Effects of twenty-minute 3G mobile phone irradiation on event related potential components and early...

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Neuroscience 157 (2008) 453–462

FFECTS OF TWENTY-MINUTE 3G MOBILE PHONE IRRADIATION ONVENT RELATED POTENTIAL COMPONENTS AND EARLY GAMMA

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. STEFANICS,a,c G. THURÓCZY,b L. KELLÉNYIa AND. HERNÁDIa*

Department of Experimental Zoology and Neurobiology, University ofécs, 6. Ifjúság str., H-7624, Pécs, Hungary

Department of Non-ionising Radiation, National “Frédéric Joliot-urie” Research Institute for Radiobiology and Radiohygiene, 5 Annatr., H-1221, Budapest, Hungary

Institute for Psychology, Hungarian Academy of Sciences, 83-85 Szonditr., H-1068, Budapest, Hungary

bstract—We investigated the potential effects of 20 minrradiation from a new generation Universal Mobile Telecom-

unication System (UMTS) 3G mobile phone on human eventelated potentials (ERPs) in an auditory oddball paradigm. Indouble-blind task design, subjects were exposed to either

enuine or sham irradiation in two separate sessions. Beforend after irradiation subjects were presented with a randomeries of 50 ms tone burst (frequent standards: 1 kHz, P�0.8,are deviants: 1.5 kHz, P�0.2) at a mean repetition rate of500 ms while electroencephalogram (EEG) was recorded.he subjects’ task was to silently count the appearance ofargets. The amplitude and latency of the N100, N200, P200nd P300 components for targets and standards were ana-yzed in 29 subjects. We found no significant effects of elec-romagnetic field (EMF) irradiation on the amplitude and la-ency of the above ERP components. In order to study pos-ible effects of EMF on attentional processes, we applied aavelet-based time-frequency method to analyze the earlyamma component of brain responses to auditory stimuli.e found that the early evoked gamma activity was insensi-

ive to UMTS RF exposition. Our results support the notion,hat a single 20 min irradiation from new generation 3G mo-ile phones does not induce measurable changes in latencyr amplitude of ERP components or in oscillatory gamma-and activity in an auditory oddball paradigm. © 2008 IBRO.ublished by Elsevier Ltd. All rights reserved.

ey words: EMF, event-related brain potentials, oscillatoryamma band synchronization, RF, UMTS 3G mobile phone.

obile telecommunication is inseparable from our every-ay life. According to estimates by Informa Telecoms &edia (London, UK) the number of individuals with at leastne active mobile subscription was about 2.5 billion by the

Corresponding author. Tel: �36-72-503-607; fax: �36-72-501-517.-mail address: hernadi@ttk.pte.hu (I. Hernádi).bbreviations: ANOVA, analysis of variance; EEG, electroencephalo-ram; EMF, electromagnetic field; ERP, event related potential; ERSP,vent-related spectral perturbation transform; GSM, Global System forobile Communication; ITC, inter-trial phase coherence; MP, mobilehone; SAR, specific absorption ratio; TEOAE, transiently evoked

htoacoustic emission; UMTS, Universal Mobile Telecommunicationystem.

nd of 2007. Due to the proximity of the antenna of theobile phone (MP) handset to the user’s ear and head, therain is inevitably exposed to high frequency electromag-etic fields (EMFs) with a relatively high specific absorptionatio (SAR). Results of experimental radio frequency do-imetry indicate that approximately 40–55% of the MP’sF output power energy is absorbed in the user’s head

Gandhi, 2002).Thus, investigation of potential effects of EMF irradia-

ion from MPs is an important environmental health issue.umerous studies have investigated the potential impactf Global System for Mobile Communication (GSM) MPMF on various brain functions in humans and today there

s a large body of positive and negative findings. In con-rast, there have been no systematic investigations re-orted to date on the possible effects of Universal Mobileelecommunication System (UMTS) EMFs emitted by theew generation (3G) of MPs on event related potentialsERPs) or brain oscillation parameters on medium or largeample of subjects.

Considering earlier studies investigating possible ad-erse effects of MP EMF on the peripheral human auditoryathway and hearing functions, it has been shown that 10in of MP EMF exposure did not induce any changes in

he generation of distortion product otoacoustic emissionsDPOAE) in humans indicating that outer hair cell functionsre unaffected by these exposure conditions (Parazzini etl., 2005).

