Spectral asymmetry index and Higuchi s fractal dimension for detecting microwave radiation effect on electroencephalographic signal

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1 Proeedings of the Estonian Aademy of Sienes, 2014, 63, 3, doi: /pro Available online at Spetral asymmetry index and Higuhi s fratal dimension for deteting mirowave radiation effet on eletroenephalographi signal Maie Bahmann *, Jaanus Lass, Anna Suhhova, and Hiie Hinrikus Department of Biomedial Engineering, Tehnomedium of the Tallinn University of Tehnology, Ehitajate tee 5, Tallinn, Estonia Reeived 21 February 2014, revised 19 June 2014, aepted 20 June 2014, available online 28 August 2014 Abstrat. This study is aimed to the omparison of the sensitivity of linear spetral asymmetry index (SASI) and nonlinear Higuhi s fratal dimension (HFD) methods for deteting modulated mirowave effet on human eletroenephalographi (EEG) signal at non-thermal level of exposure. The experiments were arried out on a group of 14 healthy volunteers exposed to 450 MHz mirowave radiation modulated at 40 Hz frequeny. The applied mirowave power was 1 W and the field power density near the head was 0.16 mw/m 2. The EEG signal was reorded from 8 hannels: frontal FP1, FP2; temporal T3, T4; parietal P3, P4; and oipital O1, O2; with the ommon reording referene Cz. Mirowave exposure inreased the group averaged SASI value about 64%. However, the alteration was not statistially signifiant (p = 0.2). The HFD method deteted small (about 1.7%) but statistially signifiant (p = 0.008) enhanement of its value with mirowave exposure. Key words: EEG analysis, mirowave radiation, spetral asymmetry, fratal dimension, EMF effet. 1. INTRODUCTION * Brain ativity is based on neuronal bioeletrial proesses, whih reate eletroenephalographi (EEG) signal. The osillations are a prominent feature of neuronal proesses and the synhronization of the osillations is a likely mehanism for erebral integration for neural ommuniation [1,2]. The properties of neuronal osillators are the result of the physial arhiteture of neuronal networks and the limited speed of neuronal ommuniation due to axon ondution and synapti delays [3]. The unperturbed brain is a omplex system of numerous self-governed osillations, but the ontent of these rhythms is still poorly understood [4]. Some results reported in reent studies by several researhers demonstrate that the brain neuronal osillators behave as physial eletri osillators. Brain osillators, like most biologial rhythms, belong to limityle and weakly haoti osillators and share features of both harmoni and relaxation osillators [1]. Detailed * Corresponding author, maie@b.ttu.ee biophysial studies have revealed that even single neurons are endowed with omplex dynamis, inluding their intrinsi abilities to resonate and osillate at multiple frequenies [5]. The spetrum of brain osillations overs frequeny range from single neurons spiking to long-range ommuniation between different neural assemblies [1,2]. The ability of neuronal assemblies to synhronize depends on the oupling strength and the distribution of natural frequenies [1]. The spetrum of the natural frequenies desribes the state of an undisturbed brain. Therefore, the spetrum of the resting EEG signal is determined by the state of the brain. Proposed in our previous studies spetral asymmetry index (SASI) has been shown to detet delination in the balane of spetral powers aused by mental disorders as depression [6,7]. On the other hand, brain eletrial osillations an be affeted by external eletromagneti field. External periodi eletromagneti stressor is expeted to indue alterations in the brain bioeletri rhythms and EEG signal. Effets of the radio frequeny eletromagneti

2 M. Bahmann et al.: Mirowave radiation effet on eletroenephalographi signal 323 field on human brain physiology have beome of major interest with inreasing appliations of teleommuniation devies [8 10]. Teleommuniation devies employ radiofrequeny radiation, modulated at different low frequenies. Exposure to modulated radiofrequeny radiation leads to periodi alterations in the brain bioeletromagneti ativity. The modulation has been shown to play a ruial role in the radiofrequeny radiation effet on the brain; however, the mehanism of the effet at non-thermal level of exposure has been unlear during deades [11 13]. The proposed in our previous study parametri model of exitation, based on the theory of eletrial osillations, has been suessful in explaining the mehanism of the non-thermal effet of modulated mirowave radiation [14]. The idea of parametri exitation is supported by our original experimental data and an ontribute to interpretation of results reported by other authors [11 14]. The effet of mirowave exposure on the brain eletrial osillations is weak and therefore diffiult to reveal. Speial linear and some nonlinear measures have been suessfully applied for deteting the effet [15 17]. SASI has demonstrated very high sensitivity in deteting depression EEG [7]. The appliability of SASI for the detetion of harateristi hanges in the EEG signal related to mirowave radiation is an interesting question. The aim of the study is the omparison of the sensitivity of linear SASI and nonlinear HFD methods for deteting modulated mirowave effet on EEG at nonthermal level of exposure. For this purpose, the SASI and HFD methods were applied to the idential human EEG data, reorded during the experiments. 