C H A P T E R

26
Noninvasive Brain–Computer Interfaces
Gerwin Schalk1,2,3, Brendan Z. Allison1,4
1National Center for Adaptive Neurotechnologies, Albany, NY, United States; 2Albany Medical College,
Albany, NY, United States; 3State University of New York at Albany, Albany, NY, United States;
4University of California San Diego, La Jolla, CA, United States

O U T L I N E

Introduction357 Brain–Computer Interfaces to Enhance Function 365

Overview of This Chapter 357 Introduction365
Electroencephalography358 User State 365
Metabolic Activity 360 Error Detection 366
Sleep367
Brain–Computer Interfaces to Replace Function 361
Image Recognition 367
Introduction361
Neuromarketing367
Communication Functions 361
Simple Communication Functions 361 Brain–Computer Interfaces to Improve Function 368
Complex Communication Functions 361 Introduction368
Control Functions 362 Improvements to Motor Function 368
Computer Functions 362 Improvements to Other Functions 370
Worn Robotic Devices 362
Summary of the Current State of Noninvasive
Mobile Robotic Devices 362
Brain–Computer Interfaces 371
Future Directions 363
Scientific and Technical Basis 371
Brain–Computer Interfaces to Restore Function 363 Translating Brain–Computer Interfaces From
Introduction363 Scientific Endeavors Into Clinically and
Devices That Produce Limb Movements 363 Commercially Successful Technologies 371
Functional Electrical Stimulation 363 Commercialization Potential of Various Noninvasive
Orthoses363 Brain–Computer Interface Technologies 372
Brain–Computer Interfaces for Restoration 363 Conclusions372
Upper Limb 363
Acknowledgments372
Lower Limb 364
References372

INTRODUCTION
Overview of This Chapter
Brain–computer interfaces (BCIs) measure brain
activity, extract features from that activity, and convert
those features into outputs that replace, restore, enhance,
supplement, or improve human functions.
BCIs may replace lost functions, such as speaking
or moving. They may restore the ability to control the
body, such as by stimulating nerves or muscles that
move the hand. BCIs have also been used to improve
functions, such as training users to improve the
remaining function of damaged pathways required to
grasp. BCIs can also enhance function, like warning a

Neuromodulation, Second Edition 357

http://dx.doi.org/10.1016/B978-0-12-805353-9.00026-7 © 2018 Elsevier Ltd. All rights reserved.
358 26.  NONINVASIVE BRAIN–COMPUTER INTERFACES

(A) (B) (C) (D)

20
0.4

AMPLITUDE (µV)
0.6

2 10 0.4
0.2 r

r2
0.2

0.0 0 0.0
10 cm 0 20 40 60 0 20 40 60
FREQUENCY (Hz) FREQUENCY (Hz)

FIGURE 26.1  (A and B) The changes in mu activity centered around 12 Hz for (A) actual and (B) imagined right-hand movements. The colors
reflect the proportion of the signal variance accounted for by the task. These two images show that imagined movements produce changes that
are less pronounced than those resulting from actual movements, but show a similar topographical distribution. (C) EEG power over site C3 for a
different subject who rested (dashed line) or performed right-hand movement (solid line). The mu activity at about 12 Hz and its harmonic around
24 Hz are both greatly reduced by movement. (D) The resulting r2 correlations for rest versus movement. This image also shows that movement
primarily affects power in the mu frequency bands and its harmonics. From Schalk, G., McFarland, D.J., Hinterberger, T., Birbaumer, N., Wolpaw, J.R.,
2004. BCI2000: a general-purpose brain–computer interface (BCI) system. IEEE Trans. Biomed. Eng. 51 (6), 1034–1043.

sleepy driver to wake up. Finally, a BCI might supple-
ment the body’s natural outputs, such as through a
third hand.
Different techniques are used to measure brain activ-
ity for BCIs. Most BCIs have used electrical signals that
are detected using electrodes placed invasively within
or on the surface of the cortex, or noninvasively on the
surface of the scalp [electroencephalography (EEG)].
Some BCIs have been based on metabolic activity that
is measured noninvasively, such as through functional
magnetic resonance imaging (fMRI).
This chapter is focused on providing an overview of
noninvasive BCIs. After a brief review of the relevant
aspects of EEG and fMRI, each of the subsequent sec-
tions is dedicated to one of the four different purposes
that a BCI may serve and that have been realized as of
this writing.
Electroencephalography
EEG sensors detect the coordinated activity of
large groups of neurons—the electrical signature of
individual or only a few neurons is not detectable by
electrodes outside the skull. EEG sensors are usually
placed in an electrode cap that is designed to position
the electrodes over specific brain regions. Some work
has presented EEG electrodes in headbands, head-
phones, glasses, or other less obtrusive headwear. For
many years, EEG electrodes were usually composed
of silver/silver chloride rings that were housed in a
plastic disk. Electrode gel was needed to establish an
electrical connection between the scalp’s surface and
each electrode. Work has validated dry electrodes that
eliminate the time and inconvenience of gel (Guger
et al., 2012; Fridman et al., 2016), but to what extent
dry electrodes provide stable EEG, in particular in
uncontrolled environments and when used by nonex-
perts, is still unclear.
Different types of features can be detected in the
EEG and may serve as the basis for BCIs. One of the
most important of these features is oscillatory activ-
ity in different frequency bands: delta (less than 4 Hz),
theta (4–8 Hz), alpha (8–12 Hz), beta (18–25 Hz), and
gamma (greater than 30 Hz). While the origin of oscil-
latory activity is still debated, oscillations probably
reflect interactions between the cortex and the thalamus
or other subcortical structures. Delta activity is most
prominent during deep sleep when high-amplitude
delta waves can be prevalent over many areas. Theta
activity is prevalent during light sleep and meditation.
Alpha activity increases over occipital areas when peo-
ple rest with their eyes closed and during light sleep,
and (along with theta and beta) may be used in BCIs to
indicate workload or concentration. The phenomenon
of “alpha blocking” refers to the decrease in alpha activ-
ity that occurs when a person is asked to open the eyes
and perform a complex task. Because this is one of the
most obvious changes in the EEG that people can eas-
ily produce, users are often asked to alternate between
eyes-closed relaxation and eyes-open concentration to
confirm that their EEG system is working properly.
The changes in EEG activity during sleep are driven
largely by activity in the pons, thalamus, and occipital
regions. Activity in the same alpha frequency range, but
detected over sensorimotor instead of visual areas, is
called the mu rhythm. The mu rhythm is modulated by
expected, actual, observed, or imagined motor move-
ments or associated sensations. These changes in mu
activity have been called event-related (de-)synchroni-
zation or ERD/S (see Fig. 26.1), and have been widely
used in BCIs.
Beta and gamma activity is most apparent during con-
centration and can also include harmonics of mu activ-
ity (Pfurtscheller, 1981; Pfurtscheller et al., 1997). These
frequency bands have been used in BCIs to detect con-
centration or information overload. Both bands are often

