject observes different actions performed by an external device
(such as prosthetic hand).
[222], [223], [224] Eye-movement paradigm: EEG signals are recorded while the
subject is instructed to have eye movement to different directions.
Discrete classes are extracted from EEG signals for controlling
external objects.
[195], [196], [197], Reflexive Semantic Conditioning Paradigm: The EEG signals is
[198], [199] modulated by presenting various statements. The paradigm is
primarily used for communication in ALS and CLIS populations.

7 Current Issues and Future Considerations

In recent years, BCI research has made significant progress in neurorehabilitation and assistive
device technology. Each of the methodologies presented in this review has promise as brain-
controlled external prosthetic devices for spinal cord injury patients and other with severe
communication disorders such as ALS, LIS, and Multiple Sclerosis (MS). No doubt, there is a
strong possibility that BCI systems will be commercialized shortly. In fact, a limited number of
commercial devices are already available. Some programs such as the BNCI Horizon 2020
project [225] has established a future roadmap for BCI systems. Nevertheless, there are critical
limitations, challenges, and issues related to BCI paradigms and platforms that should be
addressed and considered by the BCI community. It is a common practice in the BCI literature to
report the results of a study in term of classification accuracy. Few publications address issues
such as reliability of the platforms. Also, it is often not clear what are the behavioral, cognitive,
sensory, and motor functional outcomes in a BCI study. To further advance BCI research for
practical applications, we believe these important issues should be addressed in future work.

23
Training Time and Fatigue: One of the most significant challenges in BCI is the training
required for a subject to become proficient with the system. Most paradigms have lengthy
training times, which can cause fatigue in subjects. Although there are examples of long-term use
of stimulus-based BCI such as [112, 226], overall external stimulus paradigms such as P300-
based systems may cause fatigue over extended periods of use. Moreover, subject-dependency
and even inter-session variability can make it necessary for BCI researchers to collect calibration
data at the beginning of each session. To mitigate this problem, some recent studies have used
methods such as transfer learning to develop a zero training/generic BCI model that generalizes
to most subjects [81, 227-230].
Signal Processing and Novel Decoders: Many different decoding methods, signal processing
algorithms [231], and classification algorithms [30] have been recently investigated.
Nevertheless, the information extracted from EEG signals does not have a high enough signal-to-
noise ratio to control a system such as a neuroprosthetic arm with multiple degrees of freedom.
More robust, accurate, and fast online algorithms are required to be able to control a multi-DOF
system. In recent years, some researchers have suggested that source localization of EEG [232]
and active data selection [233] can improve classification performance. Other researchers have
suggested the use of advanced machine learning and deep learning methods [234-237], which
have potential to extract additional features that can improve classification. Furthermore, other
researchers have proposed adaptive classifiers and decoders in order to compensate for the non-
stationary nature of EEG signals [238]. Meanwhile, a particular standardization system is
essential to evaluate the performance of decoding algorithms in specific applications and BCI
systems [239].
From Shared Control to Supervisory Control in Closed-Loop BCIs: A closed-loop BCI is
considered to be a co-adaptive and mutual learning system where the human and computer learn
from each other, while adaptation in mathematical algorithms and neural circuits also occurs.
Millan [240] described the closed-loop BCI system as a “two-learner system.” The terms “shared
control” and “hybrid control” were also used to describe the contributions of both human and
machine in performing the control task [20, 55, 143, 241-243]. The shared BCI system includes
both high-level and low-level control systems. High-level control commands are generated by
the brain and traditional control systems are responsible for low-level control tasks. Interestingly,
in high-level control, there is always a tradeoff between the natural way of control and subject
fatigue. The ideal BCI system with mutual interaction can be described as a supervisory control
system in which the subject is the leader with minimum involvement (in high-level control), and
the BCI system serves as an intelligent system (in low-level control) [140, 244]. By cognitive
monitoring, the user can act as a supervisor of the external autonomous system instead of
continuously interacting with control commands.
The definition of a closed-loop control system is currently a controversial issue [141, 245]. In
reality, in an EEG-based BCI, some types of artificial sensory feedback, except visual feedback
[246], should be considered to provide the subject with the highest feeling of control in a closed-

