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13/03/2023, 19:26 Electroencephalography and Magnetoencephalography

Cambridge Fundamentals of Neuroscience in Psychology: Introduction to Human Neuroimaging


ISBN 9781316847916
Part III Electrophysiological Neuroimaging
Chapter 10 Electroencephalography and Magnetoencephalography

Chapter 10 Electroencephalography and


Magnetoencephalography

Learning Objectives

Explaining what each electrophysiological method measures

Following methods of signal acquisition in a research paper

Explaining the pros and cons of the electrophysiological methods

I do not remember having ever received … a


more dreadful shock than that which I
experienced by imprudently placing both my feet
on a gymnotus just taken out of the water. I was
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affected during the rest of the day with a violent


pain in the knees, and in almost every joint. To
be aware of the difference that exists between the
sensation produced by the Voltaic battery and an
electric fish, the latter should be touched when
they are in a state of extreme weakness.

Alexander von Humboldt, 1800

From Jaguars and Electric Eels, selected translation of


Voyage aux régions équinoxiales du nouveau continent
by J. Wilson (2007). (The original text is available at
http://dx.doi.org/10.3931/e-rara-24320.)

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Friedrich Wilhelm Heinrich Alexander von Humboldt was a German (Prussian, to be


precise) naturalist. His explorations to Central and South America were published as a
series of books that were widely read in Europe and beyond, making him a celebrity.
When Humboldt made the voyage, he was 31 years old and full of energy and curiosity.
In the regions along the Orinoco River, local guides told him about the gymnotus, an
electric eel that could grow to 2 m long. According to the guides, the eels could para‐
lyze a horse that had come to a pond to drink water. Humbolt wanted to experience the
discharge despite repeated warnings from the guides. He most likely did not exaggerate
his experience, because the giant eel’s discharge can reach 600 volts (V) (Catania, 2016).

Compared with the impressive power generation capacity of the eels, what our brain
generates – on the order of microvolts (μV, a millionth of a volt) – is nothing. On the
one hand, it is a blessing that our ongoing brain activity does not threaten others (elec‐
trically). On the other hand, however, it is a challenge to measure such weak signals.
For example, a fluorescent ceiling lamp can easily emit electric activity that is 100 times
higher than the brain activity. Such non-brain activity, noise, needs to be prevented or
reduced while recording. In addition, high-fidelity sensors and amplifiers are necessary.
In this chapter, two major techniques that measure the weak activity, electroen‐
cephalography (EEG) and magnetoencephalography (MEG), are introduced.

10.1 Electroencephalography (EEG)


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Electroencephalography (EEG) measures the electric signal produced by cerebral activ‐


ity. As we learned in Chapter 9, the most significant contributor to the signal is the
postsynaptic potential in apical dendrites of cortical pyramidal neurons. Throughout
the long dendrite that runs through multiple cortical layers, hundreds of thousands of
synapses – some are excitatory, and others are inhibitory – are formed. Excitatory and
inhibitory postsynaptic potentials generate a complex mixture of postsynaptic currents.
The current primarily runs in the apical dendrite (primary current), and also in brain
tissue, cerebrospinal fluid (CSF), skull, and the scalp (return current). The conductivity
of the biological tissue is not homogenous (e.g., brain tissue and CFS conduct the cur‐
rent better than the skull does). Thus, the current spreads along the skull, mixed with
currents from other sources. As a result, a complex electric field is formed spanning the
distance from the brain to the scalp. The electric signal that we obtain from a scalp elec‐
trode, therefore, reflects the activity of many different sources.

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To record the signal, we need to establish an electric circuit from the scalp to a record‐
ing device. Since most of us do not have a cable jack on the head, we use a special cable,
one end of which is an electrode: The electrode is placed on the scalp using a paste, and
the other end is connected to the recording device. How to induce a current from the
scalp could be compared with pouring water from a water tank (Fig. 10.1). The amount
of water from the tap depends on how high the water level is and how fully the tap is
opened. The voltage at the scalp is very low, but we could find a yet lower point, such as
the ground. The recorder is grounded. Thus, the current flows from scalp to the
ground. More current runs when resistance of the circuit is lower. The highest resis‐
tance occurs at the gap between the electrode and the scalp. To keep the resistance low,
the gap is filled with a conductive substance, gel or paste – the tap is opened. The
recorder is placed between the scalp electrode and the ground to convert the induced
current to voltage, just like putting a hand in the flow of water to sense how much water
is running and how high the water level is.