V.  BRAIN, COMPUTER AND MACHINE INTERFACING

 Introduction
divided into high and low, and low and high bands can
reflect more details of the brain dynamics underlying
cognition and emotion. While the source and purpose
of the brain’s different oscillatory activities are not fully
understood, they seem to generally reflect thalamocorti-
cal interactions (primarily through layers 4 and 5 of the
cortex) to coordinate activity across different regions and
neural populations (Pfurtscheller and Lopes da Silva,
1999).
In addition to oscillatory activity that is detected in
the frequency domain, electrophysiological activity in
the time domain also reveals useful information. When
activity is time locked to a stimulus, activity changes
following the stimulus are called event-related poten-
tials (ERPs). Because ERPs that result from only a
single stimulus are usually too noisy to be detected,
both researchers and BCI systems typically repeat the
task and associated stimulus several times to acquire
several ERPs that can be averaged together, resulting
in a clearer signal. ERPs are often named according to
their electrical valence (positive or negative) and time
in milliseconds from the relevant event. For example,
the P300 ERP reflects a positive change in voltage
of about 300 ms after an event, and reflects cogni-
tive processing of that event. The P300 has different
subcomponents, notably the P3a and P3b, that each
reflect different aspects of task processing. The fron-
tally prominent P3a is largest when processing novel
stimuli, and reflects attentional alerting and the need
to update working memory. The more parietal P3b
reflects memory updating and planning a response,
such as pressing a button or counting. Concordantly,
the sizes of a person’s frontal and parietal areas are
correlated with the amplitude of the P3a and P3b,
respectively. The P300 reflects contributions from
other cortical and subcortical regions as well, includ-
ing the hippocampus, anterior cingulate, and medial
temporal lobes. Earlier components, such as the P100
and N170, instead convey early perceptual processing,
and show activity in earlier processing areas such as
V1 (primary visual cortex) (Polich, 2004).
Time domain activity may also be detected prior to
an anticipated event, such as a button press. Before a
voluntary movement, the readiness potential (RP; also
called Bereitschaftspotential or BP in German) will
change across two stages (see Fig. 26.2). About 1.5 s
prior to the movement, the supplementary motor area
(SMA) and related motor preparation areas exhibit a
slow bilateral negative change in voltage. About half
a second prior to movement, a much sharper change is
apparent contralateral to the movement in the SMA and
the primary motor cortex (M1). These two stages seem
to reflect movement planning and execution, respec-
tively. The RP is one type of movement-related cortical
V.  BRAIN, COMPUTER AND MACHINE INTERFACING
359
MRCP
(A) Negative
Slope
Bereitschaftspotential
(B) EMG
(C)
Pre-BP BP NS 5µV
200ms
FIGURE 26.2  Different components of the readiness potential, also
called the Bereitschaftspotential (BP), are shown. The rightmost verti-
cal line reflects the onset of a voluntary movement. In this image, the
voluntary movement was self-paced tapping of the right index finger.
The BP phase shows a slowly developing negativity from about 1.5
to 0.5 s prior to the voluntary movement, which becomes more pro-
nounced during the period 0.5 s prior to the movement (Castermans
et al., 2013). MRCP, movement-related cortical potential; NS, negative
slope.
potential (MRCP), a family of signals that can index
movement speed, force, effort, precision, training, com-
plexity, concentration, and other factors (Shibasaki and
Hallett, 2006; Xu et al., 2016a,b).
Another time domain EEG phenomenon is the con-
tingent negative variation (CNV). The CNV is a bilateral
negative change that is prominent over the top of the
scalp, and primarily reflects activity from frontal areas.
The CNV reflects slow changes, on the order of a few
seconds, that can occur between a warning stimulus
(which informs someone that a relevant stimulus will
soon be shown) and an imperative stimulus (reflect-
ing that someone needs to take action). The CNV was
discovered over 50 years ago (Walter et al., 1964) and
has been extensively studied. It can reflect a variety of
factors, including emotional changes, focused atten-
tion, general arousal, and the stimuli’s expectancy and
perceived relevance, probability, intensity, and timing.
However, it has not been widely used in BCIs because
other types of signals described here are generally more
reliable, require less training, and allow higher band-
width communication.
Rapid presentation of visual stimuli (such as flicker-
ing LEDs or objects on a computer screen) can result
in steady-state visual evoked potentials (SSVEPs).
SSVEPs reflect the rapid firing of visual cortical areas,
primarily V1. If the user focuses attention on one stimu-
lus, EEG signals over visual areas increase in power at
that frequency and its harmonics. This allows BCIs to
detect which stimulus the user chose to attend to (see
Fig. 26.3).
If different stimuli are presented at the same fre-
quency but different phases, a BCI may also infer the
360 26.  NONINVASIVE BRAIN–COMPUTER INTERFACES

(A) (B) (E) 6.00 Hz 12.00 Hz

0.6

AMPLITUDE (µV)
0.45 0.6

R2
0.3 0.4
0.15 0.2
0 15.00 Hz 18.00 Hz
0
0 15 30 45 0 15 30 45

(C) (D)
0.6
AMPLITUDE (µV)

0.45 0.6
30.00 Hz 45.00 Hz

R2
0.3 0.4
0.6
0.15 0.2
0.4
0 0 0.2
0 15 30 45 0 15 30 45
Frequency (Hz) Frequency (Hz) 0

FIGURE 26.3  Steady-state visual evoked potential (SSVEP) activity elicited during selective attention to two oscillating checkerboards, each of
which oscillated at 6 or 15 Hz. (A and C) Spectral power for one subject over site O1 (A) or O2 (C). The solid and dotted lines show activity elicited
while the subject focused on the 15- or 6-Hz checkerboard, respectively. (B and D) The r2 values that reflect the correlation between different fre-
quencies and the instruction to focus on either target stimulus. (E) A topographic map of these differences. It is shown that selective attention to a
flickering stimulus increases power at the eliciting frequency and, to a lesser extent, the harmonics of that frequency. The SSVEP activity is much
more pronounced over occipital areas than over other sites. From Allison, B.Z., McFarland, D.J., Schalk, G., Zheng, S.D., Jackson, M.M., Wolpaw, J.R.,
2008. Towards an independent brain–computer interface using steady state visual evoked potentials. Clin. Neurophysiol. 119 (2), 399–408.

attended stimulus based on phase measurements in the

EEG (Nakanishi et al., 2014) or their autocorrelation with
an m-sequence in a variant of SSVEPs called code-based
VEPs or c-VEPs (Bin et al., 2011).
Vibrotactile stimuli can elicit steady-state somatosen-
sory evoked potentials (SSSEPs), and thereby may pro-
vide the basis for BCIs for persons without vision (Nam
et al., 2013). Steady-state auditory evoked potentials
(SSAEPs) have also been studied. Consistent with other
somatosensory evoked potentials (SEPs), SSSEPs and
SSAEPs involve activity in the corresponding primary
cortical sensory area in tandem with higher sensory
areas and relevant thalamic nuclei (lateral geniculate,
visual; medial geniculate, auditory; ventral postero-
lateral, somatosensory signals from the body). SEPs
have many clinical and research applications, primarily
exploring lower-level sensory processes. SEP research
FIGURE 26.4  These fMRI images show how a person with atten-
has also been used to study schizophrenia, depres-
tion deficit hyperactivity disorder (ADHD) exhibits different activity
sion, attentional deficits, epilepsy, and other conditions compared to a healthy control. Moreover, they show how fMRI can
(Norcia et al., 2015). reveal correlates of brain function well below the surface of the cortex,
which are difficult or impossible to detect with most other methods.
However, as of this writing, fMRI systems are practical only in hospital
Metabolic Activity settings. From ucdmc.ucdavis.edu (2014).

Techniques that measure metabolic activity detect

changes in blood oxygenation or other indirect measure-
ments of neuronal activity. Unlike electrical changes that
immediately reflect the activity of neuronal populations,
metabolic changes typically occur a few seconds after
neuronal activity changes. Despite this inherent lag,
some BCIs have used metabolic changes in successful
demonstrations.
The two most common imaging techniques that can
detect metabolic activity are fMRI and positron emis-
sion tomography (PET). FMRI and PET are volumetric
imaging techniques, i.e., they can detect changes deep
in the brain that are invisible to most electrical methods
(see Fig. 26.4). At the same time, they require expen-
sive and heavy equipment and they each incur other

