RECORDING EEG DURING REPETITIVE TRANS-CRANIAL

MAGNETIC STIMULATION

Hubert de Bruin, Mark Archambeault, Trung Trinh and Gary Hasey

Dept. of Electrical and Computer Engineering, Dept of Psychiatry and Behavioural Neurosciences

McMaster University, Hamilton, Ontario, Canada

Keywords: rTMS, Stimulus artefact, Electrode heating, Artefact reduction, EEG, Trans-cranial magnetic stimulation,

Evoked potentials.

Abstract: This paper discusses several issues related to recording EEG during repetitive trans-cranial magnetic

stimulation (rTMS). The objective of recording EEG is to obtain magnetically evoked and event related

potentials. The issue of electrode heating is discussed and experimental results presented that show graphite

as well as fully notched or “C” silver, gold or silver-silver chloride are suitable for current rTMS protocols.

Standard silver or gold cup electrodes may cause excessive scalp heating. Removal or reduction of the

magnetically induced stimulus artefact is also discussed. A new system is presented that uses sample and

hold circuitry to block most of the artefact allowing the researcher to record ipsi- and contra-lateral evoked

potentials occurring within the first few milliseconds of the magnetic stimulus.

1 INTRODUCTION

Trans-cranial magnetic stimulation (TMS) has been

used during the past two decades to elicit responses

in the human brain. At first this modality was

suggested as a technique for studying upper motor

neuron health and function. This involved placing a

coil, either circular or “figure of eight” on the scalp

with its centre of strongest magnetic field over an

area of the motor cortex and exciting the underlying

cortical tissue with 300 – 400 μsec monophasic or

biphasic pulse. The response could be immediately

measured by recording the M-wave from the muscle,

usually the thenar, innervated by the upper motor

neurons under the coil. However, in recent years,

repetitive TMS has been proposed and used to treat

neuro-psychiatric disorders such as depression by

stimulating the medial frontal cortex (e.g. Fitzgerald

et al, 2003 and Hoffman et al, 2005). Since there are

no immediate recordable results such as the M-wave

for these sites, stimulus amplitudes have been

chosen by first determining the motor cortex

threshold and using a fraction, usually from 80 to

120% of this value. As well the stimulus site and

repetition frequency are chosen by convention rather

than patient responses. However, There is very

good evidence that the cortical responses are very

dependent on the stimulus site with some sites even

having no or very limited responses (Komssi et al,

2002). It has also been found that even the motor

threshold varies considerably intra-subject from

session to session (Wasserman, 2002) and there is

considerable evidence that frontal lobe thresholds are

higher than motor cortex thresholds (Kähkönen, 2005).

If one could record the immediate brain evoked

potentials (EP), or event related potentials (ERP),

stimulus amplitude, frequency and site could be

customized for each subject. This approach will also

allow us to gain valuable insight and knowledge

about the mechanisms of rTMS applied to the frontal

lobes. However, the very large magnetic fields

associated with 1 to 3 Tesla TMS pulses couple into

the patient electrodes, electrode cables and input

amplifiers resulting in very large voltage artefacts

that can saturate the input amplifiers for up to 500

ms. This paper discusses issues related to recording

EEG during rTMS and presents a new system for

recording magnetically evoked EPs and ERPs

2 ELECTRODE SELECTION

Not only does the very high magnetic field induce

currents in the cortex and deeper brain structures it

265

de Bruin H., Archambeault M., Trinh T. and Hasey G. (2009).

RECORDING EEG DURING REPETITIVE TRANS-CRANIAL MAGNETIC STIMULATION.

In Proceedings of the International Conference on Bio-inspired Systems and Signal Processing, pages 265-272

DOI: 10.5220/0001534102650272

 SciTePress

also induces currents in the electrodes that are being

used to record the EEG. This induced current flow

will heat the electrodes. The temperature increase of

an electrode per stimulus is directly related to the

electrical conductivity of the electrode, the square of

the radius of the electrode and the square of the

stimulus strength (Roth, 1992). The conductivity of

materials tested is: Silver 62.9x10

S/m, Gold

41.0x10

S/m, Carbon 0.029x10

S/m (Serway,

2000), which suggests that silver electrodes will heat

the most per stimulus, while carbon electrodes will

heat the least per stimulus.