Note that the electrode does not apply but receives the current. The EEG technique
does not inject current to the brain. A current is applied to the brain with brain stimu‐
lation techniques: transcranial direct current stimulation (tDCS) and transcranial alter‐
nating current stimulation (tACS). These brain stimulation techniques also use elec‐
trodes that apply current to the brain. Some also receive the signal (cf. Chapter 14).
Both EEG and transcranial current stimulation are based on volume conduction, but
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electrodes with each method have different functions.

10.1.1 EEG Electrodes

Electroencephalography electrodes are placed on the scalp to register current due to


brain activity. The electrodes come in a variety of shapes and sizes. Disk or button elec‐
trodes (~5 mm of diameter) are typical, but other shapes, such as pin, comb, and grid,
are also used (Fig. 10.2). Bandages and/or glue are used to attach individual electrodes.
To attach a large number of electrodes efficiently, an electrode cap, to which multiple
electrodes are set, is often used. Materials such as silver (chemical symbol Ag), tin (Sn),
and sintered silver and silver chloride (Ag/AgCl) are used for the electrode. These ma‐
terials are conductive and safe to attach to the scalp. The signal quality differs slightly
depending on the material used (Tallgren et al., 2005). Thus, materials are chosen based
on the purpose of the recording. For example, evoked brain responses to external stim‐

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ulation often contain slow activity. The Ag/AgCl electrodes provide a stable slow signal;
thus, they are often preferred in recordings of evoked responses.

Figure 10.2 EEG electrodes.

The small gap between the scalp and the EEG electrodes is filled with a conductive sub‐
stance: paste, gel, or saline that contains ions, such as chlorite ions (Cl-). The filler is
used to decrease electric resistance, known as contact impedance, between the scalp
and the electrode. As the contact impedance decreases, the current from the scalp to
the electrode increases. The impedance affects high- more so than low-frequency activ‐
ity (Kappenman and Luck, 2010). To have a good signal-to-noise ratio (SNR or S/N)
for a wide frequency band, the impedance needs to be kept as low as possible – less
than 5 kΩ has been recommended (Picton et al. 2000). Commercial EEG recording
systems offer an impedance check function: The contact impedance is measured by
running a weak alternating current of 10 Hz to the electrodes. The test current is too
weak to be noticeable to test participants and is kept within the standard for the electri‐
cal safety of medical devices (ICNIRP, 2010).

Ideally, the locations and the number of electrodes should be determined based on the
aim of each study. For example, when we are interested in the brain response to a visual
stimulus, we would certainly place electrodes at the back of the head, near visual cor‐
tices that are located in the posterior part of the brain. However, when we are interested
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in EEG during, say, mind wandering, it is not so straightforward to decide the electrode
placement. We could place multiple electrodes covering the head to sample EEG from
the whole head. How many electrodes do we need in this situation? Is it okay to use the
same number for everyone regardless of head size? During the early years of research,
these parameters were decided in each study, researcher, and/or research group. As a
consequence, a comparison of results of several studies was, at the very least, cumber‐
some. In 1947, at the International Congress of Electroencephalography and Clinical
Neurophysiology in London, an initiative to establish the international standard for
EEG electrode placement was begun. Eleven years later, combining several major elec‐
trode placement systems, the international 10–20 system was established (Jasper,
1958).

The international 10–20 system specifies electrode locations based on a grid drawn on
the scalp. The grid lines segment of the scalp is based on 10% and 20% points on the
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perimeter of the head (see Box 10.1). The name “10–20 system” stands for this ratio of
divisions. Electrodes are placed on the grid points. The locations are referred to with
abbreviations: frontal-polar (Fp), frontal (F), central (C), parietal (P), occipital (O), and
temporal (T). Locations on the left hemisphere are given an odd number, while those
on the right hemisphere are given an even number, e.g., F3 and F4. Locations on the
midsagittal line are marked with “z” for Zentrum, e.g., Fz. The system specifies 19 elec‐
trode locations that cover the whole head (Fig. 10.3). The locations are roughly equally
spaced, suitable for monitoring activity from the whole brain. The locations are deter‐
mined by the ratio; thus, the same number of electrodes is used regardless of head size,
which made inter-individual comparison easy. The system also specifies six possible
reference electrode locations (cf. reference and ground electrodes).
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Box 10.1 The International 10–20 System in Five Steps