V.  BRAIN, COMPUTER AND MACHINE INTERFACING

 Brain–Computer Interfaces to Replace Function
practical challenges: fMRI requires a very powerful
magnetic field that is unsafe for some patients, and PET
requires the injection of radioactive tracers. Functional
near-infrared spectroscopy (fNIRS) also detects changes
in blood flow and does not have these disadvantages. It
is safe, portable, and relatively inexpensive, although,
like EEG, it is limited to the detection of activity near the
brain’s surface. FNIRS requires placing a device on the
surface of the scalp that includes an emitter and several
detectors. The emitter shines light through the scalp;
this light is reflected off of the cortex, and reflection
parameters are changed depending on local cortical
activity.
BRAIN–COMPUTER INTERFACES TO
REPLACE FUNCTION
Introduction
BCIs for replacing lost functions have been explored
primarily to help persons with conditions that impair
most or all voluntary movements, including persons
with late-stage amyotrophic lateral sclerosis (ALS) or
tetraplegia. For individuals struck by these conditions,
BCIs may replace lost functions (such as communication
or movement control) by using brain activity to control
an artificial effector (such as a robotic arm or a communi-
cation system). The following sections give an overview
of BCIs for communication or control that have been
developed as of this writing.
Communication Functions
Simple Communication Functions
The simplest type of communication system entails
binary communication, such as answering “yes” or
“no” or switching a device on or off. One early BCI sys-
tem provided control of a switch or a ball on a monitor
using EEG signals associated with right-finger move-
ment. Data were acquired from six electrode pairs over
frontal and central sites, and the system provided asyn-
chronous operation (Mason and Birch, 2000). Another
system allowed users to modulate motor imagery to
direct a cursor to answer questions (Miner et al., 1998).
In another early study, a group from the US Air Force
trained subjects to use SSVEP activity to bank an air-
craft or to perform other tasks (Middendorf et al., 2000).
BCIs for switch control have continued to develop, with
switches based on MRCPs or hybrid fNIRS–EEG activ-
ity for wheelchair control (Cao et al., 2014; Koo et al.,
2015).
BCIs for very basic yes/no communication have
gained more attention as tools for persons diagnosed
with a disorder of consciousness (DOC). For these
V.  BRAIN, COMPUTER AND MACHINE INTERFACING
361
patients, even basic communication can confirm con-
scious awareness (Lesenfants et al., 2016; Ortner et al.,
2016). For example, if they can reliably answer yes or
no to questions regarding their city of birth or a par-
ent’s name, then doctors and family members have
objective proof of the ability and will to communicate.
BCIs designed for patients with DOC are designed to
interact with patients through auditory and/or tactile
stimuli since these patients may be unable to use visual
stimuli. These systems often use EEG-based measures
of the P300 or motor imagery (Mueller-Putz et al., 2013;
Schnuerer et al., 2015; Bauernfeind et al., 2015), though
an fNIRS-based system was also demonstrated in 2016
(Hwang et al., 2016).
Complex Communication Functions
BCIs for spelling often rely on the P300, a positive
deflection in the ERP that is dominant over parietal
areas and develops about 300 ms after stimuli that con-
vey relevant information and are relatively rare (Polich,
2004; Krusienski et al., 2008). In the first P300 speller
(Farwell and Donchin, 1988), healthy users observed a
6 × 6 matrix with letters and other characters, and were
asked to silently count each time a target letter flashed.
Next, each row or column of the matrix flashed sequen-
tially. Because the users counted only the row flash and
column flash that contained the target character, only
those two flashes generated a P300. The BCI system
could thus identify the target character by analyzing
the ERPs generated by each flash. Alternatives to the
method of flashing a row or column include the single
character, checkerboard, and splotch spellers (Jin et al.,
2012; Townsend et al., 2010; Guger et al., 2009). The
P300 BCIs work reliably for nearly all healthy people
and even ALS patients (Guger et al., 2009; Kaufmann
et al., 2013).
The P300 BCIs were validated with ALS patients in
2006 (Sellers et al., 2006; Vaughan et al., 2006). Since then,
noteworthy advances include brain painting, noted
below; the face speller, in which characters change to
faces instead of flashing (Jin et al., 2012; Kaufmann et al.,
2012, 2013); and nonvisual implementations of similar
P300-based systems that can use auditory or tactile stim-
uli for patients without adequate vision (Severens et al.,
2014; Furdea et al., 2009).
Cheng et al. (2002) presented an SSVEP BCI sys-
tem with 12 boxes that each flickered at a different
frequency. The numbers 1 through 10 and two special
characters were overlaid on the boxes. By focusing on
one box, the user could transmit a cell phone number
and call that phone. Later work from the same group
demonstrated improved performance using a c-VEP
approach (Bin et al., 2011), and other work showed
that phase information can also improve performance
(Nakanishi et al., 2014). SSVEP BCIs work for nearly
362 26.  NONINVASIVE BRAIN–COMPUTER INTERFACES
all healthy adults (Guger et al., 2012), but have not
been well explored with patients (but see Lim et al.
2013; Zoltan et al. 2016).
One of the most prominent BCI research directions
in the late 20th century relied on slow cortical poten-
tials (SCPs). These are very slow drifts in the EEG that
patients can learn to increase or decrease over months
of training, prominent over central sites. Patients
with no residual movement learned to modulate their
SCPs to move a cursor to iteratively select letters or
letter groups (Birbaumer et al., 1999). SCPs have not
been widely used in BCIs for several years because
of the long training time and low communication
bandwidth.
BCIs for spelling based on motor imagery gained
attention after work showed that patients with ALS
can use motor imagery to control a BCI (Kuebler et al.,
2005). Several people, including a patient with tetraple-
gia, were able to use motor imagery to direct a cursor up
or down toward different letters or letter groups on the
right side of a monitor while the cursor moved steadily
from left to right (Vaughan et al., 2006). In the Hex-O-
Spell approach (Blankertz et al., 2006), the user views a
monitor with a hexagon surrounded by six other hexa-
gons. The central hexagon contains an arrow, while the
other hexagons each contain six letters or other charac-
ters. At the start of each trial, the arrow begins moving in
a clockwise direction. When the arrow points to a hexa-
gon containing the desired group of characters, the user
can perform motor imagery (such as left hand grasping)
to make the arrow longer until it reaches the desired
hexagon. Next, the arrow returns to its starting point,
while the other six hexagons’ contents each change to
one of the six characters that the user just chose. The
arrow begins moving again, and the user can choose one
of the six characters in the same fashion. Thus, Hex-O-
Spell provides an intuitive two-level spelling interface,
with clear trial timing and goals, based on simple binary
motor control (Severens et al., 2014; Muller et al., 2008;
Rohani et al., 2012).
Control Functions
Computer Functions
The first noninvasive BCI publication described
an SSVEP-based BCI in which the user could direct
a cursor up, left, down, or right by focusing on one
of four oscillating boxes on a monitor (Vidal, 1973).
Several groups have described noninvasive BCIs for
one-, two-, or three-dimensional cursor control (Li
et al., 2010; McFarland et al., 2010; Wolpaw et al., 2003;
Muller et al., 2008; Coyle et al., 2011; Scherer et al.,
2012; Long et al., 2015).
V.  BRAIN, COMPUTER AND MACHINE INTERFACING
Cursor movement has been extended to a variety of
tasks with noninvasive BCIs, including web browsing
(Long et al., 2015; Mugler et al., 2010; Karim et al., 2006)
and gaming/virtual navigation (Scherer et al., 2012;
Coyle et al., 2011). BCI-based control of smart homes
can also implement virtual navigation through a home
environment (Edlinger et al., 2011; Carabalona et al.,
2012).
Another way that BCIs can replace lost functions is
through providing a mechanism for creative expres-
sion. BCIs have been used to compose music based on
EEG measures of emotion (Makeig et al., 2011). The
Brain Painting system allows users to create paintings
on a monitor through motor imagery or P300 activity
(Halder et al., 2009; Muenssinger et al., 2010). Several
ALS patients have posted their paintings online, and
reported significant enjoyment using the system.
Worn Robotic Devices
BCIs have been validated for control of wearable
robotic devices such as orthoses, prostheses, and exo-
skeletons. In Pfurtscheller et al. (2010) and Ortner
et al. (2011), subjects used SSVEP activity to control
a hand orthosis. In addition, in Pfurtscheller et al.
(2010), the system also allowed subjects to use mu
activity to activate or deactivate LEDs generating the
SSVEP. This hybrid approach allowed users to reduce
the annoyance caused by flickering stimuli. Related
work with BCIs to control functional electrical stimu-
lation, prostheses, and exoskeletons shows potential
to both replace natural mobility and facilitate therapy
(Angulo-Sherman et al., 2016; Rohm et al., 2014; Rupp,
2014).
Mobile Robotic Devices
Bell et al. (2008) demonstrated a P300-based BCI
system that presented either four or six images that
each corresponded to robot control commands. Data
were recorded from 32 EEG channels while nine
healthy subjects silently counted each time a target
image flashed. The overall accuracy across subjects
was 98.4%, yielding up to 24 bits/min. Each command
could direct a mobile robot equipped with a camera
to perform complex actions, relying on the robot’s
software to perform the low-level actions needed to
navigate around a room, get a glass, or perform other
tasks. In Galan et al. (2008), two healthy subjects each
participated in five sessions with 10 trials each, during
which they used a 64-channel EEG system to drive real
and simulated wheelchairs along a predefined path.
The BCI allowed three commands based on mental
tasks (left-hand imagery, turn left; rest, forward; word
association, turn right). The two subjects attained
100% and 80% overall accuracy.
 Brain–Computer Interfaces to Restore Function
Future Directions
Several promising directions for noninvasive BCIs
could replace lost functions in different patient groups.
For persons with DOC, noninvasive BCIs could go
beyond basic assessment and communication to provide
more detailed assessment of cognitive function, rehabili-
tation, outcome prediction, more complex communica-
tion such as spelling, and basic environmental control
(Li et al., 2016). For example, detection of SSSEPs associ-
ated with tactile stimuli could allow several choices for
patients who cannot see (Choi et al., 2015). Patients may
benefit from BCI systems for bladder or bowel control
(Collinger et al., 2013).
BRAIN–COMPUTER INTERFACES
TO RESTORE FUNCTION
Introduction
BCIs may be used to restore a patient’s ability to con-
trol his or her body. This category of BCIs aims solely to
help persons with disabilities. Unlike BCIs that replace
function, which control external devices (such as a
robotic arm), BCIs that restore function eventually move
the body’s own limbs. The goal is to bypass damaged
pathways that connect to functioning effectors, such as
the patient’s arms and hands. This technology could
benefit people with stroke, brain injury, spinal cord
injury, and other conditions that damage the brain or
spinal cord.
A substantial volume of work has focused on restor-
ing function to the arms and hands. This is a prevalent
need for many patients and is a relatively safe research
direction (restoring function to lower limbs adds the risk
of falling), and stimulating nerves or muscles in the arm
to initiate hand grasping may be simpler than producing
the extremely intricate and coordinated muscle activa-
tions necessary for walking or speaking. The following
section gives an overview of devices that have been used
to produce limb movements.
Devices That Produce Limb Movements
Functional Electrical Stimulation
A functional electrical stimulator (FES) is a device
to stimulate the muscle groups that control specific
movements, such as grasping, wrist dorsiflexion, or
knee flexion. Thus, patients who have lost the ability
to trigger muscle movement owing to damage to the
central nervous system can use a BCI system to bypass
these damaged pathways and an FES system to pro-
duce movements. FES devices may stimulate muscles
V.  BRAIN, COMPUTER AND MACHINE INTERFACING
363
through transcutaneous or subcutaneous electrodes.
Transcutaneous stimulation involves two or more con-
ductive pads that are placed on the surface of the skin
such that sending a current between the pads will trig-
ger muscle contraction. This noninvasive approach
avoids the cost, need for appropriate medical staff, and
other concerns of more invasive approaches. However,
because transcutaneous stimulators cannot be posi-
tioned with the same precision as invasive stimulators,
transcutaneous stimulation is less effective for some
muscle groups, and can cause relatively more dis-
comfort and muscle fatigue. Like noninvasive neuro-
imaging systems, transcutaneous stimulation requires
mounting the electrodes in the correct locations before
each usage session, which takes several minutes.
Invasive subcutaneous electrodes can be mounted per-
manently, while percutaneous electrodes are typically
used for shorter durations.
Orthoses
Orthoses are external, noninvasive devices that are
attached to the body to facilitate movement in vari-
ous ways. Simple orthoses include plastic braces that
can be strapped to the foot and ankle that help restore
some movement to persons with foot or ankle injuries.
Simple orthoses like these have no moving parts, no
degrees of freedom, and no need for a control mecha-
nism. More complex orthoses may entail mechanical
components that are designed to move the foot, arm,
shoulder, or other body part. These systems often have
more than 1 degree of freedom, and need some mecha-
nism to control their operation. In principle, BCIs are
an appealing control mechanism, as these users already
have limited mobility and thus reduced options to
control devices. With complex orthoses, BCIs may be
used in combination with shared control so that users
can simply imagine performing the desired movement
(such as walking) and the details of the timing, loca-
tion, intensity, and duration of muscle stimulation are
managed by the BCI system (Ortner et al., 2011; Rohm
et al., 2013; Millan et al., 2010).
Brain–Computer Interfaces for Restoration
Upper Limb
The Freehand neuroprosthetic is an implanted FES
device. In relatively early work, it was combined with
a 64-channel EEG-based BCI to restore grasp func-
tion (Lauer et al., 1999; Peckham and Knutson, 2005).
Later work allowed a single patient to use the Graz
motor imagery approach, which had already been val-
idated for orthosis control (Pfurtscheller et al., 2000),
with the Freehand system (Muller-Putz et al., 2005).
364 26.  NONINVASIVE BRAIN–COMPUTER INTERFACES

