Changes of asymmetry of EEG waves in different functional states

Neuropsychologia.

1966. Vol. 4, pp. 243 to 251. Pcrgamon Press Ltd. Printed in England

CHANGES OF ASYMMETRY OF EEG WAVES IN DIFFERENT FUNCTIONAL STATES E. Yu. ARTEMIEVA Moscow University Laboratory

and E. D. HOMSKAYA

of Neuropsychology,

Moscow, U.S.S.R.

(Received 20 December 1965) Abstract-Fourteen normal adult subjects in a state of rest revealed rhythmical oscillations of values of ascending and descending fronts of the alpha waves, regular periods being conserved (6-8 and often 7 set). The duration of period does not depend on an average level of asymmetry. The periodical oscillations of asymmetry break during the change of functional states such as sleep and arousal as well as during intellectual work (counting, etc.). Then the reaction of depression of alpha rhythm may appear. This phenomenon is related to the unspecitical form of activity which appears in the system of orienting reactions. A break occurs during the Ist-12th presentation of sounds in the periodical oscillations of the asymmetry and a change of its average level. These data disappear during successive stimulations (13th-25th) and appear again when the instruction to count sounds is given. The dynamics of asymmetry of slow EEG waves are interpreted as a reflection of the activity of the slow regulating system which provides a global control of the levels of activity of the brain. THE change of the functional state of the brain-the increase and decrease of the waking state-is reflected in some change in EEG. The activation of attention in cases of intellectual work or emotional stress is accompanied by blocking of the alpha rhythm and with increase of beta-activity [l-5]. There are nevertheless data showing the activation of attention (stimulus expectation, etc.) which results in an increase of alpha-activity [6]. There are some cases when no changes in the frequency spectrum of EEG rhythm-including alpha rhythm-are observed in states of active attention. In transition from waking states to sleep, changes of EEG are observed, depending on the functional state of the cortex. Several stages of sleep can be seen in the EEG. During the first stages which follow the waking states, a regular alpha rhythm which cannot be visually distinguished from the normal state of rest is dominant. Only in the last stages of a deep sleep do the irregular flat slow waves appear in the EEG [7]. Thus the transition from arousal to sleep is observed in some changes of excitatory and inhibitory states which are visually indistinguishable and which are not reflected in any shifts of the frequency spectrum of EEG. These shifts are essentially different if we use different parameters of the shape of the EEG wave. One such parameter is the A, proposed by GENKIN [8] for evaluation of the average asymmetry of time ascending and descending segments of alpha-waves during a period t. Some experimental data show that the process of oscillation consists of repeated cycles of activity and during the time of the alpha-wave some shifts of functional states are observed. These shifts can determine some behavioral reactions (latencies of motor reactions, etc.) as well. These are the basic data for use of the A-parameter. 243

244

E. Yu.

ARTEMIEVAand

E. D.

HOMSKAYA

Normal adult subjects observed in a state of rest have a relatively stable level of asymmetry of ascending and descending fronts of the alpha-waves. This asymmetry index varies in different subjects, remaining relatively stable in the same subjects [8]. No correlation between the asymmetry index and the dominant frequency in the alpha band is observed [9]. The level of asymmetry changes during the change of functional states-sleep, fatigue, arousal, as well as during intellectual work (problem solving, etc.). There is a high correlation between the asymmetry level and the speed and success of performance which requires a certain level of intellectually stable, controlled attention. No similar changes of this parameter during intellectual work in different subjects are observed. Some subjects are characterized by an increase in the asymmetry of the ascending and descending segments of the alphawave, others by a decrease of the same indicator. In both cases the average amplitude and the frequency spectre of EEG remained stable. The asymmetry index, as sleep ensues, changes toward increase of the level of asymmetry. In these cases the level of asymmetry decreases before conventional changes in EEG become visually observable. The changes of the asymmetry level during a certain task depend upon the general background. The higher this index is during the state of rest, the higher it is during the active state. The sign of the asymmetry can be helpful for diagnostics of the focal brain lesions [lo]. It can be supposed that the level of asymmetry of ascending and descending fronts of the alpha-waves reflects some important process of brain activity and that it is connected with the level of the functional states of brain activity. We used the parameter proposed by GENKIN[8] and we found that not only the average values of asymmetry but also the time-changes in At can give some important information concerning the different states of the subjects. We studied the changes of Ai values, i.e. average of asymmetry during 1 sec. The EEG recorded with an inkwriter (the speed of the paper was 60 mm/set) and was divided into periods of 1 sec. each. The value of A1 was evaluated in each period according to the equation : ‘i=&$

s

sinxjdf.

Separate measurements were made every 25 sec. * They were symbolized by (.) if they reflected the phase of increase of the amplitude, and by (/) if they reflected the phase of decrease of the amplitude. The value of Ai was equal to the relation of the differences of number (.) and (/) to the average quantity of waves during 1 sec. We found that in normal subjects rhythmical oscillations of A1with a strict preservation of periods [ll] is observed. These oscillations will be called G-waves. Figure 1 (A, B, C and D) shows the results of the analysis of EEG recorded in four normal subjects in a state of rest. All of them had a clear alpha-rhythm. A bi-polar record of EEG from the accipito-parietal region of the brain was made. *&the length of the ascending phase of the alpha-waves; &length of the descending phase (a summarizing and integration is made during all oscillations of this section of EEG); X, and xi-records of EEG and its derivatives; -1 if xO.

CHANGES

OF ASYMMETRY

OF EEG WAVES

IN DIFFERENT

FUNCTIONAL

STATES

245

FIG. 1. Slow periodical oscillations of the asymmetry of the phase of alpha waves (G-waves) when no stimuli were given (“background”). A, B, C, D-four different normal subjects. Each segment of the abscisse is 1 set; ordinate-values of Al.

In all the subjects the values of A1 change rhythmically during 30-40 min of the EEG recording. Maximums and minimums of A1 oscillate very regularly. These regular oscillations will be mentioned here as “G-waves”. The values of the period are different in different subjects (6-8 set, mostly 7 set) with the deviation of f 0.5 sec. The periods of oscillations are independent of the average level of the asymmetry. In case A the asymmetry was positive; in case B it was negative; but the period remained unchanged. With active attention during intellectual tasks the G-waves become irregular and oscillations of values become less regular. Figure 2 (A, B and C) shows the successive changes in three normal subjects during the state of rest and during intellectual task (counting). It is clearly seen that the beginning of touting is reflected in a break of regularity but the stopping of counting is reflected in a restitution of the initial regularity of oscillation (Fig. 2A). It must be mentioned that such changes of EEG during rest and during intellectual activity (calculation) could not be discriminated by visual analysis of the curves. In all the subjects such changes cannot be detected in the brute EEG. In cases when the intellectual activity was associated with a depression of the alpharhythms, a marked alteration of the regularity of the asymmetry was seen, which preceded the depression of the alpha-rhythm (Fig. 3). The same changes were associated with the end of the depression of the alpha-rhythm. Thus it was clear that the transition from one functional state to the other is reflected in two successive stages; namly a breakdown of the regularity of the oscillation of the asymmetry of the alpha-waves, and a successive depression of the alpha-rhythm, or the reverse. A clear correlation of the dynamics of the phenomena mentioned and the general

E. Yu.

246

C

ARTEMIEVA

w

and E. D. HOMSKAYA

mmtirq

Fro. 2. Disturbances of rhythmical oscillations of asymmetry during intellectual activity (arithmetical problems) A, B, C-three different normal subjects. Under each graph are records of EEG during 3 set; vertical line-the beginning of the task given. No visual differences in both periods of EEG records are seen.

‘Depression RG.

3. Disturbances of regular oscillation of asymmetry preceding the depression of alpharhythm in normal subject.

state of the subjects was seen. When he was undisturbed and alert, G-waves remained stable during the whole session (Fig. 4A, 1, 2) and during different sessions (Fig. 4B, I, 2, 3,).

It is remarkable that these waves have certain characteristic features for the same person (Fig. 4A, 1, 2).

CHANGFS OF ASYMMETRYOF EJZG WAVE3 IN DIFFZRENT

PIJNCIlONAL

STATPS

247

FIG. 4. Slow periodical oscillations of the asymmetry and corresponding EEG records during different functional states. A, B, C-three different normal subjects.

When the subjects were excited (Fig.4B,4) or drowsy (Fig. 4C, 2) or exhausted (Fig. 4A, 2) the periodical oscillations of the index do not appear, but when placed in other conditions, the same subjects show a remarkable stability of periodical oscillations (Fig. 4A, 1; Bl, 2; Cl). This is, perhaps, why we were unable to see these regular periodical oscillations at the beginning of the session. Thus it can be seen that when the level of wakefulness has increased and when there is a state of arousal, or increased attention, or excitation, or when the above level decreases as in fatigue, a drowsy state and so on, the periodicity of the G-waves is broken. It is obvious that the periodicity of the oscillation mentioned is conserved only when some optimal level of wakefulness or some optimal fwtctionai level remains stable. The appearance of the changes of this periodicity just a little before the moment when a depression of the alpha-rhythm takes place is more evidence of these facts. We can conclude that not only the value of the asymmetry of the ascending and descending fronts of the alpha-wave during a long period of 30 set to 5 min, but also the timechanges in AI as well can be used as an indicator of the functional state of the subject.

E. Yu. ARTEMIEVAand E. D. HOMSKAYA

248

The insufficient reliability of the Al index is due to some peculiarity of the calculation technique (the average from the 10 waves which has a considerable variation), and also to some failures of the parameter A, itself [12]. That is why in some cases we do not find G-waves; we are not sure if this is so because of the absence of the periodical oscillations we try to find, or because of the technique used. What can be said concerning the nature of the asymmetry changes of the alpha-waves? It can be supposed appears

that this parameter

in the system of the orienting

is related reactions.

to the unspecific form of activity which The proof would be that G-waves should

obey the rules of the orienting reflexes, i.e. they should disappear in repetition of the stimuli and reappear when the stimuli receive some new significance. A special study was made to prove these data. In eight normal subjects (20-35 years old) with a stable alpha-rhythm the changes of the A were studied during repeated presentation of interrupted sounds of a moderate medium intensity (60 dB) the length of which was 0.5 set and with 6-12 short sounds in each pattern (first series). In the second series a verbal instruction to count these sounds was given; in the third series this instruction was countermanded. The EEG was recorded from occipital-parietal regions of the left hemisphere (bi-polar method); the speed of the ink recorder was 60 mm/set. The subject was placed in a soundproof cabin. An electroencephalograph “Alvar” was used. Subjects with a stable alpha rhythm were chosen which gave little or no depression when stimuli were given. No visual differences in the brute EEG during the presentation of indifferent and significant stimuli (series I-III) were seen. In cases when a depression of alpha rhythm was observed, it was allowed to habituate in one or two preliminary sessions and only after that did the basic experiment take place. Equal sections of EEG records were analyzed; these equal sections were singled out from the time before stimuli were presented (background data) and from the sections when sound stimuli were given. The relation of the difference (.) and (/) to the average number of waves measured during these sections was used as an index of the asymmetry. The cases when the asymmetry of the background was markedly greater than the asymmetry of the period of stimuli presentation were symbolized in the experimental protocol with (+ +). When this difference was only slight, it was symbolized with (+). The symbols (- -) and (-) were used in opposite cases; (0) signified absence of changes mentioned. In cases when a depression of alpha rhythm with presentation of sound stimuli was seen and the evaluation of our index became impossible, the symbol (“D”) was used. In the majority of our cases no depression occurred. Experiments showed that the average values of the asymmetry of the ascending and descending front of alpha waves changed differently in jrst and successive presentations of sounds. During the Ist-12th presentations, all subjects showed systematic changes of the asymmetry as compared with background values; increases as well as decreases of the index took place. During later stimulations (13th-25th presentations) the asymmetry index did not change significantly and the relation between these values and the values of the background became random. All these differences are easily seen from the summarized graph where all data of asymmetry in the background relative to the time of sound presentations are shown (Fig. 5).

CHANGES OF ASYMMJXRY OF EEG WAVES IN DIFFBRENT FUNCXIONAL STATES

249

The ordinate of the point is represented by a number equal to the sum of values in both records of EEG. When the value was expressed by one channel, the value was doubled. This technique could only mask the differences but it did not result in an illusory difference when no real difference was observed. Figure 5 shows that during the presentation of the lst-12th sounds a regular change of the asymmetry of the alpha wave takes place: as is seen, nearly all points are above the absciss, line when the next series of sounds (13th-25th) are presented the points changed their place which fact reflects variable changes of the asymmetry index. The instruction to count sounds resulted, in all eight subjects in marked changes in asymmetry which appeared during the presentation of the sound stimuli. These changes were stastitically significant (P=O.O5). I - I2 ..... ...... ... ... ..... ...... . . ... . t Sounds,

Sounds 13-25 . . . . . . . . .. . -t

:.. . .. . .. . .

Instr.” Let’s count please”

Instc “Don’t count”

. . . . .. . .. . . t . . .

t

. .

+

. .

. . . .

Fro. 5. Changes of asymmetry of the phases of the alpha waves. Summarized data obtained in eight subjects (comment in text).

The elimination of the instruction resulted in a restitution of the irregular variation of the assymmetry during the period when sounds were presented (Fig. 5). There were statistically significant changes in asymmetry when indifferent sounds were presented and in cases when the subject had to count the signals. These can be seen in Fig. 6 which shows that when the second interrupted sound complex was presented, breakdown of periodical oscillation of asymmetry of alpha waves is seen (Fig. 6A). In the course of 15, 16 and 17, /Sound2

FIQ. 6. Changes of G-waves with presentation of the interrupted sound stimuli in normal subjects. A-presentation of the second sound (periodicity of G-waves is broken); Bpresentation of the 15th-16th-17th sounds (periodicity of G-waves is conserved); C-the instruction to count the sounds results in a change of asymmetry (the oscillation of the asymmetry becomes chaotic).

sound stimuli G-waves do not lose their regularity; the periods of oscillation remain 6-7/set with a deviation 0.7 (cf. Fig. 6B). When subjects started to count the signals (Fig. 6C) the oscillations of the asymmetry lost their periodical character.

250

E. Yu. Aarnt.nsv~ and E. D.

HOMSKAYA

It can be seen that the dynamics of average values of asymmetry of the alpha-rhythm and of the periodical oscillations (G-waves) in the background as well as during presentation of irrelevant and meaningful signals are similar to the dynamics of the orienting reflex. These indices disappear after presentation of a series of similar stimuli (habituation), and they appear after the orienting reflex is restored or after the conditional reflex is established [13]. These data prove that the fluctuations of the asymmetry of the alpha waves and of the dynamics of the periodical oscillations of Al reflect the unspecific form of activity similar to the other components of the orienting reflex. That is why a correlation of the fluctuations of the asymmetry of the alpha waves with a series of components of the orienting reflex (vegetative, sensory and motor) is of considerable interest. Changes in the asymmetry of the ascending and descending fronts of the EEG waves and the periodicity of these oscillations can find its place among other indices of the orienting reflex (depression of the alpha-rhythm, secondary responses, changes of steady potentials, K-complex, etc.). The use of this parameter offers new vistas in analysis of different functional states in normal subjects as well as in subjects with local brain injuries. The periodical oscillation of the asymmetry of the EEG-waves seems to bear a close relation to the extra-slow rhythmical changes of potentials [14] observed in different brain structures. These electrical states which according to ALAJALOVA [14]are reflected in continuous changes of the excitability of the nervous elements are related to the slow humoral system which has to be distinguished from the fast nervous regulating system. The similarity of the temporal parameters described by ALAJALOVA [14],extra slow oscillation and periodical fluctuations of the asymmetry of the EEG waves suggest that all these data are related to the same slow regulating system, which provides a global and continuous control of the activity levels of the brain.

REFERENCES Arch. Psychiar. Nervkrankh. 99, 1. BERGER,H. &r.r das Elektroencephalogramm des Menschen-VI. 555-574. 1933. G. W. Normal rhythms, their development, distribution and significance. In Electroencephalo2.WAL.TER, graphy. Edited by HILL, D. and PARR,G. pp. 202-228. London, 1950. 3.MUNDY-C~TLE, A. C. EEG and mental activity. Electroenceph. clin. Neurophysiol. 9. 643-657, 1957. 4. OSWALD, J. The EEG, visual imagery and attention. Q. Jl exp. Psychol. 9, 113-119, 1957. WERRE.P. E. DE. Interrelation between Psvcholoaical and EEG Data in Normal Adults. Leiden 1957. Z: BARL&, J. Cited by DE LANGE,G. W. N., Srr&t VAN LEWEN, W. and WERRE,P. W. Correlation between psychological and EEG data. In EEG Investigation of Higher Nervous Activity. pp. 368-377. Moscow, 1962. 7.Loom, A., IIARVEY,E. and HOBART,G. Electrical potentials of the human brain. J. exp. Psychof. 19, 249-279,1936. 8.GENKIN,A. A. The asymmetry of the phases of EEG in mental activity. Proc. Acad. Sci. USSR 149, 1460-1462, 1963 (In Russian). 9.GENIUN,A. A. The Length of the Ascending and Descending Fronts of EEG as a Source of Information about Neurophysiological Processes. Ph.D. Thesis, Leningrad, 1964 (In Russian). N. I. and GENKIN,A. A. Essays in application of nonparametrical statistics in analysis of 10. MOI~~EIVA, EEG in vascular diseases of the brain. Zh. Nevropat. Psikhiat. 63, 1147-l 152, 1963 (In Russian). L. D. Analysis of A parameter in asymmetry of the length of the 11. ARTEMIEVA, E. Iv. and MESHALKIN, ascending and descending fronts of alpha-rhythm. Novyie Issled. Pedag. Naukach 4, 1965 (In Russian). L. D. and HOMSKAYA, E. D. The periodical oscillations of the asym12. ARTJMEVA, E. Iv., MESHALKIN, metry of ascending and descending fronts of alpha-waves. Novyie Issled. Pedag. Naukach 3, 249-251, 1965 (In Russian).

cHANoBs

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ASYMMETR YOFEEoWAvBpIND-

PUNCTIONALSI’ATES

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13. H~MXAYA, E. D. The influence of verbal instructions on vascular and galvanic skin components of the orienting retlexes in local brain lesions. In proceed. Acad. Pedug. Sci. No. 6, 1960 and Nos. l&2, 1961 (In Russian). 14. ALAJNAFJA, N. A. Slow Electrical Processes in the Brain. Acad. Sci USSR Press, Moscow, 1962 (In Russian).

R&sum&Chex 14 ad&es normaux en &at de repos des oscillations rythmiques des valeurs des ondes alpha dans leur portion ascendante et descendants apparaissaient selon des p&odes strictes (6/S et souvent 7 secondes). La dun% de la p&ode ne depend pas du niveau moyen d’asym&rie. Les oscillations periodiques asymetriques sont supprim& durant les modifications des etats fonctionnels tels que le sommeil et l’eveil, de m&ne que durant le travail intellectuel, par exemple dans l’activite de compter. Alors, la reaction de depression du rythme alpha peut apparaltre. Ce phenomene est relit il une forme non sp&cigque d’activitd qui se manifeste dam le syst&me des reactions d’orientation. Une rupture survient durant la premiere il la dou&me presentation des sons dam les oscillations p&iodiques de i’asymetrie, ainsi qu’une modification du niveau moyen. Ces faits disparaissent dans les stimulations successives (de la 13eme a la 2%~) et apparaissent de nouveau lorsqu’il est command6 de compter les sons. La dynamique de l’asym&rie des or&s lentes est interprMe comme rt%Miissant I’activite d’un syst&me regulateur lent, systeme qui procure un contr6le global des niveaux d’activite du cerveau. Zusamme&sswq-Vierzehn normale, erwachsene Personen, im Zustand der Ruhe, xeigten rythmische Schwankungen von Werten in den aufsteigenden und absteigenden Linien der Alpha-Wellen, wobei regelm%ge Perioden erhalten blieben (6-8 und oft 7 set). Die Periodendauer ist nicht abh&ngig vom durchschnittlichen Asymmetrie-Niveau. Die period&hen Asymmetrie-Schwankungen werden unterbrochen w&rend des Wechsels von Funktions-Zustinden wie Schlaf und Wachen sowie such wiihrend geistiger Arbeit (Rechnen etc.). Dann kann die Depressions-Reaktion des Alpha-Rythmus in Erscheinung treten. Dieses Ph%nomen steht in Eteziehung zur unspezifischen Form der Aktivititt, welche im System nascierender Reaktionen erscheint. Eine Unterbrechung tritt ein w&end des ersten bis xwolften Auftretens von Tonen in den period&hen Asymmetrie-Schwankungen, sowie eine Anderung ihres Durchschnitts-Niveaus. Diese Ergebnisse verchwinden withrend aufeinanderfolgender Reizungen (13.-25.) und erscheinen wieder, wenn die Instruktion gegeben wird. Tone zu ahlen. Die Krtifte-Wirkung der Asymmetrie in langsamen EEG-Wellen werden gedeutet als eine Reflektion deerAktivitfit des langsam regulierenden Systems, welches eine unfassende Kontrolle der Schichten der Himtatigkeit vorsieht.