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ABioelectromagnetics 00:1^8 (2005)

Effects of Radiofrequency Radiation Emitted ByCellularTelephones, on the Cognitive

Functions of Humans

Ilan Eliyahu,1* Roy Luria,2 Ronen Hareuveny,1 Menachem Margaliot,1

Nachshon Meiran,2 and Gad Shani3

1Radiation Safety Division Soreq NRC,Yavne, Israel2Department of Behavioral Sciences, Ben-GurionUniversity, Beer-Sheva, Israel

3Department of Biomedical Engineering, Ben-GurionUniversity, Beer-Sheva, Israel

The present study examined the effects of exposure to Electromagnetic Radiation emitted by astandard GSM phone at 890 MHz on human cognitive functions. This study attempted to establish aconnection between the exposure of a specific area of the brain and the cognitive functions associatedwith that area. A total of 36 healthy right-handed male subjects performed four distinct cognitive tasks:spatial item recognition, verbal item recognition, and two spatial compatibility tasks. Tasks werechosen according to the brain side they are assumed to activate. All subjects performed the tasks underthree exposure conditions: right side, left side, and sham exposure. The phones were controlled by abase station simulator and operated at their full power. We have recorded the reaction times (RTs) andaccuracy of the responses. The experiments consisted of two sections, of 1 h each, with a 5 min break inbetween. The tasks and the exposure regimes were counterbalanced. The results indicated that theexposure of the left side of the brain slows down the left-hand response time, in the second—later—part of the experiment. This effect was apparent in three of the four tasks, and was highly significant inonly one of the tests. The exposure intensity and its duration exceeded the common exposure ofcellular phone users. Bioelectromagnetics 00:1–8, 2005. � 2005 Wiley-Liss, Inc.

Key words: cognitive function ability; left hemisphere; right hemisphere; GSM

INTRODUCTION

The dramatic increase in cellular phones usageraises the question of the existence of possiblebiological effects of radio-frequency electromagneticradiation (RFR) [Stewart, 2000]. Although the effectsof the utilized frequencies (�0.9 and �1.8 GHz) havebeen studied before, two new developments in cellulartechnology warrant our attention:

1. Never before have so many people (especiallychildren) been exposed to RFR, at non-negligibleintensities with such proximity to the head(although within permitted levels according toIRPA/ICNIRP, 1998, FCC, 1996, CENLEC, 2001exposure standards).

2. Most modern cellular systems operate in a pulsatingmode in which the data is accumulated andtransmitted in short pulses. Such modulated RFRat low average power has been reported to haveeffects on the central nervous system [Bawin et al.,1975; Blackman et al., 1979, 1980].

Several recent studies on the effects of exposure toRFR from cellular phones report that exposure to900 MHz has an identifiable effect on electroencephalo-gram (EEG). Klaus and Joachim [1996] found changesin the EEG pattern of sleeping subjects during theexposure to GSM RFR. The radiation source in the saidreport had an 8 W output and the power density at thehead was estimated to be 0.05 mW/cm2. The subjectswere exposed for 8 h from one side only. Further studies[Wagner et al., 1998] tried, but failed, to replicate theresults of this study.

A study by Krause et al. [2000] tested the effects ofGSM cellular phone on the EEG during an auditory

12005Wiley-Liss, Inc. BEM/809M-04(20187)

——————*Correspondence to: Ilan Eliyahu, Radiation Safety DivisionSoreq NRC, Yavne 81800, Israel. E-mail: ilan@soreq.gov.il

Received for review 29 November 2004; Final revision received30 June 2005

DOI 10.1002/bem.20187Published online in Wiley InterScience(www.interscience.wiley.com).

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Amemory test. A standard GSM phone (at 902 MHz) wasattached to the right posterior temporal region of thehead under two exposure conditions: on or off. Theirfindings indicated that EMF decreased the theta bandactivity only during their memory retrieval task, andincreased the alpha band activity. However, a repli-cation study by Krause et al. [2004] did not confirmthese findings.

An epidemiological study by Oftedal et al. [2000]in Sweden and Norway looked for symptoms such asheadaches, feelings of discomfort or warmth behind/around the ear in GSM users and NMT users. Theirresults indicated that mobile phone users experienced avariety of symptoms either during or shortly after aphone call. A study by Koivisto et al. [2001] comparedsubjective symptoms or sensations, such as head aches,dizziness, fatigue, itching, tingling of the skin, rednessand sensations of warmth on the skin in two groups of 48subjects, who were exposed to RFR for 30–60 min.Their results did not reveal significant differencesbetween the exposure and non-exposure conditions.