The safe temperature an electrode can reach

without causing cutaneous damage depends on the

exposure time. Figure 1 shows the time-surface

temperature threshold for first degree thermal injury.

Given that current rTMS treatment can include as

many as 2,400 pulses at a frequency of 0.25Hz up to

20Hz, electrode heating is a concern for causing

thermal skin damage. Looking at Figure 1, we see

that for a 30 minute study, 46°C is the hottest

temperature any scalp EEG electrode should be

allowed to heat to.

Figure 1: Time-temperature thresholds for burning of

human skin. Source: Moritz et al, 1947.

2.1 Electrode Testing

We decided to test a number of common and

modified EEG electrodes to determine which are

suitable for recording during rTMS. Temperature

was measured using a thermistor temperature probe

with 0.01°C accuracy (Digi-Sense LN5775, Cole-

Parmer, Illinois) calibrated to +/- 0.2°C and read to

0.1°C. The TMS machine used was a Magstim

Super Rapid. The TMS coil used was a Magstim

figure-of-eight air-cooled coil P/N 1640 (Inner

diameter 56mm, outer diameter 87mm, 9x2 turns,

16.4µH inductance, 0.93Tesla peak magnetic field).

Four commercially available EEG electrode types

were tested: (i) XLTEK reusable EEG/EP

electrodes Part no. #101339 (silver cup, 10mm

diameter, 2mm hole); (ii) Standard gold cup

electrodes (10mm diameter, 2mm hole); (iii)

Ag/AgCl surface electrodes model F-E5SCH-48

(10mm diameter, 2mm hole, Grass Technologies);

(iv) EL258RT reusable general purpose 8mm

diameter, no hole, radio-translucent carbon

electrodes with carbon leads (Biopac Systems Inc.).

Several gold and silver cup electrodes were pie-

notched and a gold plated silver cup electrode

(10mm diameter, 2mm hole, Nicolet) was fully

notched (C notched) to reduce induced current as

shown in Figure 2.

All testing used a sheet of plywood that was

marked with a 1cm grid pattern to help ensure

accurate coil placement. Electrodes were attached

using EEG paste (Ten20 conductive EEG paste).

The coil was placed so that the electrode was in the

area of maximum field induced heating as shown in

Figure 3. This position agreed with previous

findings (Roth et al 1992). The testing parameters

used in this study mirrored those used in standard

rTMS treatments: 10Hz stimulation for up to 8s

trains and 20Hz stimulation for up to 3s trains;

stimulus intensity was set at 85% of our machine’s

maximum to slightly exceed 110% of motor

threshold (MT) of an average subject at our own and

other rTMS laboratories (Thut et al, 2005).

Figure 4 shows the heating and cooling curves

for the 6 different electrodes tested with 3s 20Hz

trains at the maximum heating location (r = 30mm).

A second test was performed to simulate a full

treatment session where trains of 60 to 80 stimuli

are given at 1 minute intervals for a total of up to

3000 stimuli. Figure 5 gives the test results for a

gold cup electrode using only three trains of 60

stimuli at 20 Hz. As can be seen the electrode

temperature would soon rise above the maximum

allowable 46

C if more trains were given.

Carbon electrodes were also tested at 20Hz for

3s, 85% intensity, and 20Hz for 10s, 100% intensity

and showed 0.0°C and 0.8°C temperature rise

respectively. Repeating the 100% test with no

electrode resulted in 0.3°C temperature rise,

showing that the probe accounted for some of the

increase in temperature when 200 pulses were given.

Figure 2: Notched electrodes. From left to right: C

notched, pie notched, triple pie notched.

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Figure 3: Stimulating coil showing how electrodes were

positioned underneath with respect to the r-axis, labeled in

cm.

Figure 4: Temperature effects for 6 different electrodes

from a single train of 3s at 20Hz at 85% intensity, r = 30

mm.

Figure 5: Temperature effects on gold cup electrodes from

3 trains of 3s at 20Hz at 85% intensity, r = 30 mm. Trains

were given at 0s, 60s, and 120s.

