Individual subject sensitivity to extremely low frequency magnetic field

Alexandre Legros a,*, Anne Beuter b

a Lawson Health Research Institute, Department of Imaging, St. Joseph’s Health Care, 268 Grosvenor Street, London, Ont., Canada N6A 4V2b Institut de Cognitique, Universite Victor Segalen Bordeaux 2, 146 Rue Leo Saignat, 33076 Bordeaux Cedex, France

Received 12 October 2004; accepted 16 February 2006

Available online 18 April 2006

Abstract

It is becoming important to specify the smallest effects of extremely low frequency (ELF) magnetic fields (MF) on human physiology. One

difficulty is that some people seem more sensitive and more responsive than others to MF exposure. Consequently, within- and between-subject

differences have to be taken into account when evaluating these effects. As shown in previous work, human postural tremor is sensitive to MF

exposure. But data about individual responses have not been examined in detail. Thus, postural tremor of 24 subjects was evaluated under ELF MF

‘‘on’’ and ‘‘off’’ conditions in a double-blind real/sham exposure protocol. The direction of the tremor changes was analyzed individually for three

tremor characteristics. Results showed that subjects with high amplitude tremor seem to be more responsive to MF exposure. MF had an

instantaneous effect (between ‘‘on’’ and ‘‘off’’ conditions) and also a more delayed and persistent one (between real and sham conditions), but

differences were small. Moreover, due to the within- and between-subject variability, no statistical analysis could be done. However, these results

do not show any potentially harmful effect of domestic or industrial 50 Hz MF on humans. They provide a starting point to orient future studies and

should be taken into account in the establishment of new exposure limits.

# 2006 Elsevier Inc. All rights reserved.

Keywords: Postural tremor; ELF; Magnetic field; Individual differences

NeuroToxicology 27 (2006) 534–546

1. Introduction

In 1997, an international seminar was held in Bologna (Italy)

on the biological effects and related health hazards of ambient

or environmental static and extremely low frequency (ELF)

magnetic fields (MF). Following this seminar, sponsored

among others by the World Health Organization (WHO) and

the International Commission on Non-Ionizing Radiation

Protection (ICNIRP), Repacholi and Greenebaum (1999)

recapitulated the research that is still needed to better

understand MF effects on humans. They underlined the need

to explore whether electrophysiological indices of central

nervous system activity and function are affected by ELF MF.

They also specified that published reports should include

information on the smallest MF effect that could be detected in

humans.

Several studies have been done on electrophysiological

parameters such as electroencephalogram (EEG) or evoked

* Corresponding author. Tel.: +1 519 646 6100x65959; fax: +1 519 646 6399.

E-mail address: alegros@lawsonimaging.ca (A. Legros).

0161-813X/$ – see front matter # 2006 Elsevier Inc. All rights reserved.

doi:10.1016/j.neuro.2006.02.007

potentials (Bell et al., 1992, 1994a,b; Cook et al., 2004; Heusser

et al., 1997; Lyskov et al., 1993a,b; Lyskov and Sandstrom,

2001; Marino et al., 2004). However no consensus exists on the

direction of the effects due to the wide variety of exposure

procedures used (length of the exposure, intensity and

frequency of the MF, recordings made sometimes during and

sometimes after the exposure). Moreover, MF induce artifacts

in electrophysiological data which often make recording during

exposure not possible (see for example Cook et al., 2004).

If such neurophysiological effects exist, they might have

behavioral manifestations. Many studies have been a MF effect

on cognitive performance, on reaction time (Cook et al., 1992;

Kazantzis et al., 1998; Podd et al., 2002, 1995; Preece et al.,

1998; Whittington et al., 1996) and on human motor control.

Indeed, Thomas et al. (2001) showed that a 200 mT pulsed MF

improved human standing balance. Physiological tremor is a

highly sensitive indicator of neuromotor pathway integrity and

may be influenced by more than 37 factors (Wachs and Boshes,

1966). Briefly, three mechanisms contributing to its generation

have been described: (1) short-latency spinal feedback from

stretch receptors and long-loop transcortical or transcerebellar

reflex pathways from these receptors, (2) mechanical properties

A. Legros, A. Beuter / NeuroToxicology 27 (2006) 534–546 535

of the extremities and (3) central oscillations modulating motor

neuron pool activity. Some studies analyzed the effect of

transcranial magnetic stimulation (TMS), which is a high

intensity MF stimulation of the cerebral cortex (up to 2.5 T), on

human tremor. Results showed that TMS can reduce tremor

severity in patients with essential tremor or Parkinson’s disease

(Britton et al., 1993; Gironell et al., 2002; Pascual-Leone et al.,

1994).

Recently, we explored how a low intensity MF (1000 mT,

50 Hz) could have an effect on human distal motor control by

studying postural tremor and motor control during a finger-

tracking task (Legros and Beuter, 2005; Legros et al., 2006).