24
loop form. In contrast, invasively controlled prosthetic arms include the sense of touch, which
increases the perception of a closed-loop control system [247]. In EEG-based BCI platforms,
various feedback mechanisms have been investigated, including brain stimulation [35], reaction
force [248], and somatosensory stimulation [42].
Development of New EEG Technologies: Since scalp EEG is categorized as low-cost and
affordable technology among brain monitoring technologies, it has the potential to be
commercialized for general public [3]. There are studies to determine alertness/drowsiness from
brain dynamics while evaluating behavioral changes with applications to drowsy driving. Having
a portable EEG headset helps understand the brain dynamics underlying integration of perceptual
functions of the brain in different scenarios. Some studies evaluate behavioral changes in
response to auditory signals in a driving environment and find correlations between brainwaves
and other sensory inputs such as haptic feedback. As part of development for this technology
many researchers have investigated the development of wearable and wireless EEG headsets
[173, 249]. Dry EEG sensors have also developed [250-253]. These sensors do not require skin
preparation or gel applications that are required of conventional wet sensors. The development of
these new EEG headsets could facilitate the application of BCIs beyond current levels. For
example, a forehead EEG-based BCI can be used as a sleep management system that can assess
sleep quality. The device could also be used as a depression treatment screening system that
could evaluate and predict the efficacy of rapid antidepressant agents. Nevertheless, there are
still limitations to dry electrode technology. For example, the sensors are uncomfortable to the
scalp and they are very sensitive to muscle and movement artifacts. In addition, current dry
headsets recording quality typically degrades after approximately one hour.
Neurofeedback and the Future Paradigms: One future direction of BCI is its application in
neurofeedback [254]. Neurofeedback, a type of biofeedback, is the process of self-regulating
brainwaves to improve various aspects of cognitive control. In some cases, neurofeedback-based
BCIs could potentially replace medications, thereby reducing the negative side effects of
medication. For example, this technology could help to alleviate cognitive and pathological
neural diseases, such as migraine headaches. A headache detection and management system can
notify migraine patients’ imminent migraine headaches days in advance while offering a
treatment in neurofeedback form. Neurofeedback-based BCIs could also be developed to assist
the treatment of people with addiction, obesity, autism, and asthma [255]. New EEG paradigms
can also be developed to facilitate cognitive control [256] and interaction with the environment
[154, 155]. For instance, ErrP can be used as a useful mechanism to enhance neurofeedback
since it allows a user to observe and spontaneously make the desired change in a BCI system
without the need to directly perform a control task. Moreover, new cognitive models of
neurofeedback can be developed for neuro-rehabilitation of cognitive deficits, such as ADHD,
anxiety, epilepsy, Alzheimer’s disease, traumatic brain injury, and post-traumatic stress disorder
[257-263].

25
8 Conclusions
Currently, there is a high level of interest in non-invasive BCI technology. Many variables have
facilitated the popularity of these systems. Because of wireless recording, low-cost amplifiers,
higher temporal resolution, and advanced signal analysis methodology, the systems are more
accessible to researchers in many scientific domains. As described in this review, a critical aspect
of employing a BCI system is to match the appropriate control signal with the desired
application. It is essential to choose the most reliable, accurate, and convenient paradigm to
manipulate a neuroprosthetic device or implement a specific neurorehabilitation program. The
current review has evaluated several EEG-based BCI paradigms in terms of their advantages and
disadvantages from a variety of perspectives. Each paradigm was described and presented in
terms of the control signals, various EEG decoding algorithms, and classification methods, and
target populations of each paradigm were summarized. Finally, potential problems with EEG-
based BCI systems were discussed, and possible solutions were proposed.

Acknowledgments
The authors are grateful to Dr. Jose Millan for his insightful comments to an early draft of this
manuscript. The assistance of Megan Pitz to the manuscript is also appreciated. This work was
partially supported by NeuorNET at UTK.

Author Contributions
R.A. and S.B. contributed equally and have shared first authorship. E.S. and Y.J. revised the
paper and contributed with insightful comments. X.Z. was involved in all aspects of the study.

Competing Financial Interests

The authors declare no competing financial interests.

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