FIGURE 26.5  (A) A patient using an electrode cap to detect movement imagery that causes a noninvasive (transcutaneous) functional electri-
cal stimulator (FES) system to activate and trigger grasp function. (B) A different patient who instead uses an invasively implanted FES to control
grasp. From Muller-Putz, G.R., Scherer, R., Pfurtscheller, G., Rupp, R., 2006. Brain–computer interfaces for control of neuroprostheses: from synchronous to
asynchronous mode of operation. Biomed. Tech. (Berl.) 51 (2), 57–63.

FIGURE 26.6  The left (A, top) shows an orthosis that can be opened or closed by moving along the axes shown by white arrows via steady-
state visual evoked potential activity elicited by either of the black LEDs (B, left middle). The remaining three images show the orthosis moving
throughout three stages of opening and closing. The right shows a healthy volunteer using the orthosis to move a bottle with a white foam shield.
From Ortner, R., Allison, B.Z., Korisek, G., Gaggl, H., Pfurtscheller, G., 2011. An SSVEP BCI to control a hand orthosis for persons with tetraplegia. IEEE
Trans. Neural Syst. Rehabil. Eng. 19 (1), 1–5.

Fig. 26.5 presents examples of two patients using dif-
ferent types of FES systems with BCIs to restore grasp
control.
Many groups have explored other issues relating to
functional electrical stimulation and upper limb move-
ment. Other early work (Pfurtscheller et al., 2002) com-
pared the efficacy of EEG- to EMG-based control of an
orthosis. In one study exploring long-term use, a single
C4 spinal cord injury (SCI) patient used EEG-based
motor imagery measures to control both an FES and an
orthosis to restore hand function. After a year of train-
ing, his motor imagery accuracy remained at only 70%,
but he still found the device useful (Rohm et al., 2013).
For patients who cannot attain good accuracy with
motor imagery, SSVEP activity was validated for ortho-
sis control. Seven healthy volunteers without prior
training were told to focus on one of two flickering
LEDs placed on an orthosis to either open or close it (see
Fig. 26.6). Six volunteers attained good accuracy in an
asynchronous control paradigm, although the system
produced a high rate of false positives, and some par-
ticipants did not like the flickering lights (Ortner et al.,
2011). Related work addressed these problems with a
hybrid motor imagery–SSVEP system for orthosis con-
trol. This BCI system allowed subjects to use motor
imagery as a “brain switch” to switch the LEDs on or
off, thus enabling users to eliminate both problems.
Four of six healthy participants attained good accu-
racy (Pfurtscheller et al., 2010). Ramos-Murguialday
et al. (2012) found that proprioceptive feedback led to
improved motor imagery control of a robotic exoskel-
eton (compared to no feedback).
Lower Limb
BCIs to restore control of the lower limbs often use
EEG-based imagination of walking, as this provides a