Results showed a possible MF effect on postural tremor

increasing the proportion of the low frequency component

Fig. 1. (a) Illustration of the four sequences of an experimental session. The order

time, vertical grey bands represent the 62 s recording periods and solid lines show M

line represents the status of sham MF (i.e., its position if MF was present). (b) Only 58

two parts of 29 s (before and after the MF transition). (c) Recordings 1–4 and 5–8 of

(between 2 and 4 Hz) and facilitating the decrease of tremor

intensity over time. These results were obtained by analyzing

three quantitative characteristics computed on postural tremor

time series: amplitude, peakedness and proportional power in

the 2–4 Hz range (Beuter and Edwards, 1999; Beuter et al.,

2003; Edwards and Beuter, 2000). It has been shown that

sensitivity and responsiveness to ELF MF may vary across

subjects (Levallois, 2002; Bell et al., 1991). For example,

Lyskov and Sandstrom (2001) indicated that patients with

‘‘electrical hypersensitivity’’ tend to be hyper-sympathotone,

hyper-responsive to sensory stimulation and to have heightened

arousal. Therefore, the main aim of this study was to examine

within- and between-subject differences in postural tremor

characteristics in relation to ELF MF exposure. Indeed if

of presentation of these sequences was counterbalanced. X-coordinates express

F status (‘‘off’’ when the line is down and ‘‘on’’ when the line is up). The dotted

s centered on a MF transition were kept in each recording and were composed of

Fig. 5a are, respectively, equivalent and were averaged (1 with 5, 2 with 6, . . .).

A. Legros, A. Beuter / NeuroToxicology 27 (2006) 534–546536

differences between subject responses to MF exposure would

exist (subjects more or less responsive, with heterogeneous

reactions), they would not be detected in group results but only

through an individualized examination.

2. Materials and methods

2.1. Subjects

Thirty-six men between the ages of 20 and 50 years

(37.8 � 8) occasionally subjected to 50 Hz MF during their

work were recruited among the personnel of the French

electricity company ‘‘Electricite de France’’ (EDF) and

completed the experiment. They were volunteers and gave

informed consent before their participation. None of them had

previously taken part in studies involving MF exposure. Before

testing they were required to complete a screening ques-

tionnaire to ensure that: they did not use drugs or medications

regularly; they had never experienced an epileptic seizure; they

had no limitation of hand or finger movements; they did not

suffer from chronic illness (e.g., diabetes, psychiatric, cardio-

vascular or neurological diseases); they had no cardiac or

cerebral pacemaker; and they had no metallic implant in the

head or in the thorax. This information was verified by EDF’s

occupational medicine service. All subjects were asked to

Fig. 2. Time series sampled at 1000 Hz and corresponding histograms for 10 s recor

for Gaussian white noise with two simulated myoclonic-like movements. Regular os

peaked distribution of Gaussian white noise has a lower peakedness coefficient (0.

distribution with ‘‘outliers’’ has peakedness values even lower than Gaussian white no

refrain from smoking or drinking coffee the morning of the

experimentation. The study’s protocol was reviewed and

approved by the Operational Committee for Ethics in life

sciences section of the Centre National de la Recherche

Scientifique (CNRS, France).

2.2. Procedures

Subjects were all tested at the same time of day (9.00 a.m.),

during a single session (Crasson et al., 1999; Tyrer and Bond,

1974), under natural lighting and the room temperature was

controlled at 23 8C (Lakie et al., 1994). Their handedness was

determined using the Oldfield questionnaire (Oldfield, 1971).

After completing these requirements, they sat on a plastic chair

placed in the middle of the MF generating device. Their

dominant forearm was placed in a prone position on an armrest

and the dominant tested hand was placed with the palm facing

towards the ground on a molded clay support. The armrest was

adjustable according to each subject’s morphology. A piece of

white cardboard (<1 g) was fixed on the index finger’s nail

10 cm from the metacarpophalangeal joint. A Class II laser

diode (micro laser sensor LM10, series ARN12, Matsushita

Electronic Work Ltd., Osaka, Japan) located vertically 8 cm

above the piece of white cardboard and pointing towards the

ground, transmitted a beam recording the vertical displacement.

ding of a sine wave at 2 Hz (left), for 10 s of Gaussian white noise (middle) and

cillation has a bimodal distribution with a high peakedness value (0.90) and the

79, corresponding to the expected value offfiffiffiffiffiffiffiffi2=p

p, Timmer et al., 1993). Data

ise (0.73) due to the increase of the amplitude range induced by only few values.

A. Legros, A. Beuter / NeuroToxicology 27 (2006) 534–546 537

The laser used was an analog output sensor, which used an

optical triangulation range measurement system. Its resolution

was 5 mm (2s) at the observed frequencies. It was calibrated

with a micrometer prior to each testing day. An oscilloscope,

placed 1 m in front of the subject, displayed a horizontal target

line and gave visual feedback of the index finger vertical

position. An infrared probe was fixed on the tip of the non-

dominant thumb to monitor heart rate and a temperature probe

was fixed on the palm side of the wrist to record skin

temperature. The subject and the experimenter wore ear plugs

and an anti-noise helmet in order to be isolated from

environmental noise.