2. METHODS 2.1. Experimental proedure and equipment The experiments were arried out on a group of 14 healthy young volunteers (aged 21 24), 7 male and 7 female. The EEG reording was performed for a subjet during a day in a time interval from 9 a.m. to noon. The room of experiments was dark and the subjets were lying in a relaxed position, eyes losed and ears bloked during the experiments. The resting eyes losed EEG was ontinuously reorded during 20 min. The omputer swithed the mirowave radiation on during eah even minute and off during eah odd minute of the reordings. The EEG reordings were made using Cadwell Easy II EEG equipment. The EEG signal was reorded in Hz frequeny band using 8 hannels, aording to the international eletrode position lassifiation system. The hannels for analysis were hosen to over the entire head: frontal FP1, FP2; temporal T3, T4; parietal P3, P4; oipital O1, O2; with the ommon referene Cz. The reorded EEG signals were stored on a omputer in Hz frequeny band at 80 Hz sampling frequeny. The study was onduted in aordane with the Delaration of Helsinki and was formally approved by the Tallinn Medial Researh Ethis Committee. The experiments were onduted with understanding and written onsent of eah partiipant. Mirowave radiation at the nonthermal level of field power density was seleted to be idential to that in our previous studies [13,18]. Exposure onditions were the same for all subjets in the group. The 450 MHz eletromagneti radiation was generated by the Rohde & Swartz signal generator, model SML02. The radiofrequeny signal was 100% pulse-modulated by the Rohde & Swartz pulse modulator SML-B3 at 40 Hz frequeny, duty yle 50%. The signal from the generator was amplified by the Dage Corporation power amplifier, model MSD The generator and amplifier were arefully shielded. The 1 W eletromagneti radiation output power was guided by a oaxial lead to the quarter-wave antenna NMT450 RA3206 by Allgon Mobile Communiation AB, loated lose to ear, 10 m from the skin on the left side of the head. The Central Physial Laboratory of the Estonian Health Board measured the spatial distribution of the eletromagneti radiation power density by the Chauvin Arnoux Fieldmeter CA 43 field strength meter. The alibration urves of dependene of the field power density on the distane from the radiating antenna were obtained from these measurements, performed under real experimental onditions. The field power density of the modulated mirowave at the skin from the left side of the head was 0.16 mw/m 2 as estimated from the measured alibration urves. The speifi absorption rate (SAR) was alulated using SEMCAD (Shmid & Partner Engineering AG, Zurih, Switzerland) software. The finite differene time domain (FDTD) omputing method with speifi anthropomorphi mannequin (SAM), speified in IEEE Standard 1528, was applied. The alulated spatial peak SAR, averaged over 1 g, was W/kg. During the experiments, the stability of the eletromagneti radiation level was monitored by the IC Engineering Digi Field C field strength meter EEG analysis: SASI method First, all the reorded EEG signals were divided into exposed and nonexposed signals as follows: the signal without mirowave exposure ontained all odd minutes intervals from the initial EEG reordings whereas the signal with mirowave exposure ontained all even minutes intervals from the initial EEG reordings. SASI was alulated for a single hannel as a relative differene between the powers of the EEG frequeny