In a more recent study Paglialonga et al. (2007) ana-yzed transiently evoked otoacoustic emissions (TEOAE)efore and after 10 min of MP EMF and found no signifi-ant change in the temporal and spectral fine structure ofEOAEs after irradiation showing that 10 min exposure toP EMF does not induce measurable changes in cochlear

unctions. Furthermore hearing threshold levels on pureone audiometry and TEOAE were found to be unaffectedy 10 min exposure of EMF (Uloziene et al., 2005). Studies

nvestigating the brainstem auditory evoked potentialsefore and after various MP EMF exposure conditionseported that irradiation did not produce measurable im-ediate changes of auditory brainstem waves I, III and V

Arai et al., 2003; Bak et al., 2003; Oysu et al., 2005;ievert et al., 2005; Stefanics et al., 2007). However, in atudy by Oktay and Dasdag (2006), where no effect ofMF irradiation on brainstem auditory evoked potentialsas observed, a group of long-term MP users still showedigher hearing thresholds compared with moderate usersnd control subjects indicating that a higher degree of

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G. Stefanics et al. / Neuroscience 157 (2008) 453–462454

enerated by MPs. Auditory evoked middle latency re-ponses (Na, Pa, Pb complex) were not affected afterxposure to EMF emitted by a MP for 30 min in the studyy Arai et al. (2003). In contrast, during the presence of MPMF radiation changes in the amplitude of the P50 com-onent (i.e. the Pb complex) of the auditory evoked re-ponse were observed by Papageorgiou et al. (2006).ncrease have been reported in the amplitude of the early0–200 ms) auditory evoked responses in the 30–45 Hzrequency band by Croft et al. (2002), indicating the sen-itivity of the early sensory-specific auditory response toP EMF irradiation. Regarding later components of theuditory evoked response, inconsistent findings have beeneported. Hamblin et al. (2004) observed a decrease in themplitude and latency of the N100 component to non-

arget stimuli with a delay of the P300 latency to targettimuli during exposure to genuine MP EMF relative toham condition. However, a more recent study from theame laboratory (Hamblin et al., 2006) failed to replicatehese earlier findings in a larger sample of subjects and theuthors concluded that there was no evidence indicating

hat acute MP exposure may affect the neural activityesponsible for auditory evoked responses. In a recenteview about neurophysiological effects of MP EMFs onumans Valentini et al. (2007) suggested that irradiationould influence normal physiology via changes in corticalxcitability (Ferreri et al., 2006). In contrast to this, in aecent study (Inomata-Terada et al., 2007) neither motorvoked potentials (MEPs) to single pulse transcranial mag-etic stimulation (TMS), nor the short interval intracortical

nhibition (SICI) was affected by 30 min of MP EMF expo-ure. In fact, unreplicated positive findings are not uncom-on in the field of research about MP EMF’s effects onuman brain functions. According to Krause et al. (2006)MF effects on the electroencephalogram (EEG) may beariable and not easily replicable for unknown reasons. As itas been repeatedly pointed out (Krause et al., 2006) that thexisting unsystematic observations in the field indicate theeed of further experimentation, in our study we set out to

nvestigate the potential effects of 20 min irradiation from neweneration 3G MP on ERPs in auditory oddball paradigm. Insimple auditory oddball paradigm, frequent standard and

are target stimuli are presented to the subjects and evokeRPs which are recorded by EEG. Standard stimuli evokeRP components known as N100, P200 and N200, whereas

argets additionally elicit the P300 ERP component. As theeneration of the P300 involves attention- and memory-re-

ated operations in a distributed network of brain processesBledowski et al., 2004; Polich, 2007) it allows the investiga-ion of possible effects of MP EMF on these processes. Ourtudy procedure closely followed the protocol of the auditoryddball task of Hamblin et al. (2006) to ensure comparabilityf the results though the UMTS 3G MP used in our studyiffered from the GSM MP used by Hamblin et al. (2006).

The UMTS 3G phone system has markedly differentF signals compared with the GSM system. While theSM RF signal represents a pulse modulation with 217 Hz

epetitive frequency, the UMTS signal is similar to a ran-

uency with 5 MHz bandwidth. As the GSM system haslready been tested for immediate effects, and there is aajor difference in the nature of the two RF systems, it isecessary to investigate the possible effects of the UMTSignal on auditory function in a similar testing paradigm.