Subjects participated to a single session of 65 min

composed of four sequences (Fig. 1a) in which postural

and kinetic tremors were recorded under two MF conditions

(real exposure or sham exposure). The four sequences,

separated by 3 min, lasted 14 min each and included: (1)

postural tremor under real exposure, (2) postural tremor under

sham exposure, (3) kinetic tremor under real exposure and (4)

kinetic tremor under sham exposure. Each sequence followed

the same format and the 24 possible presentation orders of

these sequences were counterbalanced. Sequences were

composed of four 62 s recording periods centered on a MF

Fig. 3. Graphical representation of the recording 1 of subject 31 (‘‘off/on’’ transition

An example of high velocity segment (HVS) is circled. (b) The same time series with

a normalized scale. Amplitude and peakedness for the first and the last 28 s are displa

line) 28 s of position time series. (e) The same graphic is displayed for velocity tim

displayed on the graphic. Velocity time series are not drawn because they do not

transition, and during each sequence, there were four MF

transitions (two ‘‘off/on’’ and two ‘‘on/off’’, see Fig. 1b).

Thus, the experimental design was AB BA AB BA with

repeated measures. Each AB or BA corresponded to a 62 s

recording of tremor with A corresponded to 31 s with the MF

‘‘off’’ and condition B correspond to 31 s with the MF ‘‘on’’.

Only 58 s of recording centered on a MF transition were kept

for analysis: the first 2 s of each time series were cut to

eliminate a possible transient effect due to the beginning of

the task, and the last 2 s were cut to equilibrate A and B

durations. The course of each experimental session was

entirely programmed and was controlled by a computer.

Therefore, neither the subject nor the experimenter knew

when the MF was really present.

Twenty-four subjects satisfied the inclusion and exclusion

criteria. In the present paper, only postural tremor (tremor

occurring while subjects had to maintain a fixed position with

their index finger) was studied under real and sham conditions.

Subjects were asked to relax and point their index finger in front

of them without hyperextending it. They had to control their

finger position by maintaining alignment between the feedback

line and the horizontal reference line displayed on the

oscilloscope.

). (a) The row displacement time series in mm during the 58 s kept for analyses.

frequencies below 2 Hz and above 40 Hz filtered out. (c) The same time series at

yed on the graphic. (d) Power spectrum of the first (full line) and the last (dotted

e series. Proportional power in the 2–4 Hz range for the first and the last 28 s is

give visual information.

A. Legros, A. Beuter / NeuroToxicology 27 (2006) 534–546538

2.3. Field exposure system and data recording

The exposure device was developed by the ‘‘Institut de

Recherche d’Hydro-Quebec’’ (IREQ, Quebec, Canada,

Nguyen et al., 2004) and is detailed elsewhere (Legros and

Beuter, 2005). Briefly, the device generated a continuous and

homogenous sinusoidal 50 Hz MF of 1000 mT centered at the

level of the head (but the trunk and arms were also exposed).

The magnetic flux density was checked at the beginning of each

session. When the MF was generated, the coils produced an

almost imperceptible buzz, which is why the subject and the

experimenter wore ear plugs in addition to an anti-noise helmet.

The ambient geomagnetic field measured in the testing room

with a handheld digital magnetometer mMAG-02WB (Macin-

tyre Electronic Design Associates, Inc., Dulles, USA) was

23 mT along the vertical axis, and 43 mT along the horizontal

axis (total ¼ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi232 þ 432p

¼ 48:76 mT). It was oriented at 238compared with the alternating MF generated by the exposure

device. Background ambient alternating MF was measured

with an EMDEX Lite monitor (ENERTECH Consultants,

Campbell, USA) and was less than 0.01 mT.

Table 1

Due to the counterbalanced protocol used, subjects can have already been exposed

Earlier exposure (min)

Before real

exposure sequence

Before sham

exposure sequence

Low amplitude tremor

Subject 36 8 16

Subject 29 0 8

Subject 12 0 16

Subject 10 0 8

Subject 13 0 0

Subject 11a 0 0

Subject 32 8 8

Subject 16a 8 8

Subject 27a 0 16

Subject 34 8 16

Subject 20 8 0

Subject 25 0 16

Subject 28 0 8

Subject 22a 8 16

High amplitude tremor

Subject 15 8 8

Subject 30b 0 8

Subject 14 8 0

Subject 18b 8 0

Subject 17 8 0

Subject 8 8 8

Subject 33c 0 0

Subject 23 0 0

Subject 31a 0 16

Subject 26 8 16

Overall mean 4 8

This table recapitulates the preceding length of exposure undergone by each subject b

of the changes observed between real and sham exposure sequences for each of the

observed characteristic had a higher value in the real exposure sequence and vicea HVS.b Burst.c Frequency.