2.2 Electrode Guidelines

Unmodified silver and silver/silver chloride

electrodes appear unsuitable for standard rTMS-

EEG studies when high stimulus intensities are

necessary, due to the high conductivity of silver. If

used at all, pulse trains should not exceed 30 pulses

and electrodes should be allowed 290s to cool

between trains, given the current TMS and coil

parameters tested. Gold cup electrodes are suitable

for rTMS-EEG studies for a Magstim cooled coil if

stimulus intensity is kept below 85%, trains do not

exceed 80 pulses, and electrodes are allowed to cool

for 220s between stimulus trains. However,

notching does work, and when notched properly (a

full notch or C) electrode heating is reduced enough

to make silver and gold-plated silver electrodes

suitable for a standard rTMS-EEG study. The newly

available carbon electrodes should be suitable for

any rTMS-EEG patient study and their heating

would not be the limiting factor in selecting

stimulating parameters. However, they are about

three times the cost of Ag/AgCl electrodes.

3 ARTEFACT REDUCTION

Most modern commercial EEG systems are

protected from large voltage transients both by input

protection diodes and low pass filtering of the EEG

signal, typically below 70 Hz. Figure 6 shows the

average EEG recorded from a standard Ag cup

electrode at FP2 using a commercial EEG system

(XLTEK desktop EEG, Oakville, Ontario, Canada),

for six high amplitude TMS pulses delivered at the

F3 position. Although the amplifier hasn’t saturated

the artefact lasts at least 100 ms obscuring any EPs

and even some shorter latency ERPs. Several

researchers (Ives et al, 2006 and Fuggetta et al 2005)

have attempted to reduce this TMS stimulus artefact,

recorded using commercial EEG systems, by

designing low slew rate preamplifiers. Although

this approach is successful if only long latency ERPs

are considered, this low bandwidth is inadequate to

preserve the much higher frequency EPs. Further,

the sampling rate of commercial EEG systems (200

– 500 Hz) is too low to represent EPs.

Virtanen et al (1999) developed a multi-channel

EEG system with artefact blocking hardware to

record both EPs and ERPs following TMS.

However, this system cannot record EPs occurring

during the first 4 ms following stimulation and the

sampling rate of 1000 Hz is too low to fully capture

the shape of very short duration EPs. We have also

developed an artefact blocking system based on

sample and hold circuitry similar to Virtanen et al’s

approach. An earlier version (Archambeault and de

Bruin, 2007) was designed as a blocking

preamplifier for commercial EEG systems.

However, the sampling rates possible for these

RECORDING EEG DURING REPETITIVE TRANS-CRANIAL MAGNETIC STIMULATION

267

systems are inadequate for multichannel EP

recording.

3.1 A New System

We decided to implement a 16 channel EEG system

with the previous artefact blocking amplifiers using

the virtual instrument language Labview running on

a standard PC equipped with a National Instruments

DAQ interface. As shown in Figure 7, the DAQ

analog outputs are used to control the sample and

hold circuit for each channel and trigger the

magnetic stimulator. The system has selectable hold

time window duration and the stimulator trigger time

within this window. The user can also select the

channel sample rate, total signal period, stimulus

rate and the number of stimuli given. During rTMS

the channel recordings are continually displayed for

analysis and verification, and synchronously

averaged for background EEG and instrumentation

noise reduction. Following completion of the

stimulus train the averge signal for each channel is

stored in an EXCEL format file for further signal

processing and analysis using programs such as

Matlab. This gives us a very flexible clinically

friendly system with aggregate sampling rates up to

200 KHz (at least 10 KHz per channel). This system

can easily be upgraded to 32 channels with different

DAQ hardware.

Subject 1

-40

-30

-20

-10

0.00.51.01.52.0

Time (s)

EP Voltage (µV)

Figure 6: Averaged ERP, created from six ERPs recorded

with XLTEK EEG machine. TMS over left hemisphere

frontal cortex. EEG recorded from right hemisphere

frontal cortex.

Ch0+

Gnd

Sample‐

and‐hold

Unity

gain

buffer

HPF

.16Hz

GainStage

(Non‐

inverting

op‐amp,

LPF

1500Hz

LabVIEW

DAQboard



Analog

Output



Computer

Magneticstimulator



Ch0‐

GainStage

(Instrumentation

Amplifier,10x

gain)

Figure 7: Artefact blocking EEG machine design using the sample-and-hold (blocking) approach (one channel shown).

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Figure 8: EEG responses for medial left frontal lobe

stimulation at F3 at 66% maximum amplitude.