The effects of RFR on cognitive functions wereexamined in several studies. Preece et al. [1999]conducted tests on a variety of short-term and long-term memory tasks, and reaction time (RT) tests. Thesubjects were exposed to RFR at 915 MHz (1 and0.25 W powers). They reported a reduction in RT, withthe shortest response time when the subjects wereexposed to 915 MHz at 1 W.

Similar tests were conducted by Koivisto et al.[2000a]: 12 different RT tests were conducted under theexposure to 902 MHz at 0.25 W. In three of the tests, areduction in the RT was observed. Another study byKoivisto et al. [2000b] examined the effects on theworking memory, and revealed a reduction in RT underexposure to 902 MHz at 0.25 W.

In two replications and an extension study done byHaarala et al. 2003, 2004, 64 subjects in two differentlaboratories in Finland and Sweden performed double-blind cognitive and short-term memory tasks. Thephone was attached to the left side of the head. Nostatistically significant differences were found betweenlaboratories, and they did not replicate the Koivistoet al. [2000a,b] results.

The Present Study

The goal of the present study was to examinewhether RFR can affect cognitive functions. Thesubjects were asked to perform four different taskswhile being exposed to different RFR condition. Thetasks chosen were those that are known to have highhemisphere specificity, i.e., they activate mostly oneside of the brain (see Smith and Joindes, 1999 for areview article). The four tasks were a verbal item

recognition task (left side), a spatial item recognitiontask (right side), and two spatial compatibility tasks (theleft compatible stimuli activate the right side, while theright compatible stimuli activate the left side).

Subjects were exposed to RFR alternatively to theleft side, to the right side and sham exposed. To the bestof our knowledge this is the first study that compareseffects of exposure to the two head sides within thesame task. This allows us to test the hypothesis of thepresent work, that performance of specific tasks isaffected by one side exposures only.

MATERIALS AND METHODS

Thirty-six healthy right-handed male subjectswere chosen. The mean age was 24 years, ranging from19 to 27. The experiment was approved by the Ben-Gurion University Medical School Ethical Committee(Beer–Sheva, Israel). The subjects gave an informedwritten consent. The subjects completed a question-naire concerning intakes of tea, coffee, alcohol and theamount of sleep they had prior to the experiment. Theparticipants reported adequate sleep in the night prior tothe experiment, and they did not drink excessively oruse CNS-affecting drugs.

Cognitive Tasks

The subjects were requested to perform fourdifferent tasks. The examined parameters were theresponse time (RTs) and the percentage of erroneousresponses made by the subjects. In all tasks, subjectswere instructed to react to the stimuli presented on acomputer screen by pressing given buttons (‘‘/’’—usingthe index finger of their right hand or ‘‘z’’—using theindex finger of their left hand) on the computerkeyboard as quickly and accurately as possible.

As differentiation between hemispheres was oneof the objects of the present study, the tasks chosen werethose for which hemisphere differentiation is wellestablished.

The tasks were coded as follows:

Spatial item recognition task—‘‘FACE’’. In thistask, three targets ‘‘faces’’ were presented sequentially,for 650 ms each, in three random locations on thescreen, chosen out of eight possible locations. After a3.5 s interval, another face appeared in a randomlocation. The subject had to decide whether the last facematched the location of any of the three target faces.They were instructed to press the ‘‘/’’ when there was amatch, or ‘‘z’’ when there was no match. This task isknown to activate a region in the right premotor cortex[Smith et al., 1998; Smith and Jonides, 1999]. Figure 1illustrates this experiment.

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AVerbal item recognition task—‘‘LETTER’’. In thistask, a small set of target uppercase letters waspresented simultaneously for 0.5 s, followed by a singlelowercase probe letter after a delay interval of 3 s. Thesubject had to decide whether the probe matched any ofthe target letters by pressing ‘‘/’’ when there was amatch or ‘‘z’’ when there was no match. This task isknown to activate the left posterior parietal cortex, threefrontal sites, and the left supplementary motor andpremotor areas [Smith et al., 1998; Smith and Jonides,1999]. Figure 2 illustrates this experiment.

Spatial compatibility—‘‘SPAT’’. In this task, a letterwas presented either on the left or on the right side of afixation letter. The subject had to activate the left or theright hand according to the side of the letter. This task isassumed to activate the right posterior parietal cortex,when the letter is in the right side of the fixation letter,and the left posterior parietal cortex when the letter is onthe left side of the fixation point [Peri and Zeki, 2000].Figure 3 illustrates this experiment.

