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Multichannel topography of human alpha EEG fields
439
Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands
MULTICHANNEL
TOPOGRAPHY
OF HUMAN
ALPHA
EEG FIELDS 1
D . LEHMANN 2
Smith-Kettlewell Institute and Department of Visual Sciences, University of the Paci/i'c, San Francisco, Calif 941 I5 (U.S.A.) {Accepted for publication: April 20, 1971)
The phenomenology of the EEG in the space domain, i.e., the description of the changes of electrical field distributions on the scalp as a function of time is still incomplete, although a considerable amount of indirect information has been accumulated. Particularly, the topography of alpha EEG has been studied since the first description of the human EEG, in the hope of gaining insight into the mechanisms which generate the EEG (Adrian and Yamagiwa 1935; Brazier 1949). Several multichannel systems for amplification and display of the EEG have been constructed (Lilly 1954; Ananiev 1956; Walter 1959; DeMott 1966). However, direct mapping of the EEG potential fields has been hindered by the problem of simultaneous recording of EEG in many channels. Recent field studies used 14-32 channels, combined with interpolation during processing (Bickford 1969; Bourne et al. 1969; Estrin and Uzgalis 1969; Petsche 1970). Phase relationships of alpha waves from different scalp areas were investigated with various techniques (Petsche and Marko 1955; Bekkering et al. 1957; Garoutte and Aird 1958 ; Walter 1959; Cooper and Mundy-Castle 1960; Liske et al. 1967; R6mond et al. 1969; Shaw 1970). Typically, much larger phase lags were seen in fronto-occipital than in transverse comparisons (Garoutte and Aird 1958; Walter 1959). One aspect of the phase relations of local alpha, the apparent migration of EEG waves, was emphasized particularly (Petsche and Marko 1955). This research was supported in part by National Institutes of Health, U.S. Public Health Service Grant NB 06038 and FR 00241. 2 Present address: Labor fiir Neurophysiologie, Neurologische Universit~tsklinik, Kantonsspital, 8006 Ziirich,
Switzerland.
Other studies dealt with the number and location of generators which could model the EEG. The typical finding of two phase reversals in occipital chains of electrodes indicated the existence of a generator in each hemisphere (Walsh 1958). A four-generator model which could account for averaged alpha in parietal areas was developed from EEG data sampled from electrodes in chain or cross arrangements (Joseph et al. 1969; R6mond et al. 1969). Application of Fourier transformation to the EEG yielded constraints about the minimum number and the location of postulated EEG generators (Walter et al. 1966; Larsen 1969). The present paper gives a phenomenology of typical EEG alpha field distributions on the human scalp, using a 48-channel recording system for off-line mapping of the scalp EEG fields. Some preliminary results were reported earlier (Lehmann et al. 1970). METHOD Five adults, 22-33 years of age, served as subjects. The subjects were taken at random from a subject pool. In conventional recordings, wellorganized alpha occurred frequently in three subjects, and less frequently in two subjects. The data presented here were obtained after a series of experiments which explored characteristics of the recording system, electrode placements and data handling strategies. The subject sat in a comfortable chair in a shielded darkroom, with his head in a chin and forehead rest. An intercom system provided communication with the experimenter. The scalp EEG was recorded from 38 to 45 Grass gold cup electrodes attached to the scalp with Grass electrode paste at approximately equal inter-electrode distances. The number of Eh,ctroenceph, clin. Neurophysiol., 1971, 3•:439 449
440
D. LEHMANN
electrodes is determined by several factors: the number of recording channels, the desired placement geometry (symmetrical around midline electrodes), the space on the scalp available for conventional electrodes and the time required for the attachment of the electrodes. The area covered by the electrode array differed slightly from experiment to experiment and is generally described by a line from the inion to the ears to approximately Fz. The inter-electrode distances were between 3.5 and 4.2 cm, depending on the subject's head dimensions and the number of electrodes, [ c~ocK60°°c / , ~ - ~ [ ,o s,~s
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The data collection was performed with an average reference (see Fig. 1). A 48-channel system was used for recording. The system was designed and built in our laboratory by Mr. Julius M. Madey. Fig. I illustrates the principal components of the system. The pre-amplifiers have a gain of 5000, a bandpass of 0.5-100 c/see (half amplitude) with 12 dB down per octave, 1.8 /~V noise peak-to-peak (0.23 /~V root mean square), an input impedance of 100 MfL and a common mode rejection ratio of 1:50,000. The output of each pre-amplifier was sampled at a rate of 750/see; the sampled output was multiplexed in 6 groups of 8 channels, post-amplified and recorded on 6 tracks of an instrumentation tape recorder as amplitude-modulated signal.