Step 1

The electrode locations are decided based on four skeletal landmarks: nasion, in‐
ion, and left and right preauricular points (Box Figure 10.1). The frontal nasal
bone suture crosses the midsagittal line at the nasion. On the scalp, it corresponds
to the lowest point of the nose ridge. The point at which the external occipital pro‐
tuberance crosses the midsagittal line is the inion. It corresponds to the point just
below the highest point on the back of the head on the midsagittal line. The preau‐
ricular point is above the intertragal notch, roughly in front of the earhole. Most of
the brain, the neocortex in particular, is located above these landmarks. Now, draw
an arc from nasion to inion via the vertex of the head, and another from left and
right preauricular points via the vertex. The front-back and left-right arcs cross at
their midpoints. The first electrode is placed at the crossing point. The location is
called the central-midline and noted as Cz (i.e., Central-Zentrum).

Step 2

Divide the nasion-Cz-inion arc in 10%, 20%, 20%, 20%, 20%, and 10% segments of
the arc length. This gives us five dividing points between nasion and inion. The first
point, the 10% point, from the nasion is called the frontal-polar-midline (Fpz). The
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second point, the 30% point from the nasion is the frontal-midline (Fz). The third
point is the 50% point from nasion or inion, i.e., Cz. The fourth point, the 70%
point, is the parietal-midline (Pz). The fifth point, the 90% point, is the occipital-
midline (Oz), which is 10% above the inion. All electrodes on the midsagittal line
are indexed with “z.”

Step 3

Likewise, divide the left preauricular–Cz–right preauricular arc in 10%, 20%, 20%,
20%, 20%, and 10% segments. This gives us five electrode locations: From left to
right, the five locations are referred to as left temporal (T3), left central (C3), Cz,
right central (C4), and right temporal (T4), respectively. Note that electrodes on the
left hemisphere are indexed with odd numbers, while those on the right hemi‐
sphere are indexed with even numbers.

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Step 4

Draw a perimeter connecting four 10% points, Fpz, T3, Oz, and T4. Divide the left
arc (Fpz-T3-Oz) in 10%, 20%, 20%, 20%, 20%, and 10% segments. The electrodes
are placed on the sedimentation points: The electrode locations are called, from
front to back, Fp1, F7, T3, T5, and O1, respectively. Likewise, the right arc (Fpz-T4-
Oz) is divided in 10% and 20% segments. This gives electrode locations Fp2, F8, T4,
T6, and O2.

Step 5

The last four locations are decided by adjacent electrode locations. Draw a short arc
between F7 and Fz and another between Fp1 and C3. The arcs cross at their mid‐
points. Location F3 is placed at the crossing point. Location F4 is defined in the
same manner using F8, Fz, Fp2, and C4. Likewise, P3 is defined by T5, Pz, O1, and
C3. Location P4 is defined by T6, Pz, O2, and C4.

In the 10–20 system, two out of the 21 scalp locations, Fpz and Oz, are not used in
order to avoid uneven electrode density, e.g., O1, Oz, and O2 electrodes would be‐
come closer than C3, Cz, and C4. Thus, the total number of electrodes is 19.
Location Fpz is sometimes used as a ground location. In higher density systems,
e.g., the 10–10 system, Fpz and Oz are included as valid scalp electrode locations.
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Based on the 10–20 system, a few more systems were developed. The international 10–
10 system (AES, 1994) divides the arcs in 10% segments. Thus, more electrode loca‐
tions, more specifically, 73 scalp locations, are specified. Four rows of electrodes are
added to the electrodes in the 10–20 system: anterior-frontal (AF), fronto-central (FC),
fronto-temporal (FT), centro-parietal (CP), temporo-parietal (TP), and parieto-occipi‐
tal (PO). Nasion, inion, and lateral positions on the perimeter are also included as elec‐
trode locations. The electrode notation differs slightly between the 10–10 and 10–20
systems; electrodes on the 10% perimeter are noted as T7, T8, P7, and P8 in the 10–10
system, which correspond to T3, T4, T5, and T6 in the 10–20 system, respectively.