3 324 Proeedings of the Estonian Aademy of Sienes, 2014, 63, 3, bands seleted higher and lower than the maximum of the EEG spetrum (alpha band) [6,7]. The balane of the powers haraterizes the EEG spetral asymmetry. Important aspet of the method is exlusion of the alpha frequeny band from the analysis. Therefore the boundary frequenies for the seleted bands were adjusted taking into aount the alpha frequeny range in the EEG power spetrum for eah individual subjet. The frequeny with the maximum spetral power f max in the region of alpha band 8 13 Hz was estimated alulating the power spetral density of the reorded EEG signal by means of Welh s averaged periodogram method. Thereafter the paraboli approximation was applied to the spetrum of the EEG entral frequeny band ( fmax ± B)Hz, where B = 2Hz was half-width of the band. The best paraboli fit for power spetral distribution was alulated by applying the Matlab POLYFIT tool. The maximum point of the fitted parabola f was taken as a entre of the entral band. The frequenies of the lower and higher frequeny bands were related to the estimated entral frequeny f. The lower frequeny band was seleted from F1 to F2, where F1 = ( f 6) Hz and F2 = ( f 2) Hz. The higher frequeny band had boundary frequenies F3 and F4, where F3 = ( f + 2) Hz and F4 = ( f + 26) Hz. The EEG signal powers W lmn and W in the lower and in the higher EEG frequeny bands respetively were alulated for eah EEG hannels (indexed by m [1, 8]) and subjet (indexed by n [1, 14]) as F 2 Wlmn = S( f) mn df, F1 F 4 W = S( f) df, (1) where S( f ) mn is the power spetral density of the reorded EEG signal in a hannel m for a subjet n. Finally, the spetral asymmetry index was alulated as SASI mn W = W W + W lmn lmn F 3. mn (2) The alulations of the SASI were performed for eah subjet and EEG hannel EEG analysis: the HFD method The HFD algorithm alulates fratal dimension of time series diretly in the time domain [19]. It is based on a measure of length Lk ( ) of the urve that represents the onsidered time series while using a segment of k samples as a unit if Lk ( ) sales like FD Lk ( )~ k. (3) The value of the fratal dimension FD was alulated aording to the following algorithm [19]. From given time series: X (1), X (2), X (3), K, X( N) a new series X is onstruted as: m k m N m Xk : X( m), X( m+ k), X( m+ 2 k), K, X m+ k, k m= 1, 2, K, k, (4) where [ ] indiates the Gauss notation. The length Lm ( k ) of every urve is alulated aording to the formula: Lm ( k) = N m k 1 N 1 X( m ik) X( m ( i 1) k). k + + i= 1 N m k k (5) The length Lk ( ) of the urve for time interval k is defined as an average over k values of Lm ( k ), FD m = 1, 2, K, k. If Lk ( ) sales like Lk ( )~ k, the urve has fratal dimension FD, whih is alulated using linear regression of graph: 1 ln ( Lk ( )) ~ ln, k where k = 1, K, kmax. The slope of the obtained line is the estimate of the fratal dimension. FD was alulated in 400 samples (5 s) window, and the window was shifted by 40 samples (0.5 s). A value of 8 was hosen for k. max FD for a subjet and hannel was ahieved using averaging over all FD values for a signal of 10 min length Statistis (6) Student s t-test for two-tailed distribution with twosample unequal variane was applied for statistial evaluation of the differene between the alulated SASI and HFD series with and without mirowave exposure. The onfidene level of p < 0.05 was onsidered statistially signifiant. 3. RESULTS Figure 1 presents SASI values averaged over a group at onditions without and with mirowave exposure. The average values of SASI are negative at both onditions. The averaged SASI value at mirowave exposure is about three times higher. Mirowave exposure inreases

4 M. Bahmann et al.: Mirowave radiation effet on eletroenephalographi signal 325 the averaged SASI value for about 64% from its initial level. However, the alteration is not statistially signifiant ( p = 0.2). SASI values for individual subjets are presented in Fig. 2. SASI is positive for 4, negative for 8, and lose to zero for 2 subjets. Mirowave exposure inreases SASI value for 6 and dereases for 4 subjets, while no onsiderable hange in SASI value is observed for 4 subjets. Figure 3 is an example, illustrating the least-squares linear best-fit urve alulated on the ln ( Lk ( )) versus ln (1 k ), indiating that the data follow power law. HFD values averaged over a group are presented in Fig. 4. Mirowave exposure inreases the value for about 1.7% and the alteration is statistially signifiant ( p = 0.008). Figure 5 presents HFD values for individual subjets. Mirowave exposure inreases HFD value for 12 and dereases for 1 subjet, almost no hange is observed for 1 subjet. Fig. 3. An example of the least-squares linear best-fit urve ln (L(k)) vs ln (1/k). Fig. 1. Values of SASI, alulated for reordings with and without mirowave exposure averaged over a group of 14 subjets and 8 EEG hannels; vertial bars denote standard deviation. Fig. 4. Values of HFD, alulated for reordings with and without mirowave exposure, averaged over a group of 14 subjets and 8 EEG hannels; vertial bars denote standard deviation. Fig. 2. Values of SASI, alulated for reordings with and without mirowave exposure for individual subjets in hannel P3. Fig. 5. Values of HFD, alulated for reordings with and without mirowave exposure for individual subjets in hannel P3.