Figure 9: EMG responses for left thenar muscle for two

recording electrodes, Ag and AgCl for wrist stimulation at

90% maximum amplitude.

3.2 System Tests

The system was tested to determine whether the

blocking circuit could manage large magnetic

artefacts and which hold window durations were

suitable. A 24 year old subject was instrumented

with Grass 10 mm Ag/AgCl electrodes at F3 and F4,

the right mastoid (reference) and the neck (ground).

60 magnetic pulses at a rate of 2 Hz were given near

F3 in the medial frontal lobe at 66% of the

maximum amplitude of a Magstim Super Rapid

stimulator. The hold time duration was set to 2.6

msec with the stimulus trigger command given at 0.3

msec after the start of the sample and hold

command. The signals were collected for 100 msec

at 5 KHz sample rate. Figure 8 shows the average

EEG signals for both locations.

In this figure the first rectangular pulse is the

offset voltage applied by the sample and hold circuit

and can be viewed as the total hold window.

Unfortunately both Labview and the Magstim

control program are Windows based and there is

some uncertainty that the magnetic stimulus is

given at the precise time (0.3 msec after the start of

hold). The maximum artefact block in this case is

2.3 msec but it could be less. The negative

excursion is due to the residual stimulus artifact,

which decays exponentially toward the baseline.

The F3 signal shows the evoked muscle M-wave

resulting from magnetic stimulation of the

temporalis muscle under the coil. This usually

occurs within 1 msec of the magnetic motor point

stimulation. F4, as expected shows no muscle

response and only the decaying artefact, which is

almost the same size as the F3 artefact. Both signals

were heavily contaminated by 60 Hz and other

environmental noise and, although not synchronized

to the stimuli, were still not entirely removed by

averaging. The laboratory contained a number of

high power instruments with large transformers

resulting in very large 60 Hz ambient noise.

Because of the residual noise in the signal we cannot

be sure the small μvolt excursions were brain evoked

potentials.

The duration and amplitude of the artefact are

determined by stimulus amplitude and shape, as well

as the impedances of the electrodes, electrode wires

and input amplifier. If these impedances were

purely resistive, the artefact would last no longer

than the stimulating pulse (400μsec). We wanted to

address the issue whether polarisable or non-

polarisable electrodes would result in less artefact.

The hypothesis was that a non-polarisable electrode

such as Ag-AgCl would store less artefact energy

because of their low capacitance. Ag or Au

commercial polarisable electrodes, on the other hand

would store more energy resulting in a larger

residual artefact when the sample and hold circuit

reconnected the electrodes to the amplifier.

The left thenar muscle of a 24 year old male was

instrumented with two electrodes, Ag-AgCl and Ag,

in close proximity. A reference Ag-AgCl electrode

distal to the second joint of the thumb and a ground

Ag-AgCl electrode on the dorsum of the hand. The

Magstim figure-of-eight coil was placed at the wrist,

5 cm equidistance from the two thenar electrodes.

The sample and hold circuitry was set to block the

RECORDING EEG DURING REPETITIVE TRANS-CRANIAL MAGNETIC STIMULATION

269

artefact a maximum of 1.7 msec after the stimulus

was given . A single 90% maximum amplitude

stimulus pulse was given by the Magstim and 100

msec of signal recorded from both electrodes at 5

KHz sample rate. Figure 9 shows the first 50 msec

of the unprocessed signals.

As for Figure 8, the hold window of 2.0 msec

appears first, followed by a rise to approximately

4.25 mV (amplifier saturation) due to the residual

stimulus artefact. The resulting signal excursion is

due to the evoked muscle M-wave and the decaying

stimulus artefact. The signals after 15 msec are due

to 60 Hz and other environmental noise. The M-

waves and decaying stimulus artefacts are very

similar with the Ag-AgCl signal decaying slightly

faster. This could also be due to the slightly

different M-waves recorded by the two electrodes.

Lower levels of stimulation that resulted in much

smaller M-waves showed the same similarities. At

this point it must be concluded that the type of

electrode has little effect on the residual stimulus

artefact and our early hypothesis that non-

polarisable electrodes would have lower

magnetically induced artefacts was wrong.