For neonatal infants, a modified 10–20 system with nine electrodes was proposed (Kell‐
away and Crawley, 1964). The neonatal system replaces Fp1 and F3 with F1, which is
on the 20% perimeter and 10% left of the midsagittal line. Likewise, Fp2 and F4 are re‐
placed by F2. In addition to F1 and F2, T3, C3, Cz, C4, T4, O1 and O2 are included.
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The 10–20 system also serves as a frame of reference on the scalp. An electrode location
that is unique to a study is often reported, referring to the 10–20 system, e.g., “… the
electrode is placed between C3 and Cz locations.” Likewise, an electric or magnetic
brain stimulation location is often specified using this system (Herwig et al., 2003).

Alternatives to the 10–20 system have been developed to cope with ever-increasing
numbers of electrodes. In the 10–20 system, the electrodes are placed on the vertices of
a rectangular lattice, e.g., Cz, C4, P4, and Pz. The distance between Cz and P4 (diago‐
nal) is longer than that between Cz and C4 (side). The unevenness increases as the
number of electrodes increases to 10–10, 10–5, and so forth. This is a problem for some
signal-processing methods, because the EEG from some brain regions is less densely
sampled than from others. The triangle lattice reduces unevenness of the inter-elec‐
trode distance. Therefore, some high-density EEG electrode arrays employ a triangular
lattice. So far, no standardization has been achieved across different triangular-lattice
systems.

Reference and Ground Electrodes

Reference electrodes provide a biological baseline voltage level for the EEG signal. Why
do we want to have such a baseline? In addition to the brain, organs such as the heart
and muscles also show electrophysiological activity. The non-brain electrophysiological
activity is often stronger than the brain activity. The non-brain activity is conducted
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through the body up to the scalp and is added to the brain activity. In other words, the
voltage between the scalp and ground is inflated by the non-brain activity. Reference
electrodes measure the biological noise. A reference electrode is attached, for example,
to the earlobes and nose tip, which are close to the scalp, but there is no brain beneath.
Therefore, the signal from the reference electrode could be regarded as noise. When
preprocessing the EEG signal, the reference signal is subtracted from that of a scalp
electrode (see Fig. 10.1).

The 10–20 system specifies six reference locations; the left and right earlobes are noted
as A1 and A2, respectively. Materials for earlobe electrodes are the same as those for
scalp electrodes, but the shape might vary, e.g., a clip for an earlobe. The designations
M1 and M2 stand for the left and right mastoids and reference electrode locations be‐
hind the ears, where the temporal bone is thick and thus is distanced from the brain.
Electrodes of the same type as those for the scalp are usually used for the mastoids.
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Nasopharyngeal electrodes are denoted by Pg1 and Pg2 and are placed in the left and
right nasal cavity, respectively. The nasopharyngeal references are used in clinical set‐
tings, such as in a diagnosis for brain death. The electrodes are rod shaped so they can
be placed in the nose cavity. Reference locations are chosen according to the aim of
each study. In addition to the six locations of the 10–20 system, other locations, e.g.,
nose tip and a combination of electrodes, could also be used. How do we decide what
reference to use? This issue closely relates to artifact removal, which is discussed in
Chapter 11 (Section 11.1.2).

The ground electrode is attached to protect participants from accidental electrical leak‐
age. The material and type of ground electrode are usually the same as those used for
scalp electrodes. The electrode is placed on the head, e.g., Fpz, an unused location in
the 10–20 system. Different locations may be used in different recording systems. The
signal from the ground electrode is sometimes used to compute the ground voltage lev‐
el. The ground level is near zero, but it fluctuates. Environmental noise, e.g., power sup‐
ply to electric appliances, affects the baseline level. The signal from the electrode is used
to compute an adequate ground level. Therefore, the ground electrode is sometimes
called the “recording reference.”

EOG Electrodes

Electrooculography (EOG) measures the electric activity caused by eye movements.


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The eyeballs are statically charged. As the eyes move, the electric field changes around
the eyes, forehead, and scalp. Thus, the charge is added to the EEG signals. In fact, the
electrooculogram (also abbreviated EOG) is one of the major artifacts in the EEG
recording. To remove the artifact, EOG needs to be monitored simultaneously with
EEG.