Spatial compatibility—‘‘SIMON’’. In this task, thesubject had to respond to stimuli that appeared either on

the left or the right side of a fixation letter. When thesymbols P or y appeared, the subject had to respondwith his left or right hand, respectively. Previous studiesindicate that [Simon and Rudell, 1967; Simon, 1990]when the side of the stimulus’ presentation matches theresponding hand (the compatible condition), responseswere faster than when there is no match between theside of the stimulus and the responding hand (theincompatible condition). This is called the Simon effect[Simon and Rudell, 1967; Simon, 1990]. Figure 4illustrates this experiment.

The test was divided into two sessions: a first 1-hseries of tasks, a 5 min break, and then another hour oftasks. Before the first hour the subjects performed a 5-min training session of the four tasks employed in theexperiment in order to minimize training effects.

All subjects performed all four tasks under either,left, right, or sham exposure conditions. This resulted in12 sub-sessions per subject. Each subject performed atotal of 1614 trials in all four experiments.

RF Exposure

Each subject had two standard NokiaTM 5110GSM cellular phones attached to his head by a speciallydesigned non-conductive frame. The phones wereplaced on both sides of the head, as shown in Figure 5.

We controlled the cellular phones power by usingan HP GSM test system model E6392B. The phoneswere operated with test SIM cards (Wavetek). This

Fig. 1. ‘‘FACE’’�spatialitemrecognitiontask�thesubjectstaskistodecidewhether theprobefaceisin thesamelocationasanyof the target faces.

Fig. 2. ‘‘LETTER’’�verbal item recognition task�the subjectstaskistodecidewhether theprobematchesanyofthetargetletters.

X Xα

X

500msec 180msec

1200msec

Waiting for response

Fig. 3. ‘‘SPAT’’�spatial compatibility�the subject has to activatetheleft or therighthandaccording to thesideofthe letter.

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Asystem maintained the phones at either no transmissionor full power transmission (890.2 MHz, 33 dBm¼ 2 Wpeak power, using the typical GSM pulse duration of577 ms and duty cycle of 1/8, yielding 0.25 W averagepower). The communication between the phones andthe test system was wireless, at an extremely smalloutput power (0.01 mW peak output power, ascompared to the 2 W peak output of the phones); thus,we consider it negligible. During the experiment, thephones were battery operated. The phones weremounted on the subject’s heads before the first taskand dismounted after the final task.

At the end of the experiments, the subjects wererequested to assess whether and when the phonesoperated. They were unable to distinguish betweenexposure/sham-exposure situations, and between thesides of the exposures.

All tasks utilized the standard laboratory PC-based software (Micro Experimental Laboratory 2.0TM)and experiments were presented on 14 inch screens. Thesubjects used standard 104-key computer keyboards.

In case of an erroneous response, the computeremitted a 400 ms beep at 500 Hz. The exposure regimeand the order of the tasks were counterbalanced across

subjects according to a balanced Latin square design.Each subject served as his own control, namely, hisperformance without exposure was compared to hisown performance under exposure (a repeated measuresdesign). The RF exposure regime was single-blinded,i.e., the experiment manager was aware of the exposuremode, while the subjects were not, since the phoneswere silent all the time. An opaque partition was placedbetween the experiment manager and the subjectsduring the experiment.

RESULTS

In each task, trials with response times longer than3 s and shorter than 100 ms were screened out. Onlytrials in which the response was correct were included inthe response time analyses. In the present work,Greenhouse–Geisser correction was applied to thedf’s, and corrected P-values were reported for allfactors (when df> 2). No speed-accuracy trade-off wasobserved in any of the tasks.

A repeated measures analysis of variance(ANOVA) including Exposure condition (right hemi-sphere, left hemisphere, and sham exposure), Session(part one or part two), and Responding Hand (right orleft) as within dependent variables on the average RT ineach condition was performed.

Results for the FACE Task

The triple interaction between exposure, sessionand side was significant (F(2, 62)¼ 3.40, P¼.037) seeFigure 6a and b. For most exposure conditions, weobserved a reduction in the response/RT from the first tothe second session (with either sham exposure, orexposure to the right side of the brain). This result isprobably due to training (see Fig. 6a). However, in theleft hemisphere exposure condition, a reversed patternwas observed when subjects responded with their lefthand: the RT in the second part of the experiment wassignificantly prolonged relative to the first part, from907 to 931 ms (F(1, 32)¼ 6.30, P¼.01) and this patternwas significantly different from the sham exposure andright side exposure averaged together (F(1, 32)¼ 5.17,P¼.02) see Fig. 6b.