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Fig. 2. Computer print map of the distribution of field values on the scalp (in 10ths of/~V, referred to the mean of all values). Head seen from above, anterior is up. 9999 indicates locations not used. The electrodes which recorded the positive and negative maximum values are identified on the right. Equipotential lines were sketched in by hand.
Electroenceph. clin. Neurophysiol., 1971, 31 : 439M49
441
MULTICHANNEL TOPOGRAPHY OF ALPHA EEG FIELDS
ofskull-brain relations. The distortion inherently necessary for the projection of a three-dimensional surface into two dimensions is of no consequence in the present study. In a given map, the arithmetic mean of the instantaneous potential values recorded from all channels (which is in fact the value of the average reference) was used as zero level. The sampling interval between maps was 1-8 msec. If necessary for survey of the map series, equipotential lines were sketched in by hand as shown in Fig. 2. The computer output also identified theelectrodes which had recorded the positive and negative maximal values in each map. Further, the average, absolute amplitude per electrode was computed for each map. The average, absolute amplitude per electrode is the sum of the absolute potential differencesbetween the local potential recorded by each electrode and the mean of the potentials recorded by all electrodes in a given map, divided by the number of electrodes used. Given equidistant electrodes, the value "average, absolute amplitude per electrode" is an indicator of the degree of relief or "hillyness" of the field distribution. From each subject, at least 30 min of spontaneous EEG were recorded during relaxation with closed eyes; after editing for accessability and artifacts, approximately 10-15 min of alpha EEG were available for processing. From this material, well-organized alpha EEG epochs of 500-1000 msec duration were selected for further analysis. For each subject, 2-7 see of alpha were analyzed. RESULTS
Examination of a series of equipotential maps obtained during alpha activity shows that some fielddistributions occur repeatedly with the same or opposite polarity. For instance, during the alpha cycle mapped in Fig. 3 we find similar field distributions with inverted polarities at 425 and 465 msec, and at 449 and 505 msec. The interval between similar distributions of inverted polarity is approximately 50 msec, i.e., one-half of one alpha cycle. Generally, the field distributions are simple, centering around one or two positive and negative maximal values in each m~p (Fig. 3). This suggests the location of the
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The upper number indicates the a m o u n t of relief in each m a p (average, absolute amplitude per electrode in microvolts); the lower number is the time in milliseconds, referring to Fig. 5, of which Fig. 3 illustrates a portion.
positiveand negative maximum in each map as descriptor of the dominant characteristics of the distribution. Plotting of the location of maximal field values shows that they tend to occur within relatively small scalp areas, which we call preferentialareas. A case of three preferential areas is illustrated in Fig. 4, where the entries indicate the frequency of occurrences of positive and negative maxima at the different electrode positions during a 640 msec epoch of alpha activity (including the sequence of Fig. 3) sampledin intervals of 8 msec. The maxima Electroenceph. clin. Neurophysiol., 1971, 31:439~t49
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Fig. 4. Location of maximal values of the fields during 640 msec of alpha (including the epoch shown in Fig. 3). Sampling in 8 msec intervals. Each dot or number represents one electrode. The numbers give the percentage of time that the maximal value occurred at the indicated electrode location. The most anterior (first) midline electrode was approximately 7 ~ of the distance nasion-inion behind Fz, the second at Cz, and the sixth at the inion. Values in A are not always the mean of corresponding values in B and C, and the totals are not equal to 1 0 0 ~ , because of rounding to multiples of 1'~. Electrodes with 6 or more percent time of occurrence are shaded. Dotted lines in A delineate the three preferential areas {see text) used in Fig. 5.