Four electrodes are placed around the eyes (Fig. 10.4). The electrodes at the left of the
left orbita and right of the right orbita measure the horizontal EOG (HEOG). The elec‐
trodes above the eyebrow of the non-dominant eye and below the infraorbital border
measure the vertical EOG signal (VEOG). The materials used for the electrodes are the
same as those used for EEG electrodes. The recording ground is usually shared with
EEG. Most commercial EEG recording systems provide an EOG interface. EOG artifact
removal is described in Chapter 11 together with other preprocessing techniques.

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Box 10.2 Dry Electrodes

Dry electrodes refer to EEG electrodes that do not require conductive filler, such as
gel and paste. Dry electrodes are used, for example, for ultra-high-density record‐
ing. As the density of the electrode increases, inter-electrode distance decreases,
e.g., 2 mm (see Fig. 10.2C). The electrodes record similar signals, but each signal
varies slightly among them. In the high-density recording, even a small leakage of
gel could cause a short circuit among the electrodes. This so-called gel-bridge
makes signals of the bridged electrodes identical, thus ruining the recording. Gel-
bridges do not occur with dry electrodes. Another advantage of dry electrodes is
convenience. The time and effort it would take to apply gel to multiple electrodes
are saved. Moreover, electrodes without wet and sticky gel are comfortable for test
participants.

Impedance of dry electrodes is often higher than it is with wet ones. To compensate
for the high impedance, a special amplifier is often required. At this time, the signal
quality is worse and special amplifiers tend to be more expensive than those of con‐
ventional systems with wet electrodes. However, the potential of the dry electrode
method is clear: Imagine a high-density electrode array worn like a headphone or
hair ornament.
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10.1.2 EEG Amplifier

The electric activity measured from the scalp is weak; the voltage – on the order of µV,
i.e., one-millionth volt – is too weak to drive any recording devices that typically re‐
quire an input signal of 5 V or more. Thus, amplification is essential for EEG record‐
ings. In fact, it is so essential that “EEG amplifier” is often used as a synonym for “EEG
recording system.” An EEG amplifier amplifies the weak signals with little distortion.
The frequency range of amplification is set typically between 0.1 and 500 Hz. The low‐
est frequency is determined by a parameter called the time constant. The longer the
time constant becomes, the slower the lowest frequency becomes. To obtain “ultra-
slow” activity, e.g., 0.1–0.03 Hz, which corresponds to the dominant frequency range in
the hemodynamic response fMRI signal, a special amplifier, called a DC amplifier, is
often used. The letters DC stands for “direct current” and the frequency of this DC
component is 0 Hz; thus, it is the slowest activity. A DC amplifier is able to amplify DC

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and very slow components without distortion. In this regard, a typical EEG amplifier is
an alternating current (AC) amplifier. Because the majority of EEG amplifiers are AC
amplifiers, we tend to skip the “AC.” In a modern EEG system, amplification is applied
more than once, first using an analog signal, then later using a digital signal. A pream‐
plifier refers to a device that amplifies and rectifies the analog signal.

After preamplification, the analog signal is fed to an analog-to-digital (AD) converter.


The AD converter samples the analog voltage signal in a short time interval, e.g., every
2 ms. The number of samplings per second is called the sampling frequency or sam‐
pling rate. For example, if we sample data every 2 ms, the data are sampled 500 times
per second. Thus, the sampling frequency is 500 Hz. If the sampling frequency is too
low relative to the signal frequency, the samples do not represent the original signal
properly: A slow component that does not exist in the original signal is generated. This
problem is called aliasing (Fig. 10.5A). According to the sampling theorem (also
known as the Nyquist theorem as introduced in Chapter 1), the sampling frequency
should be more than twice the frequency of the signal. The theorem could be under‐
stood intuitively by imagining how to code one cycle of a sine wave. At least a point at
the peak and another at the trough, i.e., two points, are needed to code one cycle. In the
case of EEG, often the frequency range of interest is 0.1–50 Hz. Thus, the sampling fre‐
quency needs to be 100 Hz or higher.
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Figure 10.5 Sampling frequency and AD level.