V.  BRAIN, COMPUTER AND MACHINE INTERFACING

 Brain–Computer Interfaces to Enhance Function 365

FIGURE 26.7  An EEG-based system to control a lower-limb exoskeleton being used by a healthy volunteer (left) and a spinal cord injury
patient (right). The work with the patient requires safety rails and nearby staff because of the risk of falling. From Lopez-Larraz, E., Trincado-Alonso, F.,
Rajasekaran, V., Perez-Nombela, S., Del-Ama, A.J., Aranda, J., Minguez, J., Gil-Agudo, A., Montesano, L., August 3, 2016. Control of an ambulatory exo-
skeleton with a brain–machine interface for spinal cord injury gait rehabilitation. Front. Neurosci. 10, 359. http://dx.doi.org/10.3389/fnins.2016.00359.
eCollection 2016.

natural and intuitive mapping between thought and User State

action and is relatively easy to detect with trained
users. One patient with paraplegia resulting from
SCI learned to either relax or imagine walking while
EEG measures of these activities were used to drive a
lower-limb orthosis (Do et al., 2013). One study with
healthy volunteers validated BCIs to start or stop an
exoskeleton by thinking about gait initiation or termi-
nation (Hortal et al., 2016a,b). In a proof-of-concept
study, three healthy people used EEG-based measures
of gait initiation to direct an exoskeleton (Lopez-
Larraz et al., 2016) (see Fig. 26.7). Luu et al. (2016) clas-
sified different types of lower-limb movements (hip,
knee, and ankle) as people trained to control a virtual
avatar’s gait over 8 days. The users’ attention during
gait was also explored using different EEG frequency
bands, which could influence feedback during system
operation (Costa et al., 2016).
BRAIN–COMPUTER INTERFACES
TO ENHANCE FUNCTION
Introduction
The BCIs described so far focus on people with dis-
abilities who seek to replace or restore lost functions.
BCIs may eventually also benefit healthy persons by
enhancing the capabilities of the central nervous sys-
tem to enable people to perform tasks better, faster,
or more easily. BCIs to enhance function are generally
“passive,” meaning that the user does not actively
have to perform mental activities devoted to con-
trolling the BCI (such as imagining movements or
counting flashes or tones). Instead, passive systems
measure activity while the user is performing other
tasks. Thus, BCIs to enhance function generally aim to
provide additional capabilities without disturbing or
distracting the user.
A substantial body of work since 2007 has shown
that the EEG offers indicators of arousal, engage-
ment, workload, emotional valence, and other factors.
Accurate real-time detection of these indicators could
be used to modify a user’s ongoing interaction with a
computer or another external device. This direction has
been explored for decades, but is still largely confined
to the laboratory.
Jung et al. (1997) detected alpha and theta changes
over electrode sites Cz and Pz/Oz while sonar opera-
tors performed a simulated sonar detection task, and
could predict periods of poor task performance. Lin
et al. (2008) demonstrated a wireless four-channel EEG
system that could detect alertness lapses and sound
a warning. In a simulated driving environment with
11 healthy participants, Wang et al. (2014) discrimi-
nated effective from ineffective warning tones using
EEG spectral activity. The authors later extended this
approach (Huang et al., 2016), which might lead to
other mitigation measures for drivers or others who do
not notice warning stimuli. In these examples, the BCI
enhances natural function by reducing the risk of disas-
ter resulting from alertness lapses.
BCIs could also enhance users’ ongoing interaction
with software. This approach could reduce errors or
keep users engaged, such as by increasing difficulty if
users are bored (Millan et al., 2010; Gevins et al., 1995;
Zander and Jatzev, 2012; Fairclough, 2009; Nijholt et al.,
2009). For example, research from NASA explored
real-time “adaptive automation” using EEG-based
measures while people performed tasks from a multiat-
tribute test battery at different difficulty levels, with the
goal of adapting the user’s workload to reduce over-
load (Prinzel et al., 2000, 2002). The Defense Advanced
Research Projects Agency (DARPA)-funded Augmented
Cognition Program also aimed to learn more about sys-
tem operators’ mental states based on EEG and other

V.  BRAIN, COMPUTER AND MACHINE INTERFACING

366 26.  NONINVASIVE BRAIN–COMPUTER INTERFACES

FIGURE 26.8  The EEG-enhanced World of Warcraft system from Nijholt et al. (2009). The left shows how EEG-based measures of stress can
change the elf character into a bear. The right shows a person playing the game.

+
scalp projection
3 µV
H
500 msec

Average +3.9

µV

–0.1

END
OF
TRIAL 0.1s–0.2s

FIGURE 26.9  The left and middle show error-related activity from Schalk et al. (2000). The left image shows event-related potentials over site
Cz, and the middle image shows the scalp projections for 40 ms around the positive peak for each subject. The right shows error activity from
Parra et al. (2003) from 100 to 200 ms after feedback presentation. These images indicate prominent central activity 100–200 ms after feedback
presentation.

measures to adapt the system’s interaction with that user
(Schmorrow et al., 2006; St. John et al., 2004). Automatic
adaptation to the state of a user has been further explored
in aviation (Brookings et al., 1996; Sterman and Mann,
1995). Kirchner et al. (2016) presented a system that
could adapt ongoing interaction with a P300 BCI system
based on EEG measures of task load.
BCIs have also been used to enhance games and cre-
ative applications. In Nijholt et al. (2009), healthy people
played World of Warcraft through conventional means
(keyboard and mouse). The system changed the player’s
game character between an elf and a bear based on EEG-
based evaluation of stress (see Fig. 26.8). Reissland and
Zander (2009) and Zander and Jatzev (2012) described
EEG-based systems to detect bluffing in a game environ-
ment and perceived loss of control. Makeig et al. (2011)
described a BCI that can produce music in real time
based on EEG measures of user emotion.
Error Detection
People inevitably make mistakes while using BCIs or
other technologies. Errors may go undetected or uncor-
rected, or users need to perform some corrective action
that requires time and attention. EEG measures can
reveal error potentials, such as event-related negativity
(ERN), if people believe they just made a mistake. Real-
time detection of ERN or similar EEG features could
be used to correct errors or other goals (Hoffmann and
Falkenstein, 2012; Wessel, 2012). Schalk et al. (2000)
recorded activity from 64 EEG channels while four sub-
jects used mu and beta activity to direct a cursor to the
word “yes” or “no,” and established the difference in
EEG activity recorded during the trials in which the
subjects did or did not succeed in controlling the cursor
to the correct target. One hundred eighty milliseconds
after subjects received feedback indicating an errone-
ous selection, they exhibited a strong positive peak,
followed by a negative peak, which was most promi-
nent over Cz (Fig. 26.9, left). The authors estimated
that, if error activity were used for error correction
within their yes/no BCI system, the system’s informa-
tion transfer rate would improve by 0% to 21% across
the four subjects. A different group also explored error
activity recorded from 64 EEG channels and implica-
tions for online error correction (Parra et al., 2003).
Seven healthy subjects performed a button-press task
in a visual discrimination paradigm. ERPs also showed