There was also a significant main effect ofResponding Hand, (F(1,32)¼ 13.3, P<.001) indicat-ing that RT was 48 ms (from 864 to 912 ms) faster forthe right hand responses (recall that all subjects wereright handed).

Results for the LETTER Task

The main effect for the factor session (F(1, 29)¼4.79, P¼.036) and Hand (F(1, 29)¼ 26.74, P<.0001)was significant, as was the interaction between these

X

XΠ X

250msec180msec

1500mse

Waiting for response

Fig. 4. ‘‘SIMON’’�spatialcompatibility�whenthesymbolsPandy appeared, the subject had to presshis left or right hand respec-tively.

Fig. 5. A subject during the experiment, with the phone frameattached.

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Afactors, (F(1, 29)¼ 9.54, P<.005). Subject improve-ment from the first to the second part of the experimentwas limited to the right hand (60 ms improvement forthe right hand as opposed to 0 ms for the left hand—seeFig. 7). The results also indicate a trend similar to theFACE experiment—RTs in the left hand were increasedunder the left side exposure condition (by 13 ms—from1014 to 1027 ms) as opposed to a slight decease in RT inthe right side and sham exposure (2 and 9 msrespectively). This trend was not significant. It ispossible that the effect of RFR is less evident on theaverage RTanalysis, but it may still affect other parts ofthe RT distribution [Ratcliff, 1979]. In order to verifythis point, we reanalyzed the data, this time using the25th (fast RT) percentile as the independent variable.The left-side exposure condition slowed left handresponses by 14 ms as opposed to acceleration for theright side and sham exposure conditions (15 and 29 ms,respectively). For left hand responses, the left exposurecondition was significantly slower than sham exposurein the second part of the experiment (F(1, 29)¼ 4.28,P¼.04). This difference was not significant in the firstpart of the experiment, F< 1.

Results for the SPAT Task

The only significant observable effect was themain effect for the factor of responding hand (F(1,

29)¼ 7.75, P<.01). Right hand responses were 9 msfaster than left hand responses (340 and 349 ms,respectively). Importantly, the same trend for the leftside exposure condition appeared also in this experi-ment (see Fig. 8): left hand responses were slowed downby 5 ms from the first to the second part of theexperiment (from 349 to 354 ms), but under the rightside and the sham exposure conditions, the left handresponses was accelerated (2 and 9 ms, respectively).The difference between the left side exposure conditionand the sham exposure condition was significant in thesecond part of the experiment (F(1, 30)¼ 6.43,P¼.01), but this difference was not significant in thefirst part of the experiment, F< 1.

Results for the SIMON Task

The ANOVA was the same as in the previousanalysis, but it included the variable compatibility(compatible vs. incompatible responses) as an addi-tional independent variable. The main significant effectwas the difference between the examination sessions(F(1, 29)¼ 10.86, P<.005), namely: the first part of theexperiment was on the average, 24 ms faster than thesecond part.

Another effect observed was the so-called Simoneffect [Simon and Rudell, 1967; Simon, 1990]—thecompatibility between the visual stimulus side and the

Fig. 6. Response times in milliseconds�left hand response (b) and right hand response (a)�‘‘FACE’’ task.Triple interactionbetweenexposure, session, andsidewassignificant.For threeof theexposureconditions,areductionintheresponsetimefromthefirst tosecondsessionwasobserved.Only in the setup in which the exposure was to the left side and the left hand responded was theresponse timeprolonged.

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Aresponding hand (F(1, 29)¼ 7.06, P¼.01), namely:compatible responses were 16 ms faster than incompat-ible responses (from 499 to 515 ms). There was noindication of any effects of RFR either in the average RTanalysis or in the fast RT analysis.

DISCUSSION

The scientific literature dealing with the effects oflow intensity radio waves emitted by cellular handsetsshows a growing interest in the existence of cognitive

Fig. 7. Response timesinmilliseconds�first andsecondsessions�LETTER task.

Fig. 8. Response timesinmilliseconds�first andsecondsessions�SPAT task.

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Aeffects. This is due to the assumption that cognitivefunctions might express very weak basic effects, if theyexist, in an observable manner, because of CNS amp-lification.

Of these effects, the linkage between RFR expo-sure and RT to external stimuli has been previouslyexamined. In particular, Preece et al. [1999] andKoivisto et al. [2000a,b] reported a shortening of theRT. Some work on verification of these reports failed toconfirm their findings [Haarala et al., 2003, 2004].