It has been suggested that the early evoked (phase-ocked) gamma activity mediates attention toward targettimuli (Engel et al., 2001; Fell et al., 2003; Herrmannt al., 2004). Several studies have reported that auditoryTiitinen et al., 1993; Yordanova et al., 1997; Debener etl., 2003; Edwards et al., 2005) and visual (Herrmann etl., 1999) target stimuli evoke larger early gamma-bandesponse than non-target stimuli. The early gamma-bandomponent (Galambos et al., 1981; Pantev et al., 1991) ofhe auditory evoked response occurs in the time window ofhe middle latency responses including the P50 compo-ent, however the origin and the mechanism generating

he gamma response are not yet fully understood (Ber-rand and Tallon-Baudry, 2000). Papageorgiou et al.2006) reported that MP EMF exposure modulated themplitude of the P50 wave and the results of Croft et al.2002) indicated that irradiation increased total EEG powerf the auditory evoked response within the 200 ms timeindow following stimulus onset in 30–45 Hz frequencyand.

As the use of the new generation (UMTS 3G) MPs isast spreading worldwide, and data concerning their pos-ible acute effects on human cognitive function represent aeed for further experiments in our current study we set out

o test possible effects of these MPs on ERP componentsvoked by standard and target tones in an auditory odd-all paradigm. Furthermore, as it is not clear whetherhanges in the amplitude of the early gamma-band re-ponse found in previous studies (Croft et al., 2002; Pa-ageorgiou et al., 2006) were caused by modulation ofither the phase-locking or the power of the evoked re-ponse, in the present study we separately analyzed thehase stability of the early gamma response across trialsnd the total power of the early evoked gamma activity.

EXPERIMENTAL PROCEDURES

ubjects

e recorded EEG from 36 healthy university students (aged9–28 years (mean 23.08), 20 females). None of the subjects hadny history of neurological or hearing disorders. The protocol of

he study was approved by the Ethical Committee of the Universityf Pécs. The recordings were carried out at the Electrophysiolog-

cal Laboratory of the Department of Experimental Zoology andeurobiology, University of Pécs, Hungary. All subjects gave theirritten informed consent after the nature of the experiment hadeen fully explained.

udiometry

he hearing status of all participants for the exposed ear waseasured for air-conducted sound stimuli at seven standard au-iometric frequencies (250 Hz, 500 Hz, 1 kHz, 2 kHz, 4 kHz, 6Hz, 8 kHz). Patch antenna was attached over the right ear.earing thresholds on the exposed ear were measured beforend after the EEG recording Block 1 and Block 2, respectively.

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G. Stefanics et al. / Neuroscience 157 (2008) 453–462 455

ncluded in the final ERP analysis were no worse than 20 dB at thetandard audiometric frequencies. The effects of experimental con-itions were analyzed with three-way repeated-measures analysesf variance (ANOVA of SESSION [Genuine vs. Sham]�BLOCK

Block 1 vs. Block 2]�FREQUENCY [250 Hz vs. 500 Hz vs. 1 kHz vs.kHz vs. 4 kHz vs. 6 kHz vs. 8 kHz]) on audiometric values.

timuli and procedure

wo pure tones (50-ms duration with 5-ms rise and 5-ms fall times)erved as frequent standard (1 kHz, P�0.8) and rare targets (1.5Hz, P�0.2). Stimulus-onset asynchrony was randomly varied be-ween 1000 and 2000 ms with a mean of 1500 ms. The tones wereelivered in a randomized order with at least one standard separatingonsecutive target tones. Auditory stimuli were presented binaurallyia headphones at 70 dB SPL The subjects’ task was to silently counthe appearance of target tones. A total of 400 responses wereollected from each subject per recording-block.

All subjects took part in two recording blocks (Block 1 followedy Block 2) per session on two sessions separated 1 week apart.etween the two recording blocks, subjects were exposed toither genuine or sham MP EMF irradiation for 20 min in a double-lind design. The order of the genuine and sham MP EMF expo-ure sessions was counterbalanced across subjects.

xposure device and conditions

xposure was administered by means of a standard Nokia 6650P via external software control for 20 min. The MP was con-ected to an external patch antenna, which was mounted on alastic headset in a position similar to that of a MP handset duringormal use. As for applicator a single sided round dual band patchntenna made by Reinheimer Elektronik (Wettenberg, Germany;odel: M30EXO-0250-03-XX) was used in order to enhance the

ocal exposure in the ear region. The 31 mm diameter 0.5 mmhick antenna has been encapsulated in a 40 mm diameter 7 mmhick transparent plastic capsule. The capsule did not have anyignificant effect on the antenna’s radiation pattern or effective-ess. The non-metallic side of the antenna was designated to be

he application side. The covering case on this side was 1 mmhick.