V.  BRAIN, COMPUTER AND MACHINE INTERFACING

 Brain–Computer Interfaces to Enhance Function
Composition
–1 figure/ground –1
scene
0 0
1 1
µV
µV
2 2
3 3
0 50 100 150 200 250 300
Time (msec)
FIGURE 26.10  Event-related potential activity elicited by images that varied in composition, content, and emotion. From Loew, A., Bradley,
M.M., Lang, P.J., 2013. Perceptual processing of natural scenes at rapid rates: effects of complexity, content, and emotional arousal. Cogn. Affect. Behav.
Neurosci. 13 (4), 860–868. Available from: http://dx.doi.org/10.3758/s13415-013-0179-1.
prominent frontocentral activity from 100 to 200 ms
after erroneous responses only (Fig. 26.9, right), which
could reduce errors by −6% to 49% across the seven
subjects.
The P300 can also indicate that the user received
feedback that was unexpected or erroneous (Polich,
2004), which could be used in adaptive BCIs (Bayliss
et al., 2004). Tong et al. (2016) used multiple features for
error detection while healthy people used a P300 BCI.
In addition to modifying users’ interactions with BCI-
based communication systems, real-time error moni-
toring could also lead to adaptations with conventional
software, such as real-time error correction when a typ-
ist makes a mistake using a word processor (Allison,
2009).
Sleep
Millions of people in the United States alone have
serious trouble sleeping, including falling asleep,
remaining asleep, and having nightmares. BCIs may be
used to enhance sleep in different ways. Sleep stages,
including sleep onset, could be identified and classi-
fied via EEG, EMG, electrooculogram (EOG), heart
rate (HR), and other signals (Beniczky et al., 2013;
Goldstein and Chervin, 2016; Lin et al., 2008; Silverman
et al., 1968). These signals have been used to modulate
a user’s environment, such as relaxing music to foster
sleep onset, or influence the timing of an alarm clock.
Image Recognition
One approach to BCI could enhance the natural abil-
ity to convey the recognition of specific images. People
employed in image recognition, such as in security,
research, or product review, often must view many
thousands of images with the goal of detecting one or
more “target” images, then pressing a button or taking
other action to convey this target detection to a com-
puter. BCIs may improve this process by automatically
determining when the user detects a target image, elim-
inating the need to respond and allowing faster image
presentation. In the rapid serial visualization paradigm
V.  BRAIN, COMPUTER AND MACHINE INTERFACING
367
Content Emotion
people –1 emotional
no people neutral
0
1
µV
2
3
0 50 100 150 200 250 300 0 50 100 150 200 250 300
Time (msec) Time (msec)
(RSVP), a sequence of single images is presented very
quickly while EEG activity is used to distinguish target
from nontarget images. Gerson et al. (2005) showed that
nine subjects who had to press a button after each tar-
get stimulus exhibited frontal EEG activity that devel-
oped 200 ms before the button press. Pohlmeyer et al.
(2011) extended this direction with a real-time system
to reorder an image database. EEG measures were com-
bined with a semisupervised artificial visual system to
estimate users’ interest in each image during RSVP and
change its position in the image sequence accordingly.
In Loew et al. (2013), 27 participants observed 128 color
images that varied in composition (figure/ground or
scene), content (people or none), and valence (arous-
ing or neutral). The images were presented serially for
330 ms each with no delay between images while 128
EEG channels were recorded. Fig. 26.10 shows how
averaged ERPs differ across these three categories.
Results could be used to order stimuli based on richer
information about each image, although extending
results to single-trial applications may be challenging.
Several articles have addressed single-trial RSVP algo-
rithms and performance, as this application is not well
suited to averaged data (Fuhrmann Alpert et al., 2014;
Manor and Geva, 2015; Lin et al., 2015; Bigdely-Shamlo
et al., 2008; Marathe et al., 2016).
Neuromarketing
The years since 2007 have seen considerable work on
neuromarketing, in which EEG, fMRI, magnetoenceph-
alography, and other physiological signals are used to
help marketing researchers learn more about people’s
decisions and reactions relating to products and services.
This type of research may not fall under the conventional
definition of a BCI (because it does not provide real-time
feedback to the user). At the same time, this approach
could adapt to users and/or modify the ongoing inter-
action with users, such as by presenting additional ads
that are similar to an ad that a user likes, to better iden-
tify which components of that ad are appealing. In a
typical paradigm, healthy participants view ads, movie
trailers, or other short clips while activity is monitored,
368 26.  NONINVASIVE BRAIN–COMPUTER INTERFACES
possibly after a brief period of adapting classifica-
tion parameters to each user. BCIs may provide more
detailed information than conventional methods such
as questionnaires and focus groups, and do not require
interrupting people, because they simply rely on signals
produced by the user during his or her natural inter-
action. For example, subconscious aspects of whether
someone likes or dislikes a car stimulus were evaluated
with ERPs (Wriessnegger et al., 2015). Several studies
from one group used EEG, sometimes in combination
with galvanic skin responses and HR measurements, to
assess memorization and attention when people viewed
advertisements (Astolfi et al., 2008; Vecchiato et al., 2011,
2012). Other work has evaluated EEG-based measures
associated with lighting and color in a marketing con-
text (Bercik et al., 2016).
BRAIN–COMPUTER INTERFACES TO
IMPROVE FUNCTION
Introduction
This section addresses BCIs that are designed to pro-
duce a lasting, perhaps permanent, improvement in ner-
vous system function to alleviate a particular condition.
Thus, BCIs to improve function differ from the other BCI
approaches, which focus primarily on providing ben-
efits during BCI use. For example, BCIs to restore motor
function may involve the same hardware and similar
software as BCIs to improve motor function, but only the
latter category focuses on training protocols that provide
lasting beneficial changes to the nervous system, and
thereby complement rehabilitation therapy.
Successful development of BCIs to improve function
would address an enormous problem: in addition to the
personal impact on the lives of patients and those who
care for them, movement and other disabilities can entail
many other costs. Patients may have limited or no ability
to work, create, or care for themselves or others. Assistive
technologies, managed care facilities, rehabilitation sys-
tems and therapies, and other ancillary costs are tremen-
dous (Demaerschalk et al., 2010; Howard-Wilsher et al.,
2016). Therapy may require numerous sessions, spread
across weeks or months, which can require being driven
to a hospital or rehabilitation center. Thus, new devices,
methods, or concepts to improve the efficacy and effec-
tiveness of rehabilitation therapy are sorely needed.
Improvements to Motor Function
Millions of people in the United States alone have dif-
ficulty moving because of disease or injury affecting the
brain and/or spinal cord. Major causes include stroke,
traumatic brain injury, tumors, and SCI. Conventional
V.  BRAIN, COMPUTER AND MACHINE INTERFACING
FIGURE 26.11  This image shows how EEG activity, processed
through a laptop, could drive conventional stroke feedback mecha-
nisms such as a functional electrical stimulator (FES) or an avatar.
From Sabathiel, N., Irimia, D.C., Allison, B.Z., Guger, C., Edlinger, G., 2016.
Paired associative stimulation with brain–computer interfaces: a new para-
digm for stroke rehabilitation. In: International Conference on Augmented
Cognition. Springer, pp. 261–272.
approaches to improve motor control include therapy,
several robotic assistive devices, functional electrical
stimulation, virtual reality, and other means.
Since 2007, many researchers have presented real-
time brain imaging, sometimes with direct electrical or
magnetic brain stimulation, as a complement to existing
movement therapy tools and methods. The expectation
is that real-time measures of motor imagery could influ-
ence devices that present feedback (Fig. 26.11). Thus,
feedback such as FES activation, avatar movement, brain
stimulation, and/or rewarding sounds or images could
occur only when the patient imagines the correct move-
ment, perhaps influenced further by movement inten-
sity or other parameters.
This combination of approaches is based on the prin-
ciple that improving the neural communication between
two relevant groups of neurons relies on the coordinated
activation between them, as per Hebbian learning and
long-term potentiation. The goal of rehabilitation ther-
apy is to strengthen the pathways connecting neurons in
the cortex (such as neurons responsible for grasping) to
neurons that directly trigger corresponding muscle activ-
ity. BCIs could add several contributions to this process.
Real-time measures of movement imagery in the cortex
can be used to automatically influence different types
of feedback while providing helpful information to a
therapist, including compliance monitoring. Electrical or
magnetic devices can stimulate relevant cortical neurons
to further increase activation when downstream neurons
are active. Other neuroimaging advances could lead to
more detailed and accurate diagnoses and treatments.
Beyond improving movement, BCIs can produce other
persistent changes to treat different patient groups.
 Brain–Computer Interfaces to Improve Function 369

(A) Training strategy 1 (B) Training strategy 2

Signal features Signal features Device that assists

movement

Impaired Impaired
efferent efferent
signal signal
Impaired Practice of
CNS volitional CNS close-to-normal
movement movement

ly
ive
Br

ss
ai

re
n
sig

og

l
pr

na
na
m

ls

tio
ar
More normal afferent signal

or
Direct training of

ar

nc
e

ls
e

fu
cortical signal

fu

na
pr
n

e
og

sig
ct

or
io

re

m
ain
na

ss
l

ive

Br
ly
(C) Goal Normal
Restored volitional
CNS movement
Normal
efferent
signal

More normal afferent signal

FIGURE 26.12  In (A), users directly train the central nervous system (CNS) to produce healthier signals, thereby leading to improved CNS
function (C). In (B), users instead attain this goal by practicing movements using a brain–computer interface assisted by a device, improving
sensory feedback and thus improving CNS function. From Daly, J.J., Wolpaw, J.R., 2008. Brain–computer interfaces in neurological rehabilitation. Lancet
Neurol. 7 (11), 103243.