5 326 Proeedings of the Estonian Aademy of Sienes, 2014, 63, 3, DISCUSSION 5. CONCLUSION The SASI method shows more remarkable enhanement with mirowave exposure (64%) ompared to the HFD (1.7%). However, the alterations, deteted by SASI, are not statistially signifiant. The advantages of SASI beome ineffetual due to high variability of results. The alulated values of SASI and HFD have remarkable differenes between individual subjets. High interindividual variability is harateristi for physiologial proesses and parameters. Suh variability auses high standard deviation in the measures alulated for a group (Figs 1 and 4). Therefore, inter-individual variability redues the probability of deteting alterations, aused by mirowave exposure. The statistial analysis shows that SASI is more affeted by inter-individual variability ompared to HFD. In addition, the results are obviously affeted by the individual sensitivity of subjets to mirowave radiation; the expeted rate of affeted subjets is about 30% [18]. This rate explains the numbers of subjets with lear alterations aused by mirowave radiation: 4 subjets aording to SASI and 6 subjets aording to HFD (Figs 2 and 5). Diverse results, ahieved using SASI and HFD, an be explained by different nature of the methods. SASI presents the balane of EEG power at higher-lower frequenies, whih are expeted to take plae during normal nondisturbed ativity of the brain [7]. The mirowave exposure disturbs the brain and an affet both, the power at lower and at higher EEG frequenies. As our previous studies showed, the mirowave exposure enhanes the level of the EEG power at a fixed EEG frequeny band [20]. Whereas the powers at the lower and at the higher EEG frequeny bands both an be enhaned by the mirowave exposure, the balane between the powers might be not so learly affeted. The mirowave exposure, disturbing the brain, is expeted to enhane the omplexity of the bioeletri proesses in the brain. Therefore, HFD is more suitable for revealing alterations, aused by mirowave exposure, ompared to SASI. On the other hand, the absolute values of HFD are not graded aording to the state of the brain. It is not possible to make deision about the mental state or disturbane of the brain for an individual based on a HFD value, while SASI, introdued for detetion of depression, differentiates depressive with positive and healthy subjets with negative values [6,7]. The SASI values beame more positive also with mirowave exposure. However, the mirowave exposure does not alter the state of the brain and does not hange the polarity of the SASI value. The SASI method, based on the balane of the powers of two EEG frequeny bands, is less suitable for the detetion of the mirowave effet, ompared to the HFD. ACKNOWLEDGEMENTS This study was finanially supported by the Estonian Ministry of Eduation and Researh under institutional researh finaning IUT 19-2 and by the European Union through the European Regional Development Fund. REFERENCES 1. Buzsáki, G. and Draguhn, A. Neuronal osillations in ortial networks. Siene, 2004, 304, Shnitzler, A. and Gross, J. Normal and pathologial osillatory ommuniation in the brain. Nature Rev. Neurosi., 2005, 6, Nunez, P. L. Neoortial Dynamis and Human EEG Rhythms. Oxford University Press, New York, Steriade, M. and Timofeev, I. Neuronal plastiity in thalamoortial networks during sleep and waking osillations. Neuron, 2003, 37, Hutheon, B. and Yarom, Y. Resonane, osillation and the intrinsi frequeny preferenes of neurons. Trends Neurosi., 2000, 23, Hinrikus, H., Bahmann, M., Lass, J., Suhhova, A., Tuulik, V., Aadamsoo, K., and Võhma, Ü. Method and devie for diagnosing a mental disorder by measuring bioeletromagneti signals of the brain. US B1 from Aug. 14, Hinrikus, H., Suhhova, A., Bahmann, M., Aadamsoo, K., Võhma, Ü., Lass, J., and Tuulik, V. Eletroenephalographi spetral asymmetry index for detetion of depression. Med. Biol. Eng. Comput., 2009, 47, Cook, C. M., Sauier, D. M., Thomas, A. W., and Prato, F. S. Exposure to ELF magneti and ELFmodulated radiofrequeny fields: the time ourse of physiologial and ognitive effets observed in reent studies ( ). Bioeletromagnetis, 2006, 27, Valentini, E., Curio, G., Moroni, F., Ferrara, M., De Gennaro, L., and Bertini, M. Neurophysiologial effets of mobile phone eletromagneti fields on humans: a omprehensive review. Bioeletromagnetis, 2007, 28, Juutilainen, J., Höytö, A., Kumlin, T., and Naarala, J. Review of possible modulation-dependent biologial effets of radiofrequeny fields. Bioeletromagnetis, 2011, 32, Huber, R., Treyer, V., Borbely, A. A., Shuderer, J., Gottselig, J. M., Landolt, H. P. et al. Eletromagneti fields, suh as those from mobile phones, alter regional erebral blood flow and sleep and waking EEG. J. Sleep Res., 2002, 11,

6 M. Bahmann et al.: Mirowave radiation effet on eletroenephalographi signal Huber, R., Treyer, V., Shuderer, J., Berthold, T., Buk, A., Kuster, N. et al. Radiation to pulsemodulated radio frequeny eletromagneti fields affets regional erebral blood flow. Eur. J. Neurosi., 2005, 21, Hinrikus, H., Bahmann, M., Lass, J., Tomson, R., and Tuulik, V. Effet of 7, 14 and 21 Hz modulated 450 MHz mirowave radiation on human eletroenephalographi rhythms. Int. J. Radiat. Biol., 2008, 84, Hinrikus, H., Bahmann, M., and Lass, J. Parametri mehanism of exitation of the eletroenephalographi rhythms by modulated mirowave radiation. Int. J. Radiat. Biol., 2011, 87, Bahmann, M., Kalda, J., Lass, J., Tuulik, V., Säkki, M., and Hinrikus, H. Non-linear analysis of the eletroenephalogram for deteting effets of low-level eletromagneti fields. Med. Biol. Eng. Comput., 2005, 43, Hinrikus, H., Bahmann, M., Kalda, J., Sakki, M., Lass, J., and Tomson, R. Methods of eletroenephalographi signal analysis for detetion of small hidden hanges. Nonlinear Biomed. Phys., 2007, 1:9, 28 July Hinrikus, H., Bahmann, M., Karai, D., Klonowski, W., Lass, J., Stepien, P. et al. Higuhi s fratal dimension for analysis of the effet of external periodi stressor on eletrial osillations in the brain. Med. Biol. Eng. Comput., 2011, 49, Hinrikus, H., Bahmann, M., Lass, J., Karai, D., and Tuulik, V. Effet of low frequeny modulated mirowave radiation on human EEG: individual sensitivity. Bioeletromagnetis, 2008, 29, Higuhi, T. Approah to an irregular time series on the basis of the fratal theory. Physia D, 1988, 31, Hinrikus, H., Bahmann, M., Lass, J., and Tuulik, V. Effet of modulated mirowave radiation on eletroenephalographi rhythms and ognitive proesses. Estonian J. Engng, 2008, 14, Spektraalse asümmeetria indeks ja Higuhi fraktaaldimensioon mikrolainekiirguse mõju leidmiseks elektroentsefalograafilises signaalis Maie Bahmann, Jaanus Lass, Anna Suhhova ja Hiie Hinrikus Käesoleva uuringu eesmärgiks oli elektroentsefalograafilise signaali (EEG) analüüsi lineaarse meetodi, spektraalse asümmeetria indeksi (SASI), ja mittelineaarse meetodi, Higuhi fraktaaldimensiooni (HFD) tundlikkuse võrdlemine moduleeritud mikrolainekiirguse mittesoojusliku mõju leidmisel. Uuringus osales 14 tervet vabatahtlikku, keda kiiritati 40 Hz sagedusega moduleeritud 450 MHz mikrolainekiirgusega. Mikrolainekiirguse võimsus oli 1 W ja väljatugevuse tihedus pea vahetus läheduses 0,16 mw/m 2. Uuringu käigus registreeriti EEG-signaal kaheksas kanalis, kasutades ühist referentselektroodi Cz: frontaalsetes FP1 ja FP2, temporaalsetes T3 ning T4; parietaalsetes P3 ja P4 ning oktsipitaalsetes O1 ja O2. Mikrolainekiirgus põhjustas uuritavate grupil SASI keskväärtuse suurenemise 64%. Muutus ei osutunud aga statistiliselt oluliseks (p = 0,2). HFDmeetod tuvastas mikrolainekiirguse korral väikese (umbes 1,7%), kuid statistiliselt olulise (p = 0,008) fraktaaldimensiooni väärtuse suurenemise.