The UMTS signal from the MP, controlled by Phoenix softwareNokia), was fed into a UMTS uplink-band amplifier, equipped with aurpose-build switch allowing for real versus sham exposures. Neareld measurements were performed on a phantom head, and thexposure parameters were controlled so that they remained below

he maximum levels authorized by the EEC recommendations, at thenner ear level. The exposure level was set relatively high, and it wasontinuously monitored and kept below the highest level allowed byU recommendation (EU, 1999) preventing substantial temperature

ncrease around the exposed surface.The maximum SAR (averaged over 1 g of mass), at a dis-

ance of 30 mm from the surface of the phantom was 0.39 W/kg.he maximum measured SAR over 1 g was 1.75 W/kg, thestimated skin levels at outer ear were 3.75 W/kg. This estimationas based on the numerical extension of the SAR measurements

n the CENELEC standardized head phantom (CENELEC, 2002).he averaged SAR over 10 g was set below 2 W/kg in any positionithin the phantom meeting the limit of public exposure to RF

equested by the 1999/519/EC Recommendation (EU, 1999).

able 1. Time windows defined for amplitude and peak latency meas

Standard

eak and measurement site N100 (Cz) P200 (Cz) Nverage peak latency (ms) 91 187 2mplitude interval (ms) 81–101 172–202 2

EG recording

EG was recorded from Fz, Cz and Pz sites (according to thenternational 10–20 system) and EOG from two channels placedbove and below the left and right outer canthi, respectively. EEGas referred to linked mastoids, the forehead served as ground.lectrode impedances were kept below 5 kohm. Recording wasontinuous with an analog band-pass from 0.16 Hz to 150 Hz at aampling rate of 1 kHz.

ata analysis

ERPs. For ERP analysis, continuous data were band-passltered between 0.5 Hz and 20 Hz and we extracted epochs from100–600 ms. After epoching, trials with a potential changeelow 0.1 �V or voltage exceeding �75 �V were rejected from

urther analysis. The accepted minimum target trial number was0. Due to excessive artifacts in any of the four recordings, sevenubjects’ data were excluded from further analysis. Epochs wereaseline-corrected for the 100-ms pre-stimulus period and aver-ged separately for standard and target stimuli and for the fourxperimental conditions. After averaging, four components of thevoked brain response were visually identified: N100, N200, P200nd P300 peaks. Component amplitudes were measured relative

o the pre-stimulus period and peak latencies were defined as theinimum and maximum points for N100, N200 and P200, P300

omponents, respectively. Time windows defined for amplitudend peak latency measurements are listed in Table 1. The effectsf experimental conditions were analyzed with three-way repea-

ed-measures ANOVA (ANOVA of SESSION [Genuine vs.ham]�BLOCK [Block 1 vs. Block 2]�ELECTRODE [Fz vs. Czs. Pz]). Greenhouse-Geisser correction of the degrees of free-om was applied where appropriate and � values are given inable 2.

Evoked gamma power and inter-trial phase coherence (ITC).voked gamma activity was analyzed by applying wavelet trans-

ormation on the averaged evoked potential waveforms. This anal-sis reveals the amplitude of gamma-band response that ishase-locked to the stimulus. Furthermore the wavelet transfor-ation was applied on single-trial data in order to reveal the phase

tability of the gamma response across trials. The differenceetween the two measures lies in the fact that the analysis of theveraged evoked potential waveforms reflects the amplitude of

he total activity for a given frequency range whereas analysis ofTC reveals phase-locking independent of the amplitude of theEG signal (e.g. Tallon-Baudry et al., 1996; Debener et al., 2003).ata processing was carried out using the interactive EEGLAB

oolbox for Matlab (Delorme and Makeig, 2004).For the analysis of gamma activity we extracted epochs from

400–1200 ms. After epoching, trials with either a potentialhange below 0.1 �V or with a potential exceeding �75 �V wereejected from further analysis. The accepted minimum target trialumber in a single block was 50. For each subject a number oftandard trials corresponding to the number of target trials wereelected for analysis. Due to excessive artifacts in any of the fourecordings, two additional subjects’ data were excluded from fur-her analysis leaving 27 subjects’ data for time-frequency analysis.