Pfurtscheller and Neuper (2006) presented future
directions in BCI research, with prominent attention
to improving functional recovery from stroke. They
noted that detecting motor imagery is essential in effec-
tive rehabilitation, and addressed related issues that
remain topical, such as virtual reality training, BCIs
that manage real-time feedback based on motor imag-
ery, first-person/kinesthetic motor imagery, and adapt-
ing parameters to each patient. Birbaumer and Cohen
(2007) suggested the use of transcranial magnetic stim-
ulation (TMS) or transcranial direct current stimula-
tion (TDCS) to strengthen Hebbian learning and thus
improve movement.
Daly and Wolpaw (2008) presented two BCI
approaches to improve function. In the first approach,
users train to produce different patterns of brain activ-
ity through feedback. The second approach relies on
repeated use of BCI to control a movement device to
encourage activity-dependent plasticity through sensory
feedback (Fig. 26.12).
Other early work suggested TMS as a tool to accel-
erate rehabilitation of cognitive, motor, and lan-
guage functions (Rossi and Rossini, 2004; Siebner
et al., 1999). The former article showed that TMS
could help patients with dystonia such as writer’s
cramp, although improvements were only transient.
Other early work with 15 chronic hemiparetic stroke
patients showed that repetitive (r) TMS (unlike sham
stimulation) improved the learning of a finger move-
ment sequence, and produced significantly larger
muscle evoked potentials (MEPs) (Kim et al., 2006);
see also Chang et al. (2015).
Some authors have continued to explore TMS for
motor rehabilitation. For example, Buetefisch et al. (2015)
showed that rTMS of 0.1 Hz, unlike other frequencies or
subthreshold stimulation, led to significant improve-
ments in acceleration and MEP size. Du et al. (2016)
found that TMS stimulation in first-time stroke patients
was more effective at 1 Hz than at 3 Hz, both of which
were more effective than sham. These and other stud-
ies using TMS to improve motor function support the
notion that simultaneous activation of both cortical and
associated downstream neurons increases motor learn-
ing. Furthermore, additional work to explore optimal
stimulation frequencies and other parameters could lead
to greater improvement.
Mrachacz-Kersting et al. (2011) found that MRCPs can
be used to trigger peripheral stimulation that improves
excitability. Mrachacz-Kersting et al. (2016) used MRCPs
to detect movement and thereby control feedback in
a rehabilitation paradigm, and described significant
improvements in functional and neuroimaging mea-
sures with only three training sessions. The authors
noted that MRCPs can provide more precise synchrony
between movement imagery and feedback, thus improv-
ing Hebbian learning.