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7 of t h e 3 8 electrodes during appr6~ximately 6 3 ~ of the time, and at the remaining 31 electrodes during approximately 40 ~ of the time (rounding to multiples of 1 ~ brings the total to 103~). The results are largely similar when positive and negative maxima are treated independently (Fig. 4, B and C). The three clusters of preferred electrode locations for the maxima are located over anterior, left occipital and right occipital areas. For further data reduction, the three preferential areas were 'defined as the electrode sites with 6 ~ and more time incidence of occurrence of positive and negative maxima, plus all neighbor electrodes unless contested by an adjacent preferential area. Demarkation lines of these preferential areas are dotted in Fig. 4, A. The anterior area is larger than the occipital areas. This is a typical finding, and more detailed examination of the data shows
Fig. 5. A : Location of positive (POS.) and negative (NEG.) maximal field values as a function of time, in the three preferential scalp areas of Fig. 4: anterior (ANT.), occipital left (OC.L.), and occipital right (OC.R.), B: Concomitant changes of the amount of relief of the whole field (average, absolute amplitude per electrode). C: Changes of local field values as a function of time at the three electrode locations in Fig. 4, A with highest percent time of occurrence of the field maxima: l=anterior, 11 ~ ; 2=occipital left, 11 ~,/,; 3 =occipital right, 13 ~o. Sampling in 8 msec intervals. Fig. 5 is based on the same data as Fig. 3 and 4.
that the maximal value drifts over time within the anterior area, i.e., the maximum occurs at neighbor or next neighbor electrodes during successive alpha cycles. The time of occurrence of the maxima in the three preferential areas of the sample epoch is illustrated in Fig. 5, A. There is a repetitive, rotational sequence ofthe location ofthe positive and negative maxima, in the following order: anterior, left occipital and right occipital area. In each preferential area, positive and negative maxima alternate, each at approximately 10 c/sec. The magnitude of the phase lags between waves recorded from the three preferential areas is illustrated in Fig. 5, C, which demonstrates the large phase difference anterior-posterior, and Electroenceph. clin. Neurophysiol., 1971, 31 : 439 449
MULTICHANNEL TOPOGRAPHY OF ALPHA EEG FIELDS the m u c h smaller lags between hemispheres, Fig. 5, C also shows the typical variance in phase lags from cycle to cycle. It should be noted that in Fig. 5, A, only information on the direction of phase lags of the field fluctuations in the three areas is represented ; there is no information on the m a g n i t u d e of the phase lags, since only one positive and one negative field m a x i m u m was determined for each time slot. The a m o u n t of relief of the field (the average, absolute amplitude per electrode) is shown as a function of time in Fig. 5, B. A periodic fluctuation of the field relief is evident at a rate of a p p r o x i m a t e l y 20/see, twice the alpha frequency, During successive peak times of the relief curve, the field m a x i m a are found alternately in the anterior area or in the occipital areas (see also Fig. 3). N o t e w o r t h y is one missing "beat" of the fluctuations of the relief at a p p r o x i m a t e l y 370 msec in Fig. 5, A, an event that was observed in
443 three records; the cyclic sequence of locations of field m a x i m a was not interrupted, merely the relief of the distribution remained low. Let us now consider another alpha sequence recorded from a second subject. Sample m a p s are shown in Fig. 6. The general features of the fields are similar to those in Fig. 3, but four preferential areas for location of field m a x i m a can be distinguished (Fig. 7). Electrodes frontal to the anterior preference location were included in the anterior preference area in Fig. 7, A. The sequence of the occurrence of the field m a x i m a (Fig. 8, A) now is anterior, right occipital, left occipital and left ear, contrary to the previous example. However, toward the end of the alpha spindle, at a p p r o x i m a t e l y 700 msec, there is a reversed sequence, a c c o m p a n i e d by declining organization of the relief cycles (Fig. 8, B) which change to slower frequencies and disappear. Fig. 8, C demonstrates that the alpha spindle starts and ends at s o m e w h a t varying times in t
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Common characteristics in all subjects The location of the scalp preference areas for
B. pos. MAXIMA
Fig. 6. Sequence of equipotential maps of alpha EEG. Time of each map is indicated in milliseconds, referring to Fig. 7 and 8, of which Fig. 6 illustrates a portion. For other explanations, see Fig. 3.