Skin temperature and heart rate were monitored during each

recording. Tremor recordings were collected by a data

acquisition system (DOCO Microsystemes, Inc., Montreal,

Quebec) sampled at 1000 Hz. Data were then transferred to

Matlab (The MathWorks, Inc., Natick, USA) for analysis. Data

were first converted from A/D volts to mm (calibration

constant = 3.97). Velocity data were obtained by numerical

differentiation of the raw displacement data. A lowpass filter

removed frequencies above 40 Hz (i.e., high frequency noise)

and a highpass filter below 2 Hz to remove the drift (with FFT

and IFFT). At the end of each of the four sequences, subjects

completed the Field Status Questionnaire (FSQ, Cook et al.,

1992; Crasson et al., 1999) to evaluate whether they were able

to detect the presence of the MF.

2.4. Postural tremor analysis

Briefly, previous work on postural tremor showed: (1) a

possible long term effect of MF exposure (comparing sham and

real exposure sequences) on proportional power in the 2–4 Hz

range, (2) a clear decrease in amplitude between the beginning

to MF or not before their different sequences of test

Difference between exposure conditions real–sham

Amplitude Peakedness Proportional power in

the 2–4 Hz range

+ � +

� + �+ � �� � +

+ + �+ � �� + �+ � +

� � +

+ � +

� + �+ � +

� + �� � +

� + �+ � +

+ � +

+ � +

+ � +

� � +

� � +

� + +

+ � +

� + �

+ � +

efore his real and sham exposure sequences of test. It gives the average direction

three characteristics by taking the difference real-sham (a ‘‘+’’ means that the

versa).

A. Legros, A. Beuter / NeuroToxicology 27 (2006) 534–546 539

and the end of recordings possibly induced by the experimental

procedure (Legros and Beuter, 2005) and (3) a more pronounced

relaxing effect when the MF was present (Legros et al., 2006).

Other results suggested a MF effect on peakedness (but with a

low statistical power). However, further investigations taking

individual subject variability into consideration were needed.

Tremor amplitude is defined as the root mean square of the

filtered (lowpass = 40 Hz, highpass = 2 Hz) position time series

centred on their mean. Peakedness quantifies the shape of the

velocity data (i.e., more peaked or flattened distribution). It is

an adapted version of the fourth statistical moment proposed by

Timmer et al. (1993) and it corresponds to the mean absolute

values of tremor time series (with their mean set to zero). A

regular, symmetric oscillation like a sine wave has a higher

value and Gaussian white noise has a lower value (Edwards and

Beuter, 2000, see Fig. 2). Note that data distribution with

‘‘outliers’’, as would occur with myoclonic-like movements in

finger position would have peakedness values even lower than

Gaussian white noise (Fig. 2). Proportional power in 2–4 Hz

range is the proportion of the power of velocity data contained

in this range compared with the spectrum between 2 and 40 Hz.

Table 2

Directions of the individual changes for amplitude linked with MF exposure

Mean over 8 trials Difference on � off (re

Low amplitude tremor

Subject 36 0.020 �Subject 29 0.020 +

Subject 12 0.021 +

Subject 10 0.023 �Subject 13 0.025 �Subject 11a 0.025 +

Subject 32 0.029 +

Subject 16a 0.030 �Subject 27a 0.031 +

Subject 34 0.033 �Subject 20 0.034 +

Subject 25 0.035 +

Subject 28 0.041 �Subject 22a 0.043 �

High amplitude tremor

Subject 15 0.051 �Subject 30b 0.052 �Subject 14 0.053 �Subject 18b 0.055 +

Subject 17 0.055 +

Subject 8 0.058 �Subject 33c 0.067 �Subject 23 0.070 �Subject 31a 0.080 �Subject 26 0.100 +

Overall mean 0.044 �

Columns present for each subject: (1) the averaged amplitude over the eight record

conditions during real exposure sequence independently of the time course (a ‘‘+’’ m

direction of the changes for an ‘‘off/on’’ transition during real and sham exposure seq

during real and sham exposure sequences, respectively.a HVS.b Burst.c Frequency.

Characteristics were first calculated on the eight A and B

conditions of each sequence (i.e., real and sham exposure, see

Fig. 1b) and then values for equivalent conditions were

averaged (see Fig. 1c).

A graphical representation of the eight recordings of a subject

is presented in Fig. 3 and was made for each subject. It contains

the original tremor position time series (Fig. 3a), the filtered

tremor position time series (between 2 and 40 Hz, see Fig. 3b) at

an adjusted individual scale, the same series at a normalized scale

for all subjects (Fig. 3c), the power spectrum of the position

signal for the first and the last 29 s of the recording (Fig. 3d), and

the same power spectrum for the velocity time series (Fig. 3e).

Corresponding amplitude, proportional power in the 2–4 Hz

range and peakedness are displayed on graphics. To complete

qualitative information given by the figures, four tables have been

provided (Tables 1–4).