Power changes in the averaged evoked potentials relative tohe baseline period were studied by computing event-related

Target

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pectral perturbation transforms (ERSP, Makeig, 1993). ERSPime-frequency matrices show changes from the spectral poweraseline, allowing the study of the time-course of the EEG signalnergy, separately for each frequency. This method generalizes

he narrow-band measures of event-related synchronization andesynchronization as introduced by Pfurtscheller and Aranibar1977) and described in detail by Delorme and Makeig (2004).

ITC was analyzed on single-trial data. ITC is a measure ofhase synchronization across trials taking values between 0 and. Higher values indicate more precise phase synchronizationetween EEG data and the time locking events (Delorme andakeig, 2004).

Analysis of gamma responses was carried out using Morletavelets of three cycles at 10 Hz with increasing cycles at higher

requencies to 100 Hz. Data contained samples from �400 msefore to 1200 ms after the stimulus events. The window size was35 ms wide and it was applied 200 times at an average step sizef 6 ms. The ERSP time-frequency matrices were baseline cor-ected by the average power calculated from the �100-0 msre-stimulus period.

For statistical analysis of the power of evoked gamma activitynd ITC, a window of 60 ms duration was selected in the 30–0 Hz frequency range. The window was centered on the peak ofamma-band activity in the grand-averaged responses at Cz elec-

rode, which was observable both for ERSP and ITC measures.he effects of experimental conditions were analyzed with four-ay repeated-measures ANOVA on the measures of gammactivity separately (ANOVA of TYPE [Target vs. Standard]�ESSION [Genuine vs. Sham]�BLOCK [Block 1 vs. Block 2]�LECTRODE [Fz vs. Cz vs. Pz]). Greenhouse-Geisser correctionf the degrees of freedom was applied where appropriate, and �alues are given in the text. Main effects and interactions wereurther specified by post hoc Tukey HSD tests.

RESULTS

ehavioral and audiometric results

e quantified behavioral data by calculating the percentagef correctly counted target stimuli for each block. To this end,eported counts for targets were subtracted from the numberf targets, and multiplied by 100/number of targets. Theverall error rate was 3.2%. The analysis of the percentagecores for each block (ANOVA of SESSION [Genuine vs.ham]�BLOCK [Block 1 vs. Block 2]) yielded no significantffects or interactions (all P�0.30).

Statistical analysis of hearing thresholds levels preced-ng and following genuine/sham MP EMF irradiationANOVA of SESSION [Genuine vs. Sham]�BLOCK [Block 1s. Block 2]�FREQUENCY [250 Hz vs. 500 Hz vs. 1 kHzs. 2 kHz vs. 4 kHz vs. 6 kHz vs. 8 kHz]) revealed aignificant main effect of FREQUENCY (F(6, 168)�29.07,�0.001, ��0.5), mainly showing descending hearing

hresholds from low to higher audiometric frequencies.owever, no other effects or interactions indicated signif-

cant effect related to either MP EMF exposition or to therder of different sessions (SHAM vs. GENUINE).

ig. 1 shows grand-averaged ERPs elicited by deviant andtandard tones at the three electrode locations (Fz, Cz,z). Both stimuli evoked the N100, N200 and P200 com-

ponents, and targets evoked the P300 response. Signifi-Tab

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ant main effects related to variations between recordingsnd topographical differences are listed in Table 2.

We have found no significant effect of EMF irradiationondition (SESSION) on the amplitude or latency of any ofhe identified ERP components (N100, N200, P200, P300).hough the analysis of the latency of the N100 componentvoked by target stimuli indicated a significant SESSION�LOCK interaction, post hoc Tukey HSD comparison cor-

ecting for type I error did not reveal significant differencesetween conditions.

amma activity

ur results revealed a prominent evoked gamma bandesponse which rose shortly after the onset of both stimu-us types and peaked at �70 ms at �44 Hz (Fig. 2).NOVA of TYPE (Target vs. Standard)�SESSION

Genuine vs. Sham]�BLOCK (Block 1 vs. Block 2)�LECTRODE (Fz vs. Cz vs. Pz) of evoked gamma activity

ig. 1. Grand-average ERP waveforms evoked by target (left column)voked the N100, P200, N200 and P300 components, however we foRP components.