3.3 Multi-Channel Tests

The multi-channel system was tested for 16 channels

of evoked potentials recorded from a male subject

instrumented using the standard 10-20 electrode

configuration. The human tests were approved by

the Research Ethics Board of St. Joseph’s Health

Care, Hamilton, Ontario, Canada. Figure 10 shows

the averaged responses for 80 stimuli given at 8 Hz

at 69% of the Magstim maximum amplitude (110%

of the motor threshold) with the coil placed over

Brodmann area 46. The signals were sampled at 5

KHz and bandpass filtered from 15 Hz to 2.5 KHz.

At the scale shown all that can be seen are the very

large amplitude muscle responses or M-waves from

the underlying temporalis and occipitofrontalis

muscles. The null response for F3 is a result of

amplifier saturation since the coil was placed over

F3 and the amplifier hold time was only 2 msec.

Figure 11 shows the same response starting at 15

msec with increased resolution. Fp1 shows EPs at

18 msec, while other EPs can also be seen at 47 and

85 msec in all channels. These synchronous EPs

may be a result of using linked reference electrodes

over the mastoid bone.

Figure 10: EEG averaged responses for 80 stimuli at 8 Hz,

69% max, Brodmann area 46. One unit = 1 mV, channels

spaced by 5 mV.

Figure 11: EEG averaged response of Fig. 10 One unit =

0.25 µV, channels spaced by 25 µV.

Figure 12: EEG averaged responses for 80 stimuli at 8 Hz,

69 % max, Brodmann area 9. One unit = 0.25 µV with

channels spaced by 25 µV.

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Figure 12 shows the results for the same stimulus

train but with the coil placed over Brodmann area 9.

Two features can be noted: (i) the F3 channel is not

saturated since the coil was not immediately over the

F3 electrode position and the pattern of EPs is

different for that shown in Figure 11.

4 CONCLUSIONS

Our research has shown that standard commercial

Au and Ag or Ag-AgCl EEG electrodes cannot be

used for general rTMS applications, due to excessive

skin heating. However, these electrodes can be used

if fully or “C” notched. Further the choice among

these electrodes does not seem to affect the

amplitude or duration of the stimulus artefact.

Although our heating results are in general

agreement with the conclusions of previous

researchers, the lack of dependency of the stimulus

artefact amplitude on electrode material does not

(Virtanen et al, 1999). Their results show that the

amplitude depends mostly on electrode size and that

Ag-AgCl electrodes had very low artefacts

compared to Ag, although this could be a result of

the very small Ag-AgCl pellet size. Further, their

fully notched Ag standard electrodes had much

lower artefact than the intact ones. The principle

contributors to the stimulus artefact are not well

understood, and electrode, wire and input amplifier

capacitances all play a part. Even in a multichannel

recording situation, where the magnetic field

orientation and amplitude is very different for each

electrode, the residual stimulus artefacts can be very

similar as shown in Figure 8. Further research will

be conducted to investigate the determining factors

for magnetically induced artefacts and how common

these are for all stimulating and recording

conditions.

The new EEG system works very well, and

depending on the stimulus strength, the amplifier

can be reconnected to the recording electrodes with

delays from 1 to 4 msec, allowing us to record EPs

as well as ERPs. The initial voltage offset

introduced by sample and hold circuitry, shown as

the square pulse in Figures 8 and 9, can be ignored

and does not affect the signal when the block is

terminated. Tests with the stimulating coil at some

distance from the electrodes resulting in very low

short duration artefacts have shown that the

amplitude returns to baseline within μsec. The test

results shown in this paper were for worst case

scenario experiments with large stimulus amplitudes

and the coil either directly over the recording

electrodes or in close proximity. However, the

system must be made more immune to

environmental noise by better shielding and cabling.

Future work will include postprocessing to

estimate and remove the exponentially decaying

residual artefact and periodic environmental noise.

Although synchronous averaging can remove

asynchronous environmental noise if enough stimuli

are given, the technique is inefficient. The number

of stimuli presented to the brain should be

determined by clinical efficacy rather than noise

reduction.

The multi-channel results show that even when

stimulus artefact is removed new signal processing

techniques will have to be developed to model and

remove the muscle M-waves.

ACKNOWLEDGEMENTS

Support for this research from the Natural Sciences

and Engineerung Research Council of Canada is

gratefully acknowledged.

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