3. Results

Heart rate and skin temperature remained stable during all

test sessions. None of the subjects self-described as being MF

al) Off! on On! off

Real Sham Real Sham

& & % %& & & && & & && & & %& % & &% % & %& & & && & % %& & & && & & &% & & && & & &% % % %& % % &

& & % %& & % %& & & && & & && & & %& & & && & & && & & && & & && % & &

& & & &

ings of the session; (2) the direction of the changes between ‘‘off’’ and ‘‘on’’

eans that amplitude was higher in the ‘‘on’’ condition and vice versa); (3)–(4)

uences, respectively; (5)–(6) direction of the changes for an ‘‘on/off’’ transition

A. Legros, A. Beuter / NeuroToxicology 27 (2006) 534–546540

Table 3

Directions of the individual changes for proportional power in the 2–4 Hz range linked with MF exposure

Mean over 8 trials (%) Difference on � off (real) Off! on On! off

Real Sham Real Sham

Low amplitude tremor

Subject 36 7.09 � & % % %Subject 29 6.72 � & & & &Subject 12 9.15 � & & & &Subject 10 4.55 � & & % %Subject 13 5.06 � & % & %Subject 11a 5.59 + % & % %Subject 32 7.48 + % & & %Subject 16a 15.83 � % & % &Subject 27a 7.61 + & & & &Subject 34 7.64 � & & & &Subject 20 4.81 + % % & &Subject 25 8.26 + & % & &Subject 28 4.91 + % % % &Subject 22a 5.66 � & & % &

High amplitude tremor

Subject 15 6.32 � & & % %Subject 30b 7.47 + % % & %Subject 14 7.13 + % & & %Subject 18b 19.88 + % & & %Subject 17 5.78 + & % & %Subject 8 10.26 � & & & &Subject 33c 1.66 � % % % %Subject 23 6.31 � & % & &Subject 31a 17.19 + % & & &Subject 26 10.07 + % & & %

Overall mean 8.02 � & & & &

Columns present for each subject: (1) the averaged proportional power in the 2–4 Hz range over the eight recordings of the session; (2) the direction of the changes

between ‘‘off’’ and ‘‘on’’ conditions during real exposure sequence independently of the time course (a ‘‘+’’ means that proportional power in the 2–4 Hz range was

higher in the ‘‘on’’ condition and vice versa); (3)–(4) direction of the changes for an ‘‘off/on’’ transition during real and sham exposure sequences, respectively; (5)–

(6) direction of the changes for an ‘‘on/off’’ transition during real and sham exposure sequences, respectively.a HVS.b Burst.c Frequency.

hypersensitive and individual responses to the FSQ indicated

that none of them was able to detect the presence of the MF.

However, some subjects noticed unusual diffuse sensations

such as prickling in the fingers (subjects 18, 22, 23, 28 and 32),

blurred vision (subject 29) or even sensation of excessive

salivation (subject 32 again). But these sensations were

described as well in the presence of the MF as in its absence.

Moreover, a Chi-square analysis conducted on the group data

showed that their answers were due to hazard (x2 = 2.16,

d.f. = 7, p = 0.9). No significant Pearson correlation with

r > 0.6 was found between the three analyzed tremor

characteristics.

Individual graphical screening of subjects’ tremor shows a

wide range of between-subject differences, be they in terms of

amplitude or frequency. By the means of the visual examination

of graphical data, four specific behaviors can be identified in

subjects’ tremor time series: (1) high or low averaged

amplitude, (2) high velocity segments (HVS, see Fig. 3), (3)

bursts (see Fig. 4) and (4) unusual frequency content (Fig. 5).

HVS are defined as short, fast movements of the index finger

having at least 1 mm in amplitude and shorter than 0.2 s

(see examples in Figs. 3a and 6). Bursts are defined as a local

increase of the peak-to-peak amplitude observed in the filtered

posture time series (of at least twice the peak-to-peak

background amplitude and lasting at least 5 s).

3.1. Graphical evaluation

Visual inspection of tremor amplitude shows in most of the

subjects lower values during the last 28 s than during the first

28 s of recording. This makes the detection of a MF effect

difficult. Overall mean of tremor amplitude for all subjects is

0.043 mm with a between-subject range of 0.080 mm (Table 1).