V.  BRAIN, COMPUTER AND MACHINE INTERFACING

370 26.  NONINVASIVE BRAIN–COMPUTER INTERFACES
Another ongoing problem that is being addressed is
our lack of a thorough understanding of how the brain
relearns movement and other tasks, especially in the
context of BCI-mediated rehabilitation. Straudi et al.
(2016) used TDCS with a robotic system to treat persons
with different types of strokes. The treatment was most
effective on patients with chronic and subcortical stroke.
Carey et al. (2005) and Fallani et al. (2013) also found that
cortical changes resulting from rehabilitative training
varied with stroke location or movement impairment.
These and other results may help guide physicians, ther-
apists, and BCI practitioners in deciding the best com-
ponents and parameters of BCI for different patients.
Young et al. (2014) used fMRI and several behavioral
assessments to compare two groups of chronic stroke
patients (mean 13.13 months after stroke onset) with
persistent trouble with upper-limb movement. Eight of
these patients participated in BCI therapy, while six had
no therapy. Only the BCI group showed fMRI changes
and improvements in behavioral performance consistent
with improved movement.
Most research has focused on upper-limb rehabilita-
tion, because this is a common need of stroke patients and
requires less extensive therapy systems. Rehabilitation
of lower-limb movement disabilities, including gait,
can also entail an exoskeleton, EMG and FES devices
for the legs and hips, and significant safety measures
to prevent falling. Despite these challenges, systems for
BCI-based gait rehabilitation have been explored (Pons
and Torricelli, 2014; Lopez-Larraz et al., 2016; Belda-
Lois et al., 2011). Jiang et al. (2015) found that MRCPs
could help predict gait initiation in healthy subjects, as
can ERD (Hortal et al., 2016b), which both groups noted
could be beneficial in gait rehabilitation. MRCPs can also
detect foot movements in other work focused on reha-
bilitation (Aliakbaryhosseinabadi et al., 2014).
In addition to work with writer’s cramp, BCIs could
be useful beyond helping stroke patients regain move-
ment. Stroke patients also have trouble with spastic
tremors, which BCIs could address (Pons and Torricelli,
2014). Persons with other movement disabilities might
also benefit, such as those with spinal injuries, trau-
matic brain injury, Parkinson disease, or cerebral palsy
(Birbaumer and Cohen, 2007; Lopez-Larraz et al., 2016;
Pons and Torricelli, 2014; Rossi and Rossini, 2004).
The increase in interest in using BCIs to improve
motor function is apparent from an abundance of review
articles. Several publications have summarized and
commented upon the use of EEG-based BCIs for per-
sistent functional improvement (Chaudhary et al., 2015;
Soekadar et al., 2015; Kubis, 2016; McCrimmon et al.,
2016; Paggiaro et al., 2016; Remsik et al., 2016; Riccio
et al., 2016; Ushiba and Soekadar, 2016). These reviews
generally find this direction to be promising, though
more extensive clinical validation is clearly needed.
V.  BRAIN, COMPUTER AND MACHINE INTERFACING
Improvements to Other Functions
BCIs, often called bio- and neurofeedback in this
domain, have been extensively explored and applied to
improve the central nervous system by improving emo-
tional and/or psychiatric factors (Marzbani et al., 2016).
Neurofeedback has been used to facilitate relaxation
in both healthy people and persons with stress-related
conditions for decades, with increased recent interest in
posttraumatic stress disorder (Gapen et al., 2016). In a
typical paradigm, users try to modulate activity in par-
ticular EEG frequency bands over different regions, such
as alpha and beta. Both healthy and disabled users, as
well as elderly persons, have also long used neurofeed-
back with the goal of improving memory (Miralles et al.,
2015; Gomez-Pilar et al., 2016; Kober et al., 2015). Related
efforts involve neurofeedback to train vigilance, distract-
ibility, and other attentional factors. While interest has
grown in such BCIs to treat patients with attention defi-
cit hyperactivity disorder or other conditions, healthy
patients have also sought to improve their attention
(Gomez-Pilar et al., 2016; Cortese et al., 2016; Ordikhani-
Seyedlar et al., 2016; Bluschke et al., 2016).
Several other patient groups have been explored.
An fMRI-based BCI system was used to train psycho-
paths to learn fear conditioning (Birbaumer and Cohen,
2007; Sitaram et al., 2014). Patients with criminal psy-
chopathy were trained to upregulate blood oxygen
level-dependent (BOLD) activity in the left anterior
insula, part of the brain’s fear circuitry. FMRI activation
showed increased BOLD activity, suggesting that the
psychopaths learned fear, although behavioral results
were not reported. This approach could be extended
to help persons with obsessive–compulsive disorder or
other groups (Buyukturkoglu et al., 2015). Interestingly,
Birbaumer and colleagues published earlier work show-
ing that patients with epilepsy could reduce seizures by
training SCP activity (Rockstroh et al., 1993), although
this approach never became part of clinical practice.
BCIs and related therapies to treat addiction could be
applied to anorexia and other eating disorders (Lackner
et al., 2016). Other BCIs aim to reduce the symptoms of
autism (Kouijzer et al., 2013; Friedrich et al., 2014, 2015;
Pineda et al., 2014) by improving mirror neuron system
function, which appears to be impaired in persons with
autism (Oberman et al., 2005). For example, in the “Social
Mirroring” game, children with autism receive positive
or negative feedback when they produce certain physi-
ological signals while interacting with a virtual character
(Friedrich et al., 2014).
An important issue in this area is the ability to per-
form BCI rehabilitation in home settings (Sabathiel
et al., 2016; Mastropietro et al., 2016; Miralles et al.,
2015). Traveling to a hospital, therapy center, or other
remote location for dozens of therapy sessions can be
 Summary of the Current State of Noninvasive Brain–Computer Interfaces
especially burdensome for patients who cannot drive
or have special transportation needs, such as a van
designed for persons with motor disabilities. Home-
based BCI training might occur in tandem with remote
therapy, thus reducing cost while still providing some
contact with medical professionals. A caregiver in the
patient’s home could be trained to mount an electrode
cap or other sensors, prepare an FES system, launch
software, review task instructions with the patient,
or help in other ways. Therapists might also conduct
“house call” rehabilitation sessions to provide these
and more advanced services.
BCIs to improve function are probably the most ambi-
tious of the five approaches. They could render other
types of BCIs unnecessary, heal a wide variety of con-
ditions, and appeal to healthy users for many reasons.
At the same time, side effects could be harmful, and
thus, overall societal impact could be complex. This
potentially broad impact means that adequate clinical
validation and ethical considerations are particularly
important.
SUMMARY OF THE CURRENT STATE
OF NONINVASIVE BRAIN–COMPUTER
INTERFACES
Scientific and Technical Basis
In accord with many other studies over the past
decades, the studies described in this chapter have pro-
vided ample evidence that noninvasive brain signal
modalities can be used to give information about the
motoric, sensory, cognitive, or affective state of a user,
and that such information can be decoded from the brain
in real time, i.e., as the user engages in a particular task.
This largely laboratory-based body of evidence provides
the scientific basis for systems that can replace, restore,
enhance, supplement, or improve human functions. The
growing miniaturization of sensor, affector, and comput-
ing technologies, as well as the great increase in perva-
siveness and affordability of computing power, provides
the technical basis for devices that can be small and rea-
sonably affordable.
Translating Brain–Computer Interfaces From
Scientific Endeavors Into Clinically and
Commercially Successful Technologies
BCI technologies have a strong scientific and technical
basis, receive modest and sustained support from fund-
ing agencies, and undeniably fascinate scientists, the
media, and the public. However, only very few BCI tech-
nologies have been translated into new clinically and
commercially successful diagnostic or treatment options.
V.  BRAIN, COMPUTER AND MACHINE INTERFACING
371
This critical issue in “moving beyond demonstrations”
has been recognized for many years—indeed, it was the
theme for the 2002 BCI Meeting in Rensselaerville, New
York. The numerous discussions in scientific articles or
BCI workshops on this topic since then have usually
centered on the necessity for further technical improve-
ments (e.g., in bit rate, practicality of EEG headsets, and
calibration or other signal processing techniques). The
implicit notion is that improvement in one or most of
those technical factors will result in commercial adop-
tion of BCI technologies. While technical improvements
of different kinds will always be welcome or may even
be critical, it is important to recognize that perhaps the
most important requirement for any successful new
technology is that its benefit exceeds its cost.
An assessment of benefit needs to consider not only
the realistic benefit of the BCI technology relative to
existing technologies, but also the number of individu-
als that are interested in using it. For example, a BCI-
based communication device may support brain-based
spelling at a rate of a few characters per minute. This
capacity to spell using the brain may be inspiring and
statistically well above chance, but it may still not pro-
vide a clinically relevant improvement over existing
augmentative communication devices or may provide
such improvement to only very few people. Likewise,
the assessment of cost needs to consider not only the
variable cost of the BCI device, but also the risks and
fixed cost of regulatory approvals, intellectual property
strategies and other legal activities, development of new
sales/marketing channels, product development, sup-
port, and the complexities associated with the change
to the BCI technologies from the traditional technolo-
gies that they replace (Allison, 2009; Millan et al., 2010;
Miralles et al., 2015). If the aggregated benefit does not
exceed the aggregated cost, commercialization will be
unlikely to succeed.
Finally, it is important to recognize that successful
commercialization in the medical sector requires suc-
cessful navigation and resolution of complex reimburse-
ment, regulatory, and legal issues. The knowledge and
people required for successful commercialization, as
well as the medical, corporate, and legal arrangements
necessary to support this process, have existed for
decades for traditional medical devices and pharmaceu-
ticals. This critical infrastructure is in a very early stage
for BCI systems, and requires substantial cost and effort
to set up. Hiring and training appropriate staff, develop-
ing procedures to follow different requirements, design-
ing and manufacturing products accordingly, testing for
compliance, developing proposals to certifying agencies
and responding to their requests, validation with tar-
get users (especially clinical trials), and ethical approv-
als create substantial but necessary challenges when
extending BCIs from the research into the commercial
372 26.  NONINVASIVE BRAIN–COMPUTER INTERFACES
domain. Furthermore, these and other issues can vary
substantially in different regions and with different
patient groups.
Commercialization Potential of Various
Noninvasive Brain–Computer Interface
Technologies
Noninvasive BCIs to replace, restore, or enhance func-
tions, such as those that enable spelling, restore move-
ments, or warn a sleepy driver, have been intensely
studied for some time. The principal challenge facing
these systems is that they need to derive an assessment
of the user’s brain state very rapidly and accurately.
Unfortunately, all current noninvasive sensors can only
produce either unreliable measurements quickly or reli-
able measurements very slowly. Given this principal
limitation, the number of users that can benefit from
these types of BCI technologies using current noninva-
sive sensor technologies is small, and/or those users
often already have access to non-BCI alternatives. For
this reason, successful commercialization of these types
of BCIs will probably require the development of as-
yet unknown sensor technologies that do not face these
issues.
Noninvasive BCIs to improve functions, such as those
that rehabilitate people with chronic stroke or incom-
plete SCI, have attracted increasing interest over the past
several years. They induce beneficial plasticity in spe-
cific central nervous system circuits and often have more
relaxed requirements regarding the rapidity or accuracy
of measurements. The number of users that can benefit
from those BCI technologies is potentially very large,
and those users often have no viable alternative. Hence,
with additional development and validation, and with
development of proper regulatory, reimbursement, and
commercialization strategies, these types of BCIs appear
to have a potential trajectory toward successful transla-
tion and commercialization. Indeed, several companies
have begun to introduce products that rehabilitate func-
tion in chronic stroke survivors, including IpsiHand
by Neurolutions (www.neurolutions.org), NBetter by
NeuroStyle (www.neuro-style.com), and recoveriX by
g.tec (www.recoverix.at).
Conclusions
In conclusion, the information that can be extracted
from the brain provides many opportunities to increase
individual or societal performance. Full realization of
these possibilities for noninvasive BCIs will probably
require the development of completely novel sensors
that can support rapid and reliable measurements of
brain function.
V.  BRAIN, COMPUTER AND MACHINE INTERFACING
Acknowledgments
This work was supported by the NIH (EB00856, EB006356, and
EB018783), the US Army Research Office (W911NF-08-1-0216,
W911NF-12-1-0109, W911NF-14-1-0440), and Fondazione Neurone.
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