C. NEG, MAXIMA
Fig. 7. Location of maximal values of the fields during 1024 msec of alpha (including sample shown in Fig. 6). The most anterior (first) midline electrode was approximately 5 },; o4 the nasion-inion distance in front of Fz, the third electrode at Cz, and the seventh electrode at the inion. Dotted lines delineate preferential areas used in Fig. 8. For other explanations, see Fig. 4. Electroenceph. c/in. Neurophysiol., 1971, 31 : 439 449
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Fig. 8. A : Location of positive and negative maximal field values as a function of time in the four preferential scalp areas of Fig. 7: anterior (ANT.), occipital right (OC.R.), occipital left (OC.L.), and left ear (L.E.). B: Changes of the amount of relief of the whole field (average, absolute amplitude per electrode). C: Changes of local field values as a function of time, at the four electrode locations in Fig. 7, A with highest percentage of time of occurrence of field maxima : 1 = anterior, 9 ~ ; 2 =occipital right, 16 %; 3 =occipital left, 14 %; 4 = left ear, 8 %. Sampling in 1 msec intervals. Fig. 8 is based on the same data as Fig. 6 and 7.
Electroenceph. clin. Neurophysiol., 1971, 3l: 439 449
MULTICHANNEL TOPOGRAPHY OF ALPHA EEG FIELDS
A
445
B
Fig. 9. Average distribution of maximal values of alpha E E G fields on the scalp. Mean of five subjects. Values in percentage of time per electrode. For visualization, contour lines were interpolated linearly between the values at the electrode positions. Percentage levels are differentiated by shading, as illustrated below Fig. 9, B. A : Electrode array includes ears. B : Electrode array with scalp electrodes only; ear values were substituted by secondary maxima on the scalp. The insets indicate the electrode positions. The circled electrode is at the vertex, the most posterior midline electrode is at the inion. Dots indicate electrodes with less than 3 ~ occurrence, open circles with more than 3 ~ occurrence.
field maxima during EEG alpha exhibited a considerable similarity in the five subjects. Fig. 9, A demonstrates topographically the frequency of occurrence (in percentage of time) of the scalp field maxima during alpha activity, averaged over the five subjects. The average frequency of occurrence was computed for each electrode, using the frequency-of-occurrence data of the first alpha epoch which had been selected for analysis in each subject. Electrode positions that had not been used in all subjects were excluded from the average. In maps where the maximum occurred at one of the excluded electrodes, the next lower value in the remaining electrode array was used, thus covering 100~ time for each analysis epoch. Fig. 9 shows that the field maxima occur preferentially in a well-defined area. Seen from the occiput, this area has the shape of an inverted Y over the sagittal midline. Peak frequencies of occurrence are found near the vertex, at the left occiput, and particularly at the right
occiput. In addition, both ears frequently record maxima. The inspection of original maps suggests that an ear electrode often is nearly equipotential with distant electrodes. To clarify this impression, the data of three subjects who had a row of electrodes just frontal to Fz were examined. Data collected from the left ear electrode were excluded from the determination of maximum values: in each map which originally showed a maximum at the left ear, the location of the next highest field value (secondary maximum) was plotted as maximum in Fig. 10, A. The secondary maxima tended to a distribution along the circumference of the electrode array, especially preferring the contralateral ear. This contrasts with the distribution of the secondary maxima after the exclusion of a left occipital electrode (Fig. 10, B), where these substitute values are reasonably centered around the original location; there is some spread to the right occiput as Electroenceph. olin. Neurophysiol., 1971, 31:439 449
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dominated in each subject. However, the limited material does not allow us to decide whether individuals preferentially show one direction of progression of field maxima. The field reliefs of all subjects exhibited 20/sec fluctuations consistently during alpha EEG.
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Fig. 10. Distribution of second highest field values, average of three subjects. Numbers indicate percentage of time of occurrence of secondary maxima. A: Original maxima were at left ear (x), Note the high incidence at the contralateral ear. B: Original maxima were at left occipital electrode ( x ).
Circle indicates vertex electrode. For further discussion see text. expected with the usual small phase lag between the oscillations in the two occipital areas. The average distribution of the field maxima of the whole population (Fig. 9, A) changed only slightly when the values at both ears were excluded and substituted by secondary maxima (Fig. 9, B). Next, we examine the difference between the occurrence of maximal values in preferential and non-preferential areas. Electrode positions showing 3% and more time of occurrence in Fig. 9 were considered preferential. There were 15 (14) preferential and 21 (20) non-preferential electrode positions in the averaged map. (Values after the exclusion of the earlobe data are in parentheses.) The mean frequency of occurrence per electrode over subjects was 5.38 (5.52) % for preferential electrodes vs. 0.92 (1.14)% for nonpreferential electrodes. The difference was significant at P < 0.005 (< 0.005) in paired t tests, Further, preferential and non-preferential electrodes were compared in each subject. The designation of electrodes as preferential or nonpreferential in the population average of Fig. 9 was used also for the individual subjects. The difference between the frequencyofoccurrence of maxima at preferential and non-preferential electrodes was significant for all subjects (P < 0.005 in rank tests), indicating a high consistency of the location of preferential areas between subjects, Progression of the field maxima in clockwise and counter-clockwise direction was seen in all subjects, although usually one direction pre-
Direct plotting of the relatively simple scalp fields was possible because of the number (48) o f available recording channels; a n array of m o r e than 4 by 4 electrodes is necessary t o
detect more than one positive and negative peak in a field. No interpolation was used for the estimation of the location of maximal field values. These maxima were found preferentially in a pre-vertex to parietal midline area, a left occipital, and a right occipital area. In simple Conditions, the maximum of a surface field will be located perpendicularly over its generator. However, the conspicuous extensions of the anterior preference area along and to both sides of the midline raises questions about the anatomical and physiological relevance of the localization. In fact, distortion of the projection of cortical areas onto the scalp is known (Driscoll and Rush 1969), and the central fissure may function as a mediator for distortion. It appears that the assumption of three stationary generator areas, each oscillating at approximately l0 c/sec, can account for the major phenomenological properties of the ohserved alpha fields. The field oscillations are not in phase in different scalp areas (e.g., Walter 1959; Liske et al. 1967), and vary around a center frequency (Garoutte and Aird 1958). Thus, the generators may well be semi-independent under the control or coordination of subcortical (Garoutte and Aird 1958; Andersen and Andersson 1968), or cortical mechanisms (Petsche and Rappelsberger 1970). Contrary to the two small occipital preference areas for field maxima, the anterior area is relatively loosely defined, shows noticeable variation between subjects, and the location of the maximum may drift within the area over time. Occasionally, bilateral preference locations are observed in the anterior area. Contrariwise, the two occipital areas are sometimes close enough to each other to prevent the detection of a trough of frequency Electroenceph. clin. Neurophysiol.. 1971, 3l: 439 449
MULTICHANNEL TOPOGRAPHY OF ALPHA EEG FIELDS
of occurrence of field maxima between them, so that in the most simple case of alpha EEG, the scalp fields center around an anterior and a posterior maximum area, opposite and alternating in polarity, with the field relief waxing and waning approximately 20 times/sec. On the other hand, bilaterally symmetrical field distributions typically are observed during early phases of visually evoked E E G potentials (Lehmann et al. 1969; Lehmann, inpress). Field values at the ears often were discontinuous with values on the adjacent scalp area but close to values along the base of the calvarium and over frontal areas (Fig. i0, A). One may speculate that these locations tend to equipotential values because of a shunting effect of the neck, and further, that the ears cause a distortion in the local field, resulting in a tendency to localize maximal values at the ears. This would account for the minor change of the average distribution of field maxima after exclusion of the ear values (Fig. 9, A and B), since the secondary maxima were distributed over many electrode sites, Well-organized alpha over frontal or vertex regions is not frequent in bipolar and unipolar recordings. Several factors may account for this: the anterior preference area is less well defined than the occipital areas. Therefore, restricted spatial sampling may miss the maximum, or may only intermittently record it, since the maximum tends to drift somewhat within the frontal area. Further, in unipolar recordings (using one or both ears as reference), there is a certain possibility that the recording electrode is near equipotential with the reference, as discussed above. On the other hand, bipolar recordings may show poorer alpha in frontal areas because of flat anterior field distributions; with greater inter-electrode distances, there is a temptation to attribute alpha to the well-known occipital alpha activity, The field maximum showed apparent migration from one preference area to the next. The maximum was recorded at one electrode position for relatively long times in comparison with the time spent in transit from one to the next preference position across several electrodes. Apparent migration of the maximum may occur during approximately one-third of the cycle time,
447
whereas during the other two-thirds, the maximum is found at one of three electrode positions. Thus, unless one assumes discontinuous movement of the generators, it is reasonable to understand the apparent migration of the field maxima as the interaction of the fields of two stationary generators (Rgmond 1968). Stable generators are compatible with the observation of moving fields or waves (Petsche and Marko 1955; Freeman and Patel 1968); for example, three generators oscillating at similar frequencies but with different phase relations can generate a rotating field. The assumption of three generator complexes does not agree well with results of intracranial recordings (DeLucchi et al. 1962; Cooper et al. 1965) which suggest the existence of many EEG generators, an observation which essentially may be extended to the theoretical proposition that there are as many E E G generators as there are active neurons. However, the scalp EEG can be understood as an averaged and smoothed reflection of cortical activity, showing the average tendencies of the underlying neuron population (DeLucchi et al. 1962; Walter et al. 1966). Thus, modelling of the scalp EEG by a minimum number of components will hopefully permit insight into general characteristics of human brain functions. SUMMARY Alpha EEG during relaxation was recorded from the scalp of five subjects, using a 48-channel system. The data were transformed into series of equipotential field maps. The field distributions were simple and showed one to two positive and negative maximal values in each map: These maximal values were located with significant preference in three scalp areas: pre-vertex to parietal, left occipital and right occipital. Preferential areas were similar in the five subjects. The maximal values stepped clockwise or counter-clockwise from preference area to preference area. Field values measured at the ears often were discontinuous with neighbor values on the scalp but tended to be similar at both ears. The amount of relief of the fields waxed and waned 20 times/sec. With successive peak values of the relief, the maximal values of the fields alternated Eh'ctroenceph. clin. Neurophysiol., 1971, 31:439 449
448
D. LEHMANN
between anterior and posterior locations. It appears that the assumption of three stationary, semi-independent generators can acc o u n t for the main features of alpha fields. RESUME TOPOGRAPHIE MULTICANAUX DES CHAMPS DE POTENTIEL ALPHA CHEZ L'HOMME
L'activit6 alpha au repos a 6tb recueillie /t partir du scalp de cinq sujets, grfice ~ un syst6me d'enregistrement fi 48 canaux. Les donn6es ont 6t6 transform6es en s6ries de cartes isopotentielles. Les distributions de champs se sont r6v616es simples et montrent une ou deux valeurs maximales positive ou n6gative dans chaque carte. Ces valeurs maximales sont situ6es de faqon pr6f~rentielle dans trois r6gions du scalp: pr~vertex fi pari6tale, occipitale gauche et occipitale droite. Ces r6gions pr6f6rentielles sont les m~mes
pour les cinq sujets. Les valeurs maximales passent d'une r6gion pr6f6rentielle ~t l'autre dans un sens ou dans l'autre. Les valeurs de champs mesur6es au niveau des oreilles sont souvent discontinues par rapport/~ celles qui sont recueillies sur le scalp voisin mais pr6sentent une tendance/t 6tre semblables des deux c6t6s. Le relief des distributions de champs va et vient 20 fois/
Les valeurs maximales successives du relief alternent d'avant en arri6re, II semble que les principaux aspects des sec.
champs de potentiel de l'activit6 alpha puissent s'expliquer dans le cadre d'une hypoth~se off l'on se
contenterait de trois g6n6rateurs semi-ind6-
pendants et stationnaires. The author thanks Mr. Julius M. Madey, B.S.E.E. for the development of the multichannel system and for his technical assistance, REFERENCES ADRIAN, E. D. and YAMAGIWA,K. The origin of the Berger rhythm. Brain, 1935, 58: 323-351. ANANIEV, V, M. The electroencephaloscope. Fiziol. Zh. (Leningr.), 1956, 42: 981-988. ANDERSEN, P. and ANDERSSON, S, A. Physiological basis of the alpha rhythm. Appleton-Century-Crofts, N . Y . , 1968, 235 p. BEKKERING, D. H., KUIPER, J. and STORMVAN LEEUWEN, W. Origin and spread of alpha rhythms. Aeta physiol, pharmacol, neerl., 1957,6: 632-640.
BICKFORD, R. G. Discussion remarks. In E. DONCHIN and D.B. LINDSLEY(Eds.),Averageevokedpotentials. NASA, U.S. Government Printing Office, Washington, D.C., 1969, SP-191:279-281. BOURNE, J. R., CHILDERS, D. G. and PERRY, N. W. A spatiotemporal representation of the visual evoked response. Proc. 8th Int. Con9 r. Biomed. Engno., Chicago, 1969, 14-9. BRAZIER, M. A. B. A study of the electrical fields on the surface of the head. Electroenceph. clin. Neurophysiol., 1949, Suppl. 2: 38-52. (~OOPER, R. and MUNDY-CASTLE, A. C. Spatial and temporal characteristics of the alpha rhythm: A toposcopic analysis. Electroenceph. clin. Neurophysiol., 1960, 12:
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Comparison of subcortical, cortical and scalp activity using chronically indwelling electrodes in man. Electro-enceph, olin, Neurophysiol., 1965, 18: 217-228. DELUCCHI,M. R., GAROUTTE,B. and AIRD, R. B. The scalp as an electroencephalographic averager. Electroenceph. clin. Neurophysiol., 1962, 14: 191-q96. DEMOTT, D. W. Cortical micro-toposcopy. Med. Res. Engn.q. 1966, 5." _3-_9. ~ "~ DRISCOLL,D. A. and RUSH, S. A theoretical model of the head relating the scalp EEG to sources within the brain. Proc. 8th Int. Congr. Biomed. En.qng., Chicago, 1969, 9-11, ESTRIN, T. and UZGALIS, R. Computer display of spatiotemporal EEG patterns. IEEE Trans. bio-med. Engng.,
1969, 16: 192-196. FREEMAN,W. J. and PATEL,H. H. Extraneuronal potential fields evoked in septal region of cat by stimulation of fornix. Eleetroenceph. clin. Neurophysiol., 1968, 24:
~.~. ~.57. GAROUTTE,B. and Amp, R. B. Studies on the cortical pacemaker : Synchrony and asynchrony of bilaterally recorded alpha and beta activity. Electroeneeph. olin. Neurophysiol., 1958, I0: 259-268. JOSEPh,J. P., REMOND, A., RIEGER, H. and LESEVRE.N. The alpha average. II. Quantitative study and the proposition of a model. Electroenceph. clin. Neurophysiol., 1969, 26: 350-360. LARSEN, L. E. An analysis of the intercorrelations among spectral amplitudes in the EEG: A generator study. IEEE Trans. bio-med. Engng., 1969, 16." 23 26. LEHM NN, D. Multichannel studies of the electrical fields of visually evoked EEG potentials in humans. Proc. 21st Int. Congr. Ophthalmol., Mexico City 1970, Excerpta Med. (Amst.), Int. Congr. Ser., (in press). LEHMANN,D., KAVANAGH, R. N. and FENDER,D. H. Field studies of averaged visually evoked EEG potentials in a patient with split chiasm. Electroenceph. clin. Neurophysiol., 1969, 26. 193-199. LEHMANN, D., KOUKKOU, M. and KAVANAGH, R. N. Multichannel topography of spontaneous and evoked EEG potentials in humans. Proc. Reg. Congr. Int. Union Physiol. Sci., Brasov, Romania, 1970, p, 114. LILLY, J. C. Instantaneous relations beteen activities of closely spaced zones on cerebral cortex; electrical figures during responses and spontaneous activity, Amer. J.
Electroenceph. clin. Neurophysiol., 1971, 31:439-~49
MULTICHANNEL TOPOGRAPHY OF ALPHA EEG FIELDS
449
Physiol., 1954, 176: 493-504. REMO'qD, A., LESEVRE, N., JOSEPH, J. P., RIEGER, H. and LISKE, E., HUGHES, H. M. and STOWE, D. E. Cross-correLAmV, G. C. The alpha average. I. Methodology and lation of human alpha activity: normative data. Electrodescription. Electroenceph. clin. Neurophysiol., 1969, enceph, clin. Neurophysiol., 1967, 22: 429-436. 26: 245-265. PETSCHE, H. Quantitative analysis of EEG data. In J. SCHADE ~HAW,J. C. A method for continuously recording characand J. SMITH (Eds.), Progress in brain research, Vol. 33, teristics of EEG topography. Electroenceph. clin. NeuroBrain mechanisms, 1970: 63-86. physiol., 1970, 29:592 601. PETSCHE, H. und MARKO,A. Toposcopische Untersuchungen WALSH,E. G. Autonomy of alpha rhythm generators studied zur Ausbreitung des Alpharhythmus. Wien. Z. Nervenby multiple channel cross-correlation. Electroenceph. heilk., 1955, 12: 87-100. clin. Neurophysiol., 1958, 10:121 130. PETSCHE, H. and RAPPELSBERGER, P. Influence of cortical WALTER,D.O., RHODES, J. M., BROWN, D. and ADEY, W. R. incisions on synchronization pattern and travelling Comprehensive spectral analysis of human EEG genewaves. Electroeneeph. clin. Neurophysiol., 1970, 28: rators in posterior cerebral regions. Electroenceph. clin. 592-600. Neurophysiol., 1966, 20: 224-237. REMOND, A. The importance of topographic data in EEG WALTER,W. G, Intrinsic rhythms of the brain. In J. FIELD phenomena, and an electrical model to reproduce them. (Ed.), Handbook of physiology , Sect. 1. Amer. Physiol. Electroenceph. olin. Neurophysiol., 1968, Suppl. 27: Soc., Washington, D.C., 1959, I: 279-298. 29-49.
Reference: LEHMANN, D. Multichannel topography of human alpha EEG fields. Electroenceph. clin. Neurophysiol., 1971, 31 : 439-449.
Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands
MULTICHANNEL
TOPOGRAPHY
OF HUMAN
ALPHA
EEG FIELDS 1
D . LEHMANN 2
Smith-Kettlewell Institute and Department of Visual Sciences, University of the Paci/i'c, San Francisco, Calif 941 I5 (U.S.A.) {Accepted for publication: April 20, 1971)
The phenomenology of the EEG in the space domain, i.e., the description of the changes of electrical field distributions on the scalp as a function of time is still incomplete, although a considerable amount of indirect information has been accumulated. Particularly, the topography of alpha EEG has been studied since the first description of the human EEG, in the hope of gaining insight into the mechanisms which generate the EEG (Adrian and Yamagiwa 1935; Brazier 1949). Several multichannel systems for amplification and display of the EEG have been constructed (Lilly 1954; Ananiev 1956; Walter 1959; DeMott 1966). However, direct mapping of the EEG potential fields has been hindered by the problem of simultaneous recording of EEG in many channels. Recent field studies used 14-32 channels, combined with interpolation during processing (Bickford 1969; Bourne et al. 1969; Estrin and Uzgalis 1969; Petsche 1970). Phase relationships of alpha waves from different scalp areas were investigated with various techniques (Petsche and Marko 1955; Bekkering et al. 1957; Garoutte and Aird 1958 ; Walter 1959; Cooper and Mundy-Castle 1960; Liske et al. 1967; R6mond et al. 1969; Shaw 1970). Typically, much larger phase lags were seen in fronto-occipital than in transverse comparisons (Garoutte and Aird 1958; Walter 1959). One aspect of the phase relations of local alpha, the apparent migration of EEG waves, was emphasized particularly (Petsche and Marko 1955). This research was supported in part by National Institutes of Health, U.S. Public Health Service Grant NB 06038 and FR 00241. 2 Present address: Labor fiir Neurophysiologie, Neurologische Universit~tsklinