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Braz J Med Biol Res 37(6) 2004

Topographic aspects of EEG photic driving in childrenBrazilian Journal of Medical and Biological Research (2004) 37: 879-891ISSN 0100-879X

Topographic aspects of photic driving inthe electroencephalogram of childrenand adolescents

1Laboratório de Neurobiologia e Neurofisiologia Clínica, Setor de Neurologia,Instituto Fernandes Figueira, Fundação Oswaldo Cruz, Rio de Janeiro, RJ, Brasil2Programa de Engenharia Biomédica (COPPE), Centro de Tecnologia,Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brasil

V.V. Lazarev1,A.F.C. Infantosi2,

D. Valencio-de-Campos2

and L.C. deAzevedo1

Abstract

The electroencephalogram amplitude spectra at 11 fixed frequenciesof intermittent photic stimulation of 3 to 24 Hz were combined intodriving “profiles” for 14 scalp points in 8 male and 7 female normalsubjects aged 9 to 17 years. The driving response varied over fre-quency and was detected in 70 to 100% of cases in the occipital areas(maximum) and in 27 to 77% of cases in the frontal areas (minimum)using as a criterion peak amplitude 20% higher than those of theneighbors. Each subject responded, on average, to 9.7 ± 1.15 intermit-tent photic stimulation frequencies in the right occipital area and to 6.8± 1.97 frequencies in the right frontal area. Most of the drivingresponses (in relation to the previous background) were significantaccording to the spectral F-test (α = 0.05), which also detectedchanges in some cases of low amplitude responses not revealed by thepeak criterion. The profiles had two maxima in the alpha and thetabands in all leads. The latter was not present in the background spectrain the posterior areas and was less pronounced in the anterior ones. Theweight of the profile theta maximum increased towards the frontalareas where the two maxima were similar, while the profile amplitudesdecreased. The profiles repeated the shape of the background spectra,except for the theta band. The interhemispheric correlation betweenprofiles was high. The theta driving detected in all areas recordedsuggests a generalized influence of the theta generators in prepubertaland pubertal subjects.

CorrespondenceV.V. Lazarev

Laboratório de Neurobiologia e

Neurofisiologia Clínica

Instituto Fernandes Figueira

FIOCRUZ

Av. Rui Barbosa, 716

22250-020 Rio de Janeiro, RJ

Brasil

Fax: +55-21-2551-0547

E-mail: [email protected]

Received April 27, 2003

Accepted March 22, 2004

Key words• Electroencephalogram• Intermittent photic

stimulation• Photic driving• Brain topography• Children• Adolescents

Introduction

The driving response to intermittent photicstimulation (IPS) is an important functionaltest used in electroencephalography (EEG)in order to enhance the manifestation of thelatent sources of rhythmic bioelectrical ac-tivity including its pathological forms (1,2).In previous communication, we investigated

the structural specificity of the local drivingresponse in children and adolescents (3). Inorder to integrate the reactions to differentIPS frequencies and compare their ampli-tudes, we have proposed a “profile” of thedriving reaction composed of the amplitudespectra measurements at the frequencies ofstimulation from different EEG epochsmatched to a range of fixed frequencies of

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IPS across the EEG frequency range. Theseprofiles proved to repeat the shape of thebackground spectra with high Pearson corre-lation coefficients between them, both hav-ing the maximum peaks in the alpha fre-quency band. However, in the profiles ofchildren and adolescents, the second maxi-mum driving response was detected in thetheta band, not present in the backgroundEEG spectra and not described in the litera-ture on the driving reaction in adults. Thisheightened theta responsiveness was con-sidered to be peculiar for the age groupstudied. In comparison with the spectrum ofthe resting EEG, the driving profile sug-gested the possibility to provide a fuller rep-resentation of the set of potential oscillators.

The aforementioned results were de-scribed for the right occipital region (3) gen-erally considered representative for the studyof the EEG effects of visual stimulation (4-6). However, there is much supporting evi-dence in the literature for the thesis that thedriving response may be observed in othercortical regions as well. Furthermore, theregional specificity may be very important inclinical and psychophysiological diagnosis,especially with respect to local alterations inthe functional state of the brain.

First of all, this concerns hemisphericspecificity. Various types of interhemisphericdifferences in the EEG driving reaction wereobserved in adult subjects and patients (7-9)and it was shown that IPS may emphasizethe functional asymmetry (10). It has evenbeen proposed that in certain cases the sensi-tivity of the left and right hemispheres to IPSmay differ in relation to high and low stimu-lation frequencies (11).

Clinical research has shown that the in-terhemispheric relationships between theharmonic components of the responses toIPS might be of importance in topographicdiagnosis (12,13). The asymmetric drivingeffects such as a locally increased rhythmicresponse at the delta or beta frequencies aswell as a reduced or a disproportionately

strong response within the alpha-band mayindicate a focal disturbance and should betaken into account as indicators of a func-tional alteration (14). Cortical lesions of adestructive type may cause ipsilateral de-pression or attenuation of driving, whereasirritative lesions, such as those of epilepticscars, may lead to an increased response onthe side of the focus (15,16). In paranoidschizophrenia, an increased interhemispheric(17) and decreased intrahemispheric coher-ence (18) was observed during IPS, reveal-ing, according to the authors, a less lateral-ized cerebral organization than in normalsubjects and a more diffuse, undifferentiatedfunctional organization within the hemi-spheres. Asymmetrical effects of driving re-actions have also been utilized in researchon the pathology of the visual field (1).

The regional specificity of the drivingreactions in the sagittal direction has beenless explored. However, in normal adult sub-jects, the driving response in the premotor,motor and sensorimotor cortical areas mayinterfere directly with motor activity (19).The topography of the driving responses atthe alpha frequencies permitted the identifi-cation and localization of the sources of thealpha rhythm in the thalamic structures byconstructing equivalent dipole models (20).

Certain alterations in the sagittal distri-bution of the driving reaction have beenobserved in the alpha band in schizophrenicpatients. Their lower photic driving occurredacross most brain areas except for the centro-temporal regions (21), and in the frontalareas, it could be higher than in the occipitalones (22). Some reduction in photic drivingand significant topographic alterations werefound in the parieto-occipital regions of pa-tients with presenile Alzheimer’s disease(23). In the positron emission tomography ofregional blood flow, EEG photic drivingcorrelated with activation of occipital corti-cal and some subcortical structures, and inphotosensitive epileptic patients, the nucleiactivated during paroxysmal responses were

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different from those activated in non-parox-ysmal driving. For this reason, the latterwere associated with an inhibition of epilep-tic discharges (24).

Thus, the topographic aspect of photicdriving looks promising for the study of theregional specificity of the functional state ofthe brain and its pathological alterations.Some approaches to quantitative EEG topo-graphic mapping may be used in the study ofthe complex spatial patterns of this phenom-enon (25). However, all the aforementioneddata concern adult subjects. In our prelimi-nary examination of several children andadolescents suffering from migraine (26),we detected a low spatial consistency inpeak frequencies and a decreased interhemi-spheric correlation of the photic driving pro-files by the methodology detailed in the pre-vious communication (3). Thus, the study ofthe photic driving topography in normal sub-jects of this age group is very important as anormative basis for clinical studies. How-ever, the weaker response with the loweramplitude in the regions anterior to the oc-cipital visual areas is usually one of thereasons for the latter to be an almost exclu-sive point of the examination of the drivingresponses (4-6).

The objective of the present study was toindicate with computerized criteria the pres-ence of the photic driving responses in vari-ous brain areas, to assess the sensitivity andphysiological significance of these indica-tors and to compare the driving profiles indifferent regions in order to reveal the nor-mal topography of the potential latent oscil-lators not present in the resting EEG andcharacteristic for the age group studied.

Material and Methods

The topography of the driving responseswas investigated in the same 8 male and 7female volunteers, between 9 and 17 yearsof age with a median age of 13.3, who weredescribed in the previous communication

(3). None was overtly left-handed (accord-ing to the writing hand and the reports of theparents) and none had a history of neurologi-cal, psychiatric or drug-related illness. Thelocal Ethics Committee approved this re-search and the subjects or persons respon-sible gave informed consent to participate inthe study.

EEG signals were recorded during a stateof relaxed wakefulness (initial background,2-3-min duration), during IPS of variousfrequencies and during wakefulness betweenstimulations at different frequencies. Theeyes of the subjects were closed throughoutthe experiment. Each presentation of a fixedfrequency lasted 20-30 s, with the same peri-ods between stimulations. One series ofstimulations consisted of the following flickerfrequencies: 3, 4, 5, 6, 8, 10, 12, 15, 18, 21,and 24 Hz.

The EEG was recorded with an 18-chan-nel Nihon Kohden polygraph (EEG-4418),at 14 scalp points, according to the Interna-tional 10/20 System, with unilateral refer-ences to the corresponding earlobes. Thesepoints were located over the following areasof the left (odd index) and right (even index)hemispheres: occipital (O1, O2), parietal (P3,P4), central (C3, C4), frontal (F3, F4), poste-rior temporal (T5, T6), mid-temporal (T3,T4), and anterior temporal (F7, F8). Therecording characteristics were: 0.3-s timeconstant, 70-Hz high frequency filter and15-µV/mm sensitivity. The EEG signals wererecorded on magnetic tape with a TEACXR-7000 tape recorder (Tokyo, Japan) withsimultaneous paper recording, after digitali-zation with an A/D converter (12-bit preci-sion) at a sampling frequency of 256 Hz.The instants of stimulation were also ac-quired to be used as reference when applyingthe signal processing techniques. In order toavoid the possible short post-stimulation ef-fect (27), the first 5 s after each stimulationwere excluded from analysis.

For each IPS frequency, before and dur-ing stimulation, the EEG signals were sec-

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tioned into M = 10 epochs of equal duration(2 s). Then, the spectra were estimated andthe spectral F-test (SFT) was applied. Thepower spectrum was estimated using themodified periodogram of Bartlett based onthe Discrete Fourier Transform of the 2-sduration epochs, resulting in a frequencyresolution of 0.5 Hz. For each lead, the spec-trum was represented as an amplitude spec-trum (i.e., the square root of the absolutepower) and the presence of the driving re-sponse at the frequency of stimulation wasascertained by in-house software as an am-plitude peak which was at least 20% higherthan the amplitudes at adjacent frequencies(± 1 Hz). In computer simulation, this levelof prevalence gave a false-positive rate ofless than 5% when the spectrum of signalswas white, i.e., when there was no responseto the stimuli (3). Henceforth, this will bereferred to as “the 20% criterion”.

The SFT was calculated as the ratio of thepower spectra obtained from the EEG duringand before stimulation (28). Knowing that inthe absence of spectral change the ratio ofaveraged periodograms follows an F-distri-bution, the null hypothesis (H0) of the ab-sence of response can be tested (29). Thus,the critical value was determined as SFTcrit= 2.12 for a level of significance of α = 5%and the SFT at any frequency was comparedto this value. If SFT(f) <SFTcrit, the absenceof response in the frequency f was accepted,but if SFT(f) ≥SFTcrit, H0 was rejected.

The results of the spectral analysis werepresented for each subject as 14 spectro-grams plotted according to the electrode scalpposition, as illustrated in Figure 1A. Foreach lead, the estimated spectrum is de-picted as an amplitude spectrum, i.e., thesquare root of the absolute power, with afrequency resolution of 0.5 Hz. The SFTvalues were also topographically plotted inthe same way (Figure 1B). The frequency ofstimulation and its harmonics were indicatedby vertical lines (Figure 1).

The group data of the driving presence

Figure 1. An example of individual spectrograms (A) and spectral F-test value diagrams (B)(subject M) with a strong generalized driving response to 6-Hz intermittent photic stimula-tion in almost all the scalp points recorded (marked above each spectrum or diagram).Abscissas: frequency of EEG, in Hz. Vertical lines mark a frequency of stimulation and itsharmonics, i.e., 6, 12, 18 Hz, etc., from left to right. Ordinates: A = amplitude spectra, in µV/√Hz; B = spectral F-test values; horizontal line = critical value 2.12 for a level of significanceα = 5%.

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obtained by the 20% peak criterion and theSFT (α = 5%) at each fundamental frequencyof stimulation (first harmonic) in each scalplead were plotted as percent of subjects whoresponded to the given frequency of IPS atthe given lead for the two different sche-matic scalp maps according to the electrodepositions. The two maps were compared bysubtraction of the values of the second mapfrom those of the first one.

In order to compare the magnitude of theresponses to all the frequencies of stimula-tion, amplitude spectra measured at all fre-quencies were plotted on the same diagramcalled “the frequency profile of the drivingreaction” (or simply, “the profile”) (3).

The similarity of different profiles at dif-ferent scalp points was evaluated by thePearson correlation coefficient (R). The sta-tistical significance of the differences be-tween profiles at each frequency was calcu-lated by the Wilcoxon test.

Results

The spectrograms of Figure 1A illustratean example of a strong driving response tothe IPS of 6 Hz in subject M. The figureshows the existence of peaks at the stimula-tion frequency and at some of its harmonics(12 and 18 Hz). In the occipital region, thesepeaks are more pronounced compared tothose of other regions. One may see that thepeak amplitudes decrease towards the fron-tal areas where the third harmonic of 18 Hzdisappears. Furthermore, it is interesting tonote that at 12 Hz (EEG frequency of thealpha band) the relative contribution washigher than at the stimulation frequency (seediscussion of this effect in Ref. 3).

Figure 1B depicts the SFT of the 14 EEGleads for the same subject M at the same IPSof 6 Hz. Based on SFTcrit = 2.12 (indicatedby the horizontal line), the null hypothesis ofthe absence of response was rejected(α = 5%) (false-positive rate), particularlyfor the frequency of stimulation and some of

its harmonics. For most of the other frequen-cies, H0 was accepted, that is, no responsecould be identified. Thus, one can say that inthe central, parietal and occipital regions thepresence of responses occurs at 6, 12 and 18Hz. Furthermore, in the occipital regionsthere was also a response at 24 Hz while inthe other ones no responses were identifiedat this frequency.

Comparing Figure 1A and B one can seethat most of the driving responses recordedin all brain areas were detected by bothspectral peak (the 20% criterion) and SFT.However, there were some cases of detec-tion of significant changes in the EEG bySFT against an absence of any visible peakin the spectrum, such as in F4, F8 and T4 atthe frequency of 18 Hz. Sometimes, thesecases did not relate to the harmonics of theIPS frequency, such as in T4 at 3.5 and 26Hz, and could be rejected by an increase ofthe significance level to 2 or 1%. On theother hand, a spectral peak meeting the 20%criterion could not be confirmed by SFT,such as in F7 at 6 Hz.

Using the 20% criterion for the spectro-grams, the response to stimulation was mostoften found, as expected (4-6), in the occipi-tal areas. For the frequency of stimulation(first harmonic), this occurred, on average,in 85% of subjects (minimum 70% at 21 Hzand maximum 97% at 4 Hz; Figure 2A).However, in the other 12 regions, the drivingresponse was also observed in more thanhalf the subjects at all IPS frequencies ex-cept for the 3-Hz case. On average, it wasdetected in 65% of subjects - minimum val-ues of 29% at 3 Hz and 53% at 4 Hz and amaximum value of 72% at 15 Hz (Figure2A). Even in the frontal areas, where thedriving response may be expected to be thelowest (4-6), it occurred, on average, in 61%of cases. In F4, for example, one subjectresponded, on average, to 6.8 ± 1.97 (mean ±SD) frequencies of stimulation or to 62% ofthe 11 IPS frequencies presented. Only onesubject was not responsive to stimulation in

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Figure 2. Scalp maps with the percentage of subjects showing a driving response according to the criterion of peak values 20% greater than those ofadjacent frequencies (A) and spectral F-test (B) at each of 11 frequencies of intermittent photic stimulation (IPS, Hz) in each lead. Each square cellrepresents a lead (plotted on each map according to the head scheme in the right lower corner of the figure) with a percentage for the group of 15subjects at a frequency of IPS given above the corresponding map. To the right of each map - average data for I: 12 leads except O1 and O2; II, III andIV: 4 leads of a corresponding line; V: for O1 and O2 (see the head scheme in the right lower corner of the figure). C, Maps of difference of thepercentages between 20% criterion and spectral F-test in each lead.

any region. Therefore, as in our previouscommunication (3), most of the group databelow refer to 14 subjects, excluding theunresponsive subject. In F4, in almost allcases of stimulation, an increase in ampli-tude spectra relative to the background wasobserved at all the EEG frequencies corre-sponding to those of IPS (Figure 3).

When the mapping of the results of theSFT at all stimulation frequencies for allsubjects (Figure 2B) was compared with the20% criterion maps (Figure 2A), the re-sponses were found to be significant in mostcases of the driving peak in the spectrum atthe fundamental stimulation frequency (Fig-

ure 2C). For the general group the number ofthe significant changes in the EEG at allfundamental frequencies of stimulation was88.8% of the peak responses in the occipitalareas and 92.6% in the remaining areas.However, at frequencies of 3 to 15 Hz, inmost of the leads (always in the occipitalones), 1 to 6 subjects responded with a spec-tral peak at the stimulation frequency notconfirmed by the SFT. On the other hand,there were some areas where significantchanges in the EEG at the stimulation fre-quency could be observed in some subjects(1 to 5 in a lead) without being related to thedriving spectral peak. Such areas prevailed

A: 20% criterionA: 20% criterionA: 20% criterionA: 20% criterionA: 20% criterion

B: Spectral F-testB: Spectral F-testB: Spectral F-testB: Spectral F-testB: Spectral F-test

C: DifferenceC: DifferenceC: DifferenceC: DifferenceC: Difference

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at frequencies of 18 to 21 Hz. At the lowerfrequencies and at 24 Hz, this phenomenonwas never detected in the occipital regions.

The profiles of the driving responses ob-tained for the different brain areas proved tohave both similar and distinguishing fea-tures in comparison with the occipital reac-tions described in our previous communica-tion (3). For example, this was observed inthe right hemisphere where, as mentionedabove, the profile in F4 was expected todiffer most from that of O2. The shape of theprofiles for F4 and O2 (which have differentgeneral amplitude levels) can be comparedon the basis of the amplitude ratios of thetheta, beta and delta maxima to the alphapeak (Figure 3). Both profiles had twomaxima in the alpha and theta bands. How-ever, the amplitude ratios between them weredifferent.

In O2, an increased theta maximum (ex-ceeding half the maximum in the alpha band)was observed in 11 of 14 subjects. It was, onaverage, 70.5 ± 14.6% of the profile’s alphapeak amplitude, with the theta maximumnever exceeding the alpha one. In the restingEEG, the same ratio was 30.8 ± 9.9% (ex-cluding subject T who did not have an alphapeak in the background EEG). An increasein amplitude spectra at the theta maximum(compared to the background) exceeded halfof that in the alpha band in 10 subjects. Inthese cases, it was, on average, 94.7 ± 35.4%of the alpha maximum increase (Figure 3). Inthe remaining 4 subjects, the profile’s thetamaximum was 38.8 ± 10.8% of that of thealpha band, the background ratio was 29.0 ±11.9%, and the ratio of the maximum ampli-tude increase in the theta band to that of thealpha band was 39.0 ± 11.0%.

In F4, in the same group of 11 subjectswho had an increased theta maximum in O2,such maximum was, on average, 120.7 ±39.9% of that of the alpha maximum, ex-ceeding 100% in 7 cases. In the resting EEG,this ratio was 100.1 ± 36.7% (93.8 ± 31.9%without subject T, see above). An increase in

amplitude spectra (compared to the back-ground) was at the theta maximum, on aver-age, 179.2 ± 112.6% of the alpha maximumincrease (Figure 3). In the remaining sub-jects, the profile’s theta maximum was 80.5± 25.5% of the alpha one, while the back-ground ratio was 79.7 ± 28.8%, and the ratioof the maximum theta increase to the alphaincrease was 67.3 ± 15.5%.

The ratio of the profile beta maximum tothe profile alpha maximum was also higherin F4 than in O2. In F4, in 14 subjects it was52.6 ± 17.9% in the driving profile, 83.2 ±47.6% (>100% in the same 5 subjects whodisplayed such prevalence in the theta band)

Figure 3. Group average driving profiles in the right frontal (F4) and occipital (O2) areas.Ordinate: amplitude spectra, in µV/√Hz individual values for each subject being rangedbefore averaging for each frequency band from maximum to minimum. Abscissa: fre-quency of intermittent photic stimulation and of EEG. Solid line: driving profile; dashed line:initial background; bars: change in amplitude spectra during stimulation in relation to thebackground.

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in the amplitude increase in relation to thebackground, and 36.4 ± 12.1% in the back-ground. In O2 these ratios were 32.5 ± 15.5%in the driving profile, 45.1 ± 33.9% in theamplitude increase, and 18.6 ± 6.1% in thebackground. Nevertheless, in F4, the profilemaximum in the beta band was only 49.2 ±10.9% of the alpha peak (Figure 3).

In F4, a relatively high amplitude of thedriving response to IPS of 3 Hz was alsoobserved, corresponding to 86.0 ± 25.7% of

the alpha peak. This ratio was substantiallyhigher than 42.7 ± 16.7% in O2. However,one can see in Figure 3 that a similar interre-gional ratio occurred in the resting EEG, i.e.,97.9 ± 26.7% and 36.5 ± 18.1%, respec-tively.

The specificity of the ratios between theamplitudes of the driving reaction in differ-ent frequency bands appears to depend onthe frequency structure of the backgroundEEG. In F4, similarly to O2 (3), a high levelof correlation between profiles and back-ground spectra was observed, with an aver-age correlation coefficient Rdb = 0.75 ± 0.15(P < 0.001; in O2, Rdb = 0.82 ± 0.13). How-ever, in O2, a decreased value of such acorrelation in some subjects was caused pre-dominantly by the appearance of an addi-tional maximum in the theta band (not pres-ent in the background spectrum) and its rela-tive weight in the overall profile. The ratio ofthe amplitude spectra of this maximum tothat of the alpha peak was negatively corre-lated with the values of Rdb (R = -0.77, P <0.001) (3). In F4, such a decrease in Rdbcould depend on a disproportionately in-creased driving response not only in thetheta band but also in the beta band. This wasreflected on the negative correlation of thevalues of Rdb with the amplitude spectra atthe maxima in both the theta (R = -0.78, P <0.001) and beta (R = -0.69, P < 0.01) bands.

The most pronounced theta driving in thefrontal and occipital areas was observed inthe same subjects: the theta maxima in theseleads correlated in this group with R = 0.75(P < 0.001).

In the brain areas of the same hemispheresituated between the frontal and occipitalpoles, an intermediate characteristic of thedriving profile form was observed. This wasreflected on the lower values of the Pearsoncorrelation coefficient between the profilesof relatively more distant scalp points (Fig-ure 4). The driving profile for O2 correlatedwith that of P4 (R = 0.80 ± 0.12, P < 0.001),C4 (R = 0.66 ± 0.23, P < 0.01), and F4 (R =

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Figure 4. Average driving profiles for 10 subjects with the peak alpha frequency of 10 Hz, inthe frontal (F), central (C), parietal (P), occipital (O), anterior temporal (Ta), temporal (Tm),and posterior temporal (Tp) areas. Ordinate: amplitude spectra, in µV/√Hz. Abscissa: fre-quency of intermittent photic stimulation and EEG. Solid line: profile for the right hemi-sphere; dashed line: profile for the left hemisphere.

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0.68 ± 0.21, P < 0.01). The profile of F4correlated with that of C4 (R = 0.94 ± 0.06,P < 0.001) and P4 (R = 0.74 ± 0.23, P <0.001).

The topographic differences describedhere in the profile shape occurred mainlydue to a general decrease in the relativeweight of the alpha activity towards the fron-tal region. However, a less pronounced de-crease in the voltage of the driving reactionwas also observed in the other bands (Figure4). For example, with respect to the 14 sub-jects, the average amplitude of the profilealpha peak in F4 was 3.49 ± 1.44 µV/√Hza or32.3% of 10.81 ± 3.17 µV/√Hz in O2, in theright hemisphere. In contrast, the profilemaximum in the theta band was 3.61 ± 1.38µV/√Hz or 54.4% of 6.64 ± 2.79 µV/√Hz inO2. With this exception, a certain differencebetween F4 and O2 was detected in the peakprofile frequencies in several cases, therebycontributing to decreasing somewhat the simi-larity between the profiles. From O2 (aver-age alpha frequency 9.57 ± 1.16 Hz) to F4(9.43 ± 1.45 Hz), the frequency of the profilealpha peak decreased in 2 cases and in-creased in 1 case. In the theta band, therewere both an increase and a decrease of theprofile peak frequency from O2 (4.86 ± 0.86Hz) to F4 (4.93 ± 0.73 Hz) - 5 cases each.

In the left hemisphere, the profile shapesand the amplitude ratios of the profile maximain the different bands were very similar sincethere was a high interhemispheric similaritybetween the symmetrical scalp point profiles(Figure 4). Relatively lower average Rs werefound between the posterior temporal (R =0.88 ± 0.08, P < 0.001) and the mid-temporal(R = 0.86 ± 0.13, P < 0.001) leads due to thelower values in some subjects, whereas inthe other area, the average R was 0.94 ± 0.05(P < 0.001).

In the alpha band, the prevalence of theprofile peak amplitude in the right hemi-sphere was significant only in the occipitalareas (P < 0.05) where the average ratio ofthe right peak amplitude to the left one was1.12, the right-side prevalence (ratio >1.0)being observed in 10 of 14 subjects. In mostcases (88%), the profile peak alpha frequencyin symmetrical leads was the same.

In the theta band, the significant right-side prevalence of the profile maximum (P <0.05) was also observed only in the occipitalareas, with an average interhemispheric ra-tio of 1.10 (>1.0 in 9 subjects).

Discussion

The present results show that in the pre-adolescent and adolescent children exam-ined the high responsiveness to the IPS wascharacteristic for all brain regions. Even inthe frontal ones, an increase in amplitudespectra relative to the background was ob-served in the most subjects at all EEG fre-quencies. Such an increase may serve as anadditional driving response indicator if weconsider that the non-specific orienting re-action to photic stimuli usually produces anamplitude decrease at the adjacent frequen-cies (3,5,30). It may be supposed that thedriving reactivity in the age group studied isincreased in comparison with that of adultsnot only in the occipital areas, as it was notedin our previous communication (3) on thebasis of literature data (1,2,16), but also inthe other areas.

The spectral peak criterion for the detec-tion of the driving response proposed in ourprevious communication (3) proved to beuseful in the topographic study of the phe-nomenon, especially together with the SFT.An application of the latter is very important

aThe unit of the power spectrum is µV2/Hz, as habitually used for the background EEG, and that of the amplitude spectrumtherefore is µV/√Hz. This will be used throughout the current work. In the driving reaction, consisting of sinusoidal oscillations ata number of well-defined frequencies, the amplitudes of the harmonics (in µV) can be calculated by multiplying the amplitudespectral values at the corresponding frequencies by 1.41 (for the spectral resolution of 0.5 Hz employed).

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for a statistical evaluation of the reactions tothe IPS, and it did confirm the significanceof most of the responses obtained, even ofthe low-amplitude ones in the anterior re-gions.

However, the discordant cases of the spec-tral peak and of statistical criteria are worthyof special consideration. According to thephysiological conception of the driving re-sponse, the resonance frequency selectivityis its principal feature. Thus, the detection ofchanges in the EEG at the IPS frequency bythe SFT without a spectral peak may beconsidered to be a driving response onlywhen there are no changes at the adjacentEEG frequencies. Otherwise, the changes,even when related to the IPS but not selec-tive for its narrow frequency, may be non-specific, such as the EEG desynchronizationas part, for example, of the orienting reac-tion and synchronization in the habituation(5,30). This type of EEG desynchronization/synchronization, in spite of being most pro-nounced in the alpha band, may take place inall other bands (31,32).

In some cases of selective EEG changesdetected by the SFT only at the IPS fre-quency, SFT proved to be a more sensitivedriving indicator than the spectral peak crite-rion, at least when the latter was taken at the20% level of excess over the adjacent fre-quencies. Indeed, most cases of SFT indica-tions not accompanied by the spectral peakcriterion fall on the anterior areas and on thehigher beta frequencies when the drivingresponses usually are of low amplitude. Thisneeds further investigation.

On the other hand, the orienting reactionduring IPS mentioned above may also resultin the spectral peak not confirmed by theSFT. In such a case, its effect of non-specificgeneral EEG desynchronization neutralizesthe selective driving synchronization, andthe latter forms a driving spectral peak with-out significant EEG changes at the stimula-tion frequency (or its harmonics) due to anamplitude decrease at the adjacent frequen-

cies. We described such a case for the alphaband in the previous communication (3).This may partially explain a relative preva-lence of these cases in the occipital areas atthe low frequencies of IPS presented at thebeginning of stimulation series when theorienting reaction must be most pronounced.

Thus, the two criteria used for the drivingresponse detection proved to be quite reli-able, sensitive and mutually complementaryinstruments in reviewing the estimate of thedriving topography.

The construction of an individual drivingprofile proved to be a quite convenient andinformative tool for a detailed assessment ofthe driving responses and for the quantita-tive comparison of the reactions to differentfrequencies of IPS in different regions. Theprofiles for the photic driving induced bystimulation frequencies from 3 to 24 Hzshowed that all the main features describedfor the right occipital area (3) were valid forall the other regions. Their correlation withthe background EEG spectra, showing maxi-mum responses at the dominating frequen-cies alpha and theta, further supports theresonance nature of the driving reaction(4,21,27,33-35) discussed in our previouswork (3). This correlation also means that inall brain regions, the reactivity to a given IPSfrequency is relatively stable since the mag-nitude of the response is usually propor-tional to the background amplitude spectraat the same EEG frequency, regardless of thestimulation times which are different fordifferent IPS frequencies. This makes pro-files maintain their shape in time and princi-pal amplitude proportions between the fre-quency bands characteristic for the back-ground spectrum but on a higher amplitudelevel. Thus, the profile may be treated assomewhat equivalent to a spectrum (3).

On the other hand, profiles may reflectthe latent power of some neuronal oscilla-tors (1,36-39) such as those of the thetapeaks revealed in children and adolescentsin our previous (3) and present research. In

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the background spectra, these peaks werenot observed in the occipital areas and wereless expressed in the other ones. This per-mits us to consider the driving profile to be amore complete representation of an individ-ual’s set of potential oscillators in compari-son with the resting EEG spectrum. In theprofile, the manifestation of these oscillatorsmay be seen at a higher synchronizationlevel, presumably closer to the maximum incertain cases, such as those of the alpha bandconsidered in our previous communication(3). For this reason, regarding the complexcharacteristics of an individual’s EEG, some-times it practically seems less importantwhether such a maximum in a profile isreached due to the resonance-like drivingmechanisms or beyond them (spontane-ously), although the magnitude of the driv-ing response itself in relation to the back-ground level reflects some special individualneurophysiological mechanisms of certainimportance for psychophysiological andclinical research and diagnostics. The prob-lem is that this magnitude is dependent onthe background state which is difficult tocontrol. The profile must reflect a relativelymore standardized functional state of thebrain due to external stimulation consideredto minimize uncontrolled subjective varia-tions in a current state (39). This demon-strates another advantage of the profile, whichwas found to be more stable than a restingEEG spectrum in an individual (3). The long-term stability of the frequencies of the indi-vidual driving reactivity in adults has beenconsidered to reflect constitutional featuresof the EEG (33,35,40).

Such individual stability, together withfeatures differing from those of adults, en-ables us to propose the use of the drivingprofile in children and adolescents as anindicator of the ontogenesis of the electricalactivity of the brain and as an individualcharacteristic of a developmental stage. Theprincipal peculiarity of the profile during theprepubertal and pubertal periods seemed to

be the additional theta peak, which was notpresent in the resting EEG spectrum of theoccipital areas (3). The study of the drivingreaction topography demonstrates an increaseof relative weight of the theta peak in theprofile up to its predominance in the anteriorareas. Even in the frontal region, where thetheta peak may be seen in the resting EEGspectra, the IPS selectively augments itsweight in comparison with the profile alphapeak. The results show that, in preadoles-cents and adolescents, the influence of themechanisms of generation of theta activity istopographically more generalized than itseems to be in the resting EEG. This mayprobably reflect the resting EEG structure inthe previous stages of development for whichan increased spectral power of theta anddelta activities is characteristic (2). This needsfurther investigation in younger age groups.

The responsiveness to at least 2/3 of theIPS frequencies presented, revealed in al-most any cortical area, proves to be of diag-nostic value for the topographic aspect of thedriving reaction in children and adolescents.This is a very promising development forfunctional brain mapping and its clinicalapplications. Therefore, the normative dataabout the peculiarities of the profile shape invarious cortical areas of healthy childrenand adolescents are important as controls forclinical studies. The topographic parametersof the normal driving reaction, such as theinterhemispheric symmetry of the profileswith some prevalence of the right hemi-sphere in the occipital areas, their gradualamplitude decrease in the frontal directionwith a decrease of intrahemispheric correla-tion and an increase of the weight of the thetapeak, etc., can be compared with those of thepatients with regional alterations in cerebralfunctioning of both an organic and func-tional nature (14-18,21-23). Our preliminaryresults obtained for some children sufferingfrom migraine actually demonstrated a pro-nounced interhemispheric asymmetry in theprofile shape not observed in the resting

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EEG spectra. They may probably reflect somedeficiency in the interhemispheric coordina-tion of the functioning of neuronal oscilla-tors of different frequencies (26). This find-ing seems promising for the study of theneurophysiological mechanisms of this typeof pathology, and may be important in elabo-rating electrophysiological methodologies fordiagnostic purposes. The data confirm theposition of some authors that the features ofthe driving reactions to IPS constitute themost reliable EEG indicators for the differ-ent types of headaches (37,38), and show

that the topographic aspect may substan-tially increase the informative value of thismethodology. Exploring the topographiccharacteristics of the driving responses maybe very important in EEG studies and for theneurophysiological attributions of regionalalterations in the functional state of the brain.

Acknowledgments

The authors are grateful to Dr. D.M.Simpson for his help with part of the soft-ware and for useful discussion.

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