Several subjects have HVS which affect the computation of the

characteristics. For example, subject 11 has HVS in three

recordings (Fig. 6). Despite the fact that once it occurs at the

time of MF transition, there is no evidence that it is linked with

MF exposure (see Fig. 6d). HVS are noted in four other subjects

(subjects 16, 27, 22 and 31) and they are also not linked with the

presence, the absence or the transition of the MF. Bursts are

present in two subjects (subjects 18 and 30) and correspond to a

local increase of tremor amplitude. These events were visually

A. Legros, A. Beuter / NeuroToxicology 27 (2006) 534–546 541

Table 4

Directions of the individual changes in peakedness linked with MF exposure

Mean over 8 trials Difference on � off (real) Off! on On! off

Real Sham Real Sham

Low amplitude tremor

Subject 36 0.780 + % % & &Subject 29 0.784 + % % & %Subject 12 0.790 + % & & &Subject 10 0.785 + % & & &Subject 13 0.801 + % & & &Subject 11a 0.789 + & & & &Subject 32 0.758 � & & % &Subject 16a 0.767 + & % & %Subject 27a 0.789 � % % % %Subject 34 0.754 + % % % %Subject 20 0.791 + % % & &Subject 25 0.784 � & & % &Subject 28 0.783 + % % & &Subject 22a 0.772 + % % & %

High amplitude tremor

Subject 15 0.789 + % % & &Subject 30b 0.744 + & & & &Subject 14 0.769 � & & % &Subject 18b 0.763 � % % % &Subject 17 0.784 + % % % %Subject 8 0.781 + % % % %Subject 33c 0.807 + & & & &Subject 23 0.771 + % & % %Subject 31a 0.742 + % % % %Subject 26 0.786 + % % & &

Overall mean 0.778 + % % & %

Columns present for each subject: (1) the averaged peakedness over the eight recordings of the session; (2) the direction of the changes between ‘‘off’’ and ‘‘on’’

conditions during real exposure sequence independently of the time course (a ‘‘+’’ means that peakedness was higher in the ‘‘on’’ condition and vice versa); (3)–(4)

direction of the changes for an ‘‘off/on’’ transition during real and sham exposure sequences, respectively; (5)–(6) direction of the changes for an ‘‘on/off’’ transition

during real and sham exposure sequences, respectively.a HVS.b Burst.c Frequency.

detected by the experimenter during the experimental session.

They occur sometimes in ‘‘off’’, sometimes in ‘‘on’’, some-

times in sham conditions and they do not seem linked with MF

exposure. For subject 33, the frequency content of tremor time

series is very different from other subjects: his tremor is highly

organized around 10 Hz and this is consistent across recordings

(see Fig. 5 for example). MF does not appear to affect his 10 Hz

oscillation.

Following this visual analysis of all subjects’ recordings,

three remarks can be made to orient deeper investigations. First,

subjects have a relatively wide range of tremor amplitude (with

proportions from 1 to 5 between subjects 26 and 36) and have to

be classified in two groups regarding their overall mean

amplitude (above and below 0.043 mm): subjects with high

amplitude tremor and subjects with low amplitude tremor.

Second, the direction of the changes within- and between

subjects has to be individually evaluated for each characteristic.

And third, the specific behaviors of subjects (HVS, bursts and

unusual frequency content) have to be taken into account to

interpret the direction of the changes. Four recapitulative tables

have been made to support this approach: Table 1 summarizes

the direction of the changes between real and sham exposure

sequences for the three characteristics; Tables 2–4 present the

direction of the changes between ‘‘off’’ and ‘‘on’’ conditions

for amplitude, proportional power in the 2–4 Hz range and

peakedness, respectively. Each characteristic is analyzed

separately. Note that all transitions, be they ‘‘off/on’’ or ‘‘on/

off’’, also correspond to a begin/end recording (it is impossible

to record a transition without this time effect).

3.2. Amplitude

For 12 subjects, all corresponding averaged recordings (see

caption of Fig. 1c for details) show a systematic begin/end

decrease in amplitude independent of the MF status (they all

have arrows downwards in Table 2). Twenty-two averaged

transitions concerning 12 subjects show a begin/end increase in

amplitude values and only nine in the real exposure sequence

(during ‘‘off/on’’ transitions for subjects 11, 20, 28 and during

‘‘on/off’’ transitions for subjects 15, 16, 22, 28, 30 and 36, see

Table 2). Each of these exceptions is analyzed regarding the

corresponding graphical representation and results show that

A. Legros, A. Beuter / NeuroToxicology 27 (2006) 534–546542

Fig. 4. Recording 6 of subject 30 (sham). A burst is clearly visible in the second part of the recording (a and b). This event is not linked with MF but it influence

amplitude, peakedness (c) and frequency distribution (d and e).

they are due to the presence of HVS (for subjects 11 and 16), of

bursts (for subjects 30), or more often of small amplitude

fluctuations or tremor irregularities occurring in the last 29 s of

time series (for subjects 10, 13, 15, 17, 20, 26, 28 and 36).

Moreover the increase in amplitude over time during real

exposure is never reproduced from one corresponding

recording to another. Fourteen subjects out of 24 have lower

amplitude during averaged ‘‘on’’ than ‘‘off’’ conditions. But

these differences are very small (below 10 mm, which is near

the laser resolution) except for three high amplitude tremor

subjects: subjects 23, 30 and 31 who have values of �14, �23

and�11 mm, respectively. The reasons are: a smaller amplitude

in the ‘‘on’’ condition of one of the two ‘‘on/off’’ transitions for

subject 23; a burst in the second half of one ‘‘on/off’’ transition

for subject 31; a HVS during an ‘‘off’’ condition for subject 31.