n the 30–50 Hz and 40–100 ms time-frequency window B

evealed a significantly higher gamma amplitude for tar-ets (F(1, 26)�4.79, P�0.05, ��0.16). A main effect ofLECTRODE was observed (F(2, 52)�8.4, P�0.001,�0.81). Post hoc analysis revealed that the evokedamma amplitude was significantly higher at Cz electrode

han at Fz and Pz electrodes (P�0.03). Furthermore, aignificant TYPE�BLOCK interaction (F(1, 26)�8.36,�0.01) was observed which was caused by significantlyigher evoked gamma amplitude for targets compared withtandards in the first block (P�0.01) as revealed by postoc Tukey HSD comparison. No other effects or interac-

ions reached the level of significance.ITC analysis revealed a peak in phase-locking both for

argets and standards in the gamma frequency range at70 ms post stimulus at �40 Hz (Fig. 3). For statisticalnalysis a time-frequency window in the 30–50 Hz and0 –100 ms intervals was selected. ANOVA of TYPETarget vs. Standard)�SESSION [Genuine vs. Sham]�

dard (right column) stimuli at Fz, Cz and Pz sites. As expected, stimuliffect of MP EMF exposure on the latency and amplitude of any of the

and stan

LOCK (Before vs. After)�ELECTRODE (Fz vs. Cz vs.

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z) of ITC measures yielded solely a significant main effectf ELECTRODE (F(2, 52)�17.5, P�0.001, ��0.94). Post

ig. 2. Grand-averaged ERSP time-frequency matrices calculated by wan total power compared with the baseline period. The signal power (in darmer colors representing higher power values (color bar at the right sarked by white boxes.

ig. 3. Grand-averaged time-frequency plots showing phase-locking (I

oc test showed that phase-locking values were signifi-antly higher at Cz than at Fz, and phase locking was

ed analysis of the averaged evoked potentials showing relative changese to the pre-stimulus baseline (�100-0 ms) is shown by color code with

bottom panel). The time-frequency window used for measurements is

s for targets (left column) and standards (right column). Phase-locking

velet-basB) relativ

TC) value

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DISCUSSION

ehavior and audiometry

n our experiment, subjects easily detected the targetones. Analysis of behavioral data collected before andfter genuine and sham MP EMF irradiation indicated noffect of EMF exposure on task performance. Audiometric

ests of hearing threshold levels before and after genuinend sham MP EMF exposure also failed to indicate anytatistically significant changes in the hearing functionsue to MP EMF exposure.

esults of our current investigation indicate that a single 20in irradiation from 3G MPs does not induce measurable

hanges in the latency and amplitude of the N100, N200,200 and P300 ERP components. This negative finding isorroborated by the behavioral data also indicating no

nfluence of MP EMF on subjects’ performance to detectnd count target tones. This is in accordance with recentesults of Hamblin et al. (2006) where the authors collectedata from a large sample of subjects (n�120) and found noffect of GSM exposure on behavioral and electrophysio-

ogical measures. The present data are also in line withreliminary results obtained parallel with our study byleinlogel et al. (2008), where the authors studied EEGicrostates around the P100 component measured dur-

ng a visual checkerboard stimulation, the N100 from aassive auditory paradigm and P300 components fromn auditory oddball and a continuous performance task

n 15 young male subjects. The authors found no effectsf low levels (0.1 or 1 W/kg SAR) of GSM or UMTS 3Gxposure on the above EEG microstates, furthermoreehavioral performance parameters were also unaf-

ected by irradiation.In the present study, the main effects on latencies and

mplitudes of N100, P200, N200 and P300 componentselated to variations between recording blocks and elec-rode sites are in good agreement with most of the obser-ations reported in the literature. We observed a significantecrease of the N100 amplitude over repeated blocks both

or target and standard stimuli. A similar finding was re-orted by Carrillo-de-la-Pena et al. (1999) for standardsnd the authors suggested that this effect indicated habit-ation to the stimuli reflected by a general decrease inrousal level. Although N100 for targets previously was

ound to be unaffected by repetition (Romero and Polich,996), our results show that habituation is not restricted totandard stimuli but affects the amplitude of the N100omponent evoked by targets as well.