For signal processing on a computer, the sampled values are binarized. In 1-bit coding,
each value is coded 0 or 1 relative to a single threshold, e.g., the mean voltage value. In
2-bit coding, the value is coded in 22 = 4 levels: 00, 01, 10, and 11 (Fig. 10.5B).
Similarly, 3-bit encoding has 23 = 8 levels: 000, 001, 010, 011, 100, 101, 110, and 111; 4-
bit encoding would be 24 = 16 levels: 0000, 0001, 0010, and so on. The level of binariza‐
tion is called the AD level. The higher the level, the more details of the signal are en‐
coded. For EEG recording, AD level is typically 8 bit: 28 = 256 levels, or higher.

The digitized EEG is a large matrix of data points; M data points in time by N elec‐
trodes. Together with the EEG data matrix, recording information, e.g., sampling fre‐
quency, channel labels, and participant information, is saved. When a task is applied,
event markers, e.g., stimulus onset and response button press, are also saved. Some
EEG file formats save EEG and recording information in one file, while other formats
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save them in separate files. Most EEG recording systems and analysis packages support
multiple output file formats.

10.1.3 Procedure for Data Acquisition

The last element of the EEG recording involves the test participants. Without their co‐
operation, no good signal is acquired. Therefore, it is important to keep them happy
and relaxed as much as possible. When electrodes are attached, it takes some minutes
for the conductive gel to stabilize the contact impedance between the electrodes and
the scalp. Other sensors, such as EOG electrodes, are also attached to monitor artifacts.
Cables from the electrodes and the sensors are secured to prevent drift artifacts caused
by motion of the cables. The participant is seated in a chair or lies on a bench in an
electrically shielded room. The shielded room is covered by conductive materials. The
materials capture and drain environmental electric noise activity (cf. a Faraday cage).
Thus, the space inside of the room is not affected by the noise. It is also possible to mea‐
sure EEG without a shielded room; recent EEG recording systems often offer effective
noise reduction functions with which a reasonable signal can be obtained. Also, a test
room is usually sound attenuated, and the lighting is adjusted to control background
sensory inputs.

During the recording, the participant is instructed to minimize body motion. Chin-,
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head-, and/or armrests could be used to help the participants to keep the same posture
comfortably, which in turn helps to reduce noise. At the beginning of the recording ses‐
sion, a rest or baseline period is recorded. Blocks of specific task manipulations follow.
Often, the rest/baseline period is repeated after the task. After a recording session, elec‐
trodes are removed, and gel is wiped or washed off.

The methods section in an EEG paper is rather uninviting; it is filled with technical
terms and abbreviations. That “jargon,” however, tells us what was done concisely and
precisely. By now, we have learned enough details to understand a typical section of
recording information. Here is an excerpt from an EEG paper (Bruggemann et al.,
2013) in which recording information is described. Let’s try to read it!

Electrocortical data were recorded from 30 Ag/AgCl


sintered electrodes, arranged according to the international
10–10 system, and referenced to the nose tip. Only data
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13/03/2023, 19:26 Electroencephalography and Magnetoencephalography

from fronto-central electrodes (i.e., F3, Fz, F4, FC3, FCz,


FC4, C3, Cz, C4) are reported here. … Horizontal and
vertical electro-oculograms were recorded from tin
electrodes positioned adjacent to the outer canthus of each
eye, and above and below the left eye, respectively. The
electrical impedance of each electrode was maintained at
less than 10 kilo-ohms. These data were acquired
continuously via NeuroScan SynAmps hardware with Scan
4.3 software. … The sampling rate was 500 Hz.

10.2 Magnetoencephalography (MEG)

Magnetoencephalography (MEG)measures the magnetic field resulting from brain ac‐


tivity. In Section 9.1.2 in Chapter 9, we learned how a magnetic field emerges as a result
of electrophysiological activity of neurons: As postsynaptic currents run in the apical
dendrites of cortical pyramidal cells, a magnetic field is formed perpendicular to the di‐
rection of the current. Magnetoencephalography measures the strength of the magnetic
field. The source of the MEG signal is the same as that of the EEG signal. In this sense,
MEG could be considered as the twin of EEG. However, the MEG signal is not identical
to the EEG signal. For example, the magnetic field permeates brain tissue, cere‐
brospinal fluid (CSF), skull, scalp, and air with little distortion. This is a big difference
TMG 80:62:80 3202 raM 31 ,noM ,ua.ude.bleminu.tneduts@atorihm

from the electric field, which is bent and mixed as

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