Thus, overall mean amplitudes are lower during the ‘‘on’’

condition. Concerning the differences between real and sham

exposure sequences, half of the subjects have higher amplitude

during real exposure and the other half during sham (Table 1).

3.3. Proportional power in the 2–4 Hz range

As shown previously (Legros and Beuter, 2005), propor-

tional power in the 2–4 Hz range is not significantly affected by

the begin/end effect. Thus, the effect of the MF should be more

visible for this characteristic. Six subjects exhibit similar

tendencies across the different MF conditions: they have all

arrows in Table 3 going in the same direction independently of

MF status (downwards for subjects 8, 12, 27, 29 and 34 and

upwards for subject 33, see Table 3). Four subjects show a

decreased proportional power in the 2–4 Hz range during ‘‘off/

on’’ transition concomitant with an increase during ‘‘on/off’’

transition (subjects 10, 15, 22 and 36). Seven subjects show the

opposite behavior (subjects 14, 18, 20, 26, 30, 31 and 32). But

only three out of these eleven subjects (subjects 14, 15 and 36)

have a consistent behavior between the two corresponding

recordings (tendencies in Table 3 result from their averaging,

see Fig. 1a and b for details). On average, half of the subjects

have higher values during ‘‘on’’ conditions, independently of

their individual specificities (HVS, burst or frequency).

Concerning differences between mean values in real and sham

exposure sequences, only two subjects out of ten have lower

values during real exposure (see Table 1).

3.4. Peakedness

Peakedness is not significantly influenced by the beginning/

end effect (Legros and Beuter, 2005) but its general tendency is

to increase at the end of recordings (except for ‘‘on/off’’

transition under real exposure, see Table 4). Six subjects show a

consistent begin/end tendency independently of the different

MF conditions (four arrows going in the same direction:

A. Legros, A. Beuter / NeuroToxicology 27 (2006) 534–546 543

Fig. 5. Recording 5 of subject 33 (‘‘off/on’’ transition). He exhibits a powerful 10 Hz component in his postural tremor (d and e) which gives a noisy aspect to his

postural tremor time series (a–c). It seems independent of the MF status.

peakedness increases for subjects 8, 17, 27, 31 and 34 and

decreases for subject 33). Thus, if MF had an effect on

peakedness, changes during ‘‘off/on’’ and ‘‘on/off’’ transitions

should go in opposite directions. This is the case for 12 subjects

of whom nine showed an increase of peakedness during ‘‘off/

on’’ and a decrease during ‘‘on/off’’ transitions (subjects 10, 12,

13, 15, 22, 26, 29, 28 and 36). Three show opposite tendencies

(subjects 14, 25 and 32), but only subject 28 shows consistent

tendencies across all the corresponding recordings. On average,

peakedness values are higher during ‘‘on’’ than during ‘‘off’’

conditions for 19 subjects and for only two subjects among the

10 with high amplitude tremor. Eight subjects have higher

peakedness values during real than during sham exposure

condition, but only three among the 10 with high amplitude

tremor.

4. Discussion

We attempted to answer three questions, namely: can we

detect MF effects in human postural tremor? Are some subjects

more responsive to MF exposure than others? Do responsive

subjects all react in the same manner to MF exposure?

First, two types of intermittent behaviors (i.e., HVS and

bursts) were detected in many subjects’ postural tremor. These

events represent superimposed involuntary motor activity and

make it difficult to interpret results. But they are a part of human

behavior and can in turn give information about the possible

MF effects on motor control activity. However, results show

that there is no evidence that MF could produce or modulate

these intermittent behaviors. Nevertheless, we have to take

them into account to understand the results.

Secondly, tremor amplitude decreases between the begin-

ning and the end of a 60 s recording. This phenomenon has

already been shown in previous work (Legros and Beuter, 2005)

and was interpreted as a consequence of the relaxation of the

subject induced by the experimental procedure involving

sensory auditory deprivation (Legros et al., 2006; Lundervold

et al., 1999). This effect is highly consistent within- and

between subjects: only one subject does not exhibit such a

tendency. Moreover, many subjects seem to be more sensitive

than others to the effect of time on postural tremor: four of them

follow the same tendencies with proportional power in the 2–

4 Hz range and peakedness. But subject 33 is an outlier: while

the three other subjects decrease their proportional power in

low frequencies and increase their peakedness, he goes in the

opposite direction. It might be due to his unusual postural

tremor which is highly organized around 10 Hz (other

frequencies are negligible). Thus, when his tremor decreases

in amplitude over time, the 10 Hz oscillations decrease in

power, and consequently other frequencies increase in

proportion (Fig. 2). Concerning peakedness, if a sinusoidal

oscillation is more regular, its peakedness increases: if power of

A. Legros, A. Beuter / NeuroToxicology 27 (2006) 534–546544

Fig. 6. The HVS produced by subject 11 during: (a) a sham recording, (b) an ‘‘off/on’’ transition and (c) an ‘‘on/off’’ transition. (d) The zoom on the raw data (grey

line) and on the lowpass filtered data (40 Hz, dotted line) simultaneously to the ‘‘on/off’’ MF transition shows that the HVS begin before the transition.

the 10 Hz oscillation decreases for subject 33, his tremor is less

‘‘regular’’ and peakedness decreases.