The significant differences found between frontal, cen-ral and parietal sites in both the N100 and P200 ampli-udes were further analyzed by Tukey HSD post hoc tests.esults revealed the amplitude gradient Cz�Fz�Pz for

he N100 component and Cz�Pz�Fz for P200 component

revious results reported by Carrillo-de-la-Pena et al.1999).

Furthermore, we observed a reduction in the amplitudef the N200 component to standards between the first andecond blocks which may reflect a decrease in the arousal

evel. The amplitude of the N200 component to standardshowed the gradient [Fz, Cz]�Pz and the N200 latencyisplayed a pattern of Pz�Cz�Fz gradient. That is, N200mplitude to standards increased from parietal to frontallectrodes, whereas N200 latency increased from frontal

o parietal sites. The latency of N200 evoked by targetsncreased from the first to the second block while it wasnaffected by the exposure to EMF. A compatible obser-ation of increase in latency of N200 to targets with in-reasing trial blocks was reported by Polich (1989). N200mplitude to targets showed the gradient Pz�Cz�Fzhich pattern is the opposite to the results of Carrillo-de-

a-Pena et al. (1999) whereas N200 latencies were longert Fz and Cz than at Pz, which is in good agreement withrevious findings (Lew and Polich, 1993; Carrillo-de-la-ena et al., 1999). In contrast to standards, N200 ampli-

ude to targets decreased from parietal to frontal sites,hereas N200 latency decreased from frontal to parietallectrodes.

P300 amplitude decreased from the first to secondlocks which is a thoroughly studied phenomenon related

o habituation (Polich, 1989; Romero and Polich, 1999; Linnd Polich, 1999; Ravden and Polich, 1999; Pan et al.,000). P300 amplitude is sensitive to the development ofutomaticity (Lew and Polich, 1993) and may reflect theeduction of attentional resources required to the comple-ion of the task. P300 amplitude showed a Pz�Cz�Fzradient similarly to results reported by Ji et al. (1999),avden and Polich (1999), Polich and Bondurant (1997)nd Carrillo-de-la-Pena et al. (1999). P300 latencies were

onger at Fz than at Cz and Pz sites, which pattern is ingreement with the results of Polich and Bondurant (1997).

arly gamma activity

ur findings related to the power of early evoked gammactivity are in line with and replicate previous observationsbout target stimuli evoking stronger gamma-band re-ponse than unattended standards (Tiitinen et al., 1993;ordanova et al., 1997; Debener et al., 2003; Edwards etl., 2005). In the visual modality, early gamma activity wasuggested to play a role of an early interface betweenottom-up and top-down processes (Busch et al., 2006).ccording to the match-and-utilization model of Herrmannt al. (2004), the early gamma-band response plays a role

n the process of matching of bottom-up signals with mem-ry contents and correspondence leads to the enhance-ent of the early gamma responses. The early gammactivity is generated at least partially in the auditory cortexPantev et al., 1991) by feature-selective neural assem-lies (Schadow et al., 2007) and it can be modulated byttentional processes (Tiitinen et al., 1993; Yordanova etl., 1997; Debener et al., 2003; Edwards et al., 2005). Inur study, targets evoked significantly higher gamma-band

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ower of the gamma-band response evoked by targetsecreased which may indicate a decline in the amount ofttentional resources allocated to the task.

However, we found no effect of MP EMF irradiation onhe magnitude of the early gamma activity, in contrast tohe results reported by Papageorgiou et al. (2006) androft et al. (2002). In the study by Papageorgiou et al.

2006) subjects were evaluated with an auditory digit spanest. Tones signaled the beginning and the end of the digitist which had to be memorized. There were two tonesiffering in frequency, the low tone indicating that the num-ers had to be recalled in the same order as presented,hereas the high tone signaled that subjects had to recall

he numbers in the opposite order. The authors found thathe amplitude of the P50 component evoked by the lowone increased during the presence of MP EMF comparedith sham irradiation, at Fp1 and O1 electrodes, whereas

he amplitude of the P50 evoked by the high tone de-reased at the Fp1 position only during MP EMF irradia-ion. The authors suggested that MPs affect pre-attentivenformation processing. There are several differences be-ween their study (Papageorgiou et al., 2006) and ours inhe experimental methodology and design, which may ac-ount for the discrepancy between their previous resultsnd the present data.