In these studies only one side of the head wasexposed: the left side [Preece et al., 1999; Koivisto et al.,2000a,b; Haarala et al., 2003, 2004] and the right side[Krause et al., 2000]. The responding hand was the righthand in some works [Koivisto et al., 2000a,b; Haaralaet al., 2003, 2004], while in the other publications thiswas not clearly specified.

In the present work, we thus added specificexaminations of possible differences between right/leftside exposures and right/left responding hand.

We considered these details to be of relevance, dueto the differentiation between the right/left brainhemispheres functions.

The present work is, to the best of our knowledge,the first attempt to examine directly these two res-ponding conditions. To achieve these purposes, we usedtwo phones, placed simultaneously on both sides of thehead, and in fact, our results indicated that the effect ofRFR was evident only in the left head side exposure andleft hand responding combined condition.

The statistically significant finding was a slowingeffect in left hand responses under left side RFRexposure condition only (found in the spatial itemrecognition task—‘‘FACE’’). This effect became evi-dent only in the second part of the experiment (namely:after an hour of test, of which 40 min were under fullpower exposure). The same trend was also observed inthe spatial compatibility task—‘‘SPAT’’, but was signi-ficant only in the specific comparison analysis.

While the effects of RFR were not evident in allexperiments, it is possible that the dependent variable ofaverage RT is not sensitive enough to detect thoseeffects [Ratcliff, 1979]. In this respect we have shownthat at least in one task (Verbal item recognition—‘‘LETTER’’) the effects were not apparent in the usualaverage RT but were detectable in other parts of the RTdistribution. Specifically, we found changes on the 25thpercentile (the fast part of the RT distribution).

It is noteworthy that although all the detectedeffects were expressed in left hand slowing, andappeared under left side exposure, we cannot statethat a hemisphere dependence was detected, as thefunctions affected are related to activities of bothhemispheres.

The origin of the differences between our resultsand the former studies is unclear, and could result formseveral reasons such as: the exposure methodology—right and left hemispheres, the responding hand—left orright, the exposure time, and the differences in thecognitive tasks. These differences seem to be significantand should be examined in future studies.

It can be concluded that more work is required toverify our results and to reconcile the differencesbetween our study, and the former studies in which anopposite effect, or no effect were found. In addition, theinvolvement of confounding factors must be examinedfurther.

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Softproofing for advanced Adobe Acrobat Users - NOTES toolNOTE: ACROBAT READER FROM THE INTERNET DOES NOT CONTAIN THE NOTES TOOL USED IN THIS PROCEDURE.

Acrobat annotation tools can be very useful for indicating changes to the PDF proof of your article.By using Acrobat annotation tools, a full digital pathway can be maintained for your page proofs.

The NOTES annotation tool can be used with either Adobe Acrobat 4.0, 5.0 or 6.0. Other annotation tools are also available in Acrobat 4.0, but this instruction sheet will concentrateon how to use the NOTES tool. Acrobat Reader, the free Internet download software from Adobe,DOES NOT contain the NOTES tool. In order to softproof using the NOTES tool you must havethe full software suite Adobe Acrobat 4.0, 5.0 or 6.0 installed on your computer.

Steps for Softproofing using Adobe Acrobat NOTES tool:

1. Open the PDF page proof of your article using either Adobe Acrobat 4.0, 5.0 or 6.0. Proofyour article on-screen or print a copy for markup of changes.

2. Go to File/Preferences/Annotations (in Acrobat 4.0) or Document/Add a Comment (in Acrobat6.0 and enter your name into the “default user” or “author” field. Also, set the font size at 9 or 10point.

3. When you have decided on the corrections to your article, select the NOTES tool from theAcrobat toolbox and click in the margin next to the text to be changed.

4. Enter your corrections into the NOTES text box window. Be sure to clearly indicate where thecorrection is to be placed and what text it will effect. If necessary to avoid confusion, you canuse your TEXT SELECTION tool to copy the text to be corrected and paste it into the NOTEStext box window. At this point, you can type the corrections directly into the NOTES textbox window. DO NOT correct the text by typing directly on the PDF page.

5. Go through your entire article using the NOTES tool as described in Step 4.

6. When you have completed the corrections to your article, go to File/Export/Annotations (inAcrobat 4.0) or Document/Add a Comment (in Acrobat 6.0).

7. When closing your article PDF be sure NOT to save changes to original file.

8. To make changes to a NOTES file you have exported, simply re-open the original PDFproof file, go to File/Import/Notes and import the NOTES file you saved. Make changes and re-export NOTES file keeping the same file name.

9. When complete, attach your NOTES file to a reply e-mail message. Be sure to include yourname, the date, and the title of the journal your article will be printed in.