Third, a short term MF effect is difficult to argue (differences

between tremor during ‘‘off’’ and ‘‘on’’ conditions), however

an effect on amplitude and peakedness is possible, especially

for subjects with high amplitude tremor: among the 10 high

amplitude tremor subjects, seven had a lower amplitude and

eight had a higher peakedness in the ‘‘on’’ condition (as seen in

the lower part of the second column of Tables 2 and 4),

independently of the type of transition (‘‘off/on’’ or ‘‘on/off’’).

This is consistent with previous results (Legros and Beuter,

2005) showing a significant MF effect on peakedness and a

non-significant tremor amplitude decrease. MF have also been

shown to accentuate the relaxation effect over time (Legros

et al., 2006).

Fourth, results of proportional power in the 2–4 Hz range

and of peakedness suggest a long term MF effect (i.e.,

differences between tremor during real and sham exposure) for

subjects with high amplitude tremor: the presence of MF for

8 min (two 4-min exposures spaced by 4 min) induces lower

peakedness for seven out of 10 subjects and higher proportional

power in the 2–4 Hz range for eight out of 10 subjects (as shown

by the ‘‘�’’ and the ‘‘+’’, respectively, in the lower part of the

last two columns of Table 1). This also confirms previous

results and shows that these characteristics are sensitive to MF

exposure.

The effect on peakedness was not retained in our previous

work mainly because, on average, it was higher during MF

‘‘on’’ than during MF ‘‘off’’ conditions, but it was lower during

real than during sham exposure and its statistical significance

was small. However, individual analyses presented here suggest

that subjects with high amplitude tremor tend to be more

responsive to MF exposure. Moreover, it is possible that ELF

MF can modulate human motor behavior with different delays

corresponding to different control mechanisms.

Our first assumption was that since MF induces micro-

currents in the central and peripheral nervous system, it could

instantaneously modulate its activity (this is shown for

example by Marino et al., 2004, on an EEG study), and

therefore may act on motor behavior (as shown by Thomas

et al., 2001, on postural sway). But it is also possible that MF

exposure lead to longer term effects. For example, Chen et al.

(1997) showed that TMS at 0.9 Hz during 15 min leads to a

mean decrease of cortical excitability lasting at least 15 min

following the stimulation. More precisely, they showed a

decrease in motor evoked potential amplitude of 19.5%.

According to these authors this result may be due to a change

in the level of depolarization of the postsynaptic neuron, as

shown by Artola et al. (1990) with animal studies. Even if the

physiological basis of these observations is unknown,

Gironell et al. (2002) speculate that it could be the same

mechanism that explains the ‘‘anti-tremor effect’’ they

A. Legros, A. Beuter / NeuroToxicology 27 (2006) 534–546 545

observed in a study showing that repetitive TMS of the

cerebellum improves tremor in patients with essential tremor.

But if this kind of long term effect occurred, the preceding

exposure sequences undergone by subjects would have had an

effect on the following one, and this is not seen in our data

(see Table 1). Cook et al. (2004) showed that the effect of a

200 mT pulsed MF on human EEG disappears after a delay

between 3 and 7 min. If these delays are those involved here,

it could explain the effect between real and sham exposure: in

a real exposure sequence, the MF effect would persist when

MF is turned ‘‘off’’ and could affect the following ‘‘off’’

conditions (before it is turned ‘‘on’’ again, but in a sham

condition its effect would have already disappeared).

Our findings provide a new basis to orient future research.

They show that MF exposure to a 50 Hz, 1000 mT MF could be

detected in human postural tremor, and that some subjects are

more responsive than others. The effects could be detected

immediately during exposure but also after a delay. However

due to the relatively wide range of between-subject variability

and the very subtle within-subject recorded differences, no

clear significant statistical differences exist: a larger sample

size would help to get deeper insight into individual

differences. Moreover, following Cook et al. (2004), real

and sham exposure sessions have to be programmed on two

separate days to avoid perturbations due to the possible

persisting effect of the MF.

To conclude, at the behavioral level of observation explored

in this study, there is no evidence of a potentially harmful effect

of a short exposure to a 50 Hz domestic or industrial MF and

this should be taken into account for establishment of new

exposure limits.

Acknowledgements

We thank the participants, Hydro-Quebec for financial

support (Drs. M. Plante and D. Goulet), and Dr. D. Nguyen for

designing the exposure system. We acknowledge EDF and Dr.

N. Foulquie for subjects’ recruitment, DOCO Microsystemes,

Inc., Montreal, for the data acquisition system and Dr. P.P. Vidal

for his support.

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