As the P50 component originates in the auditory cortexlong the Heschl’s gyrus (Huotilainen et al., 1998; Borg-ann et al., 2001) and P50 is known as a sensory-specific

esponse, it would be more reasonable to expect possiblenfluences of MP EMF at fronto-central electrode sitesather than at Fp1 or O1. As fronto-central positions areore sensitive to P50 generator sources, they should bet-

er reflect possible changes in pre-attentive informationrocessing.

The auditory gamma-band response which we studiedere was suggested to occur in parallel with the P50esponse (Galambos et al., 1981; Pantev et al., 1991) andt was demonstrated to mediate attentional processes (Ti-tinen et al., 1993; Yordanova et al., 1997; Debener et al.,003; Edwards et al., 2005). However, we found it unaf-

ected by a single 20 min MP EMF. Croft et al. (2002)eported an increase in the power of gamma-band re-ponses in the 30–45 Hz band to auditory stimuli in a–200 ms poststimulus time window at midline frontal and

ateral posterior sites during MP EMF exposure in an au-itory discrimination task. There are again several differ-nces between their study (Croft et al., 2002) and ours in

he experimental methodology and design which may ac-ount for the discrepancy between their results and ours.

Theoretically, changes in phase-locking or in thetrength of the neural generators of the evoked brain re-ponses may lead to alterations in the magnitude of thevoked response. In the present study, we analyzed these

wo factors separately and we found no evidence that MPMF would influence them. We are not aware of any othertudies so far directly addressing the issue of possibleffects of MP EMF on phase-locking.

Our current results suggest that 20 min MP EMF ex-

elated to the precise timing of the early gamma-bandesponse. Furthermore, Arai et al. (2003) studied the ef-ects of 30 min EMF emitted by a MP on auditory evokediddle latency responses, including the P50 componentnd found no effect of exposure which is compatible withur current negative result. Behavioral effects of MP EMFn attention were tested in the study by Russo et al. (2006)

n a large sample of volunteers in a simple reaction task, aigilance task, and a subtraction task and the authorsound no significant effects of exposure on performance.his is consistent with the behavioral results by Croft et al.

2002) and Papageorgiou et al. (2006) where no changesn behavioral performance were reported. In general, whenehavioral data are available, electrophysiological mea-ures are easier to interpret within the context of an infor-ation-processing model (Picton et al., 2000).

Though our current behavioral and various electro-hysiological results suggest that 20 min MP EMF doesot induce measurable changes in the early gamma-bandesponse in a simple auditory oddball paradigm, we wish tomphasize that differences in experimental methodologynd design can be an explanation for the discrepancyetween the results of studies reporting effects of MP EMFn brain responses related to early attentional mecha-isms (Croft et al., 2002; Papageorgiou et al., 2006) andur current results.

While our current negative results indicate that auditoryRPs and early gamma response were not affected sig-ificantly by 20 min MP EMF, it should be kept in mind that

he present results were obtained from a young andealthy population of university students volunteering inur study. We suggest, that further studies should test theossible effects of MP EMF in different healthy subgroups,.g. in children, adolescents or elderly and possibly variousroups of neurological patients should be involved in future

nvestigations as they might be more vulnerable due topecific deficits. Furthermore, the lack of significant acuteffects of MP EMF studied usually in young and healthyolunteers, does not indicate the non-existence of possibleccumulating effects of long term cell phone usage.

CONCLUSION

n summary, in our study we replicated previous findings ofo effect of MP EMF exposure on the amplitude and

atency of N100, N200, P200 and P300 auditory evokedesponses. Furthermore, brain mechanisms of auditoryelective attention reflected by the early gamma-band re-ponse were not found to be affected by a single 20 minP EMF exposure to the new generation (3G) MP EMF.

cknowledgments—This work was supported by the Europeanommission–Framework of the Programme of Community Action

n the Field of Public Health of the EC DG Health and Consumerrotection, EMFnEAR Project, Contract No.: 2004127.

We thank Ildikó Jacsó, Annamária Steinbach and Mirtillakács for their help in data acquisition. We are grateful tohomas Wehmeier at Informa Telecoms & Media for providing usith up-to-date numbers of unique mobile users and to Profs.

stván Czigler and István Winkler for valuable comments on data

nalysis. István Hernádi was in receipt of the Bolyai Researchellowship of the Hungarian Academy of Sciences.

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(Accepted 28 August 2008)(Available online 9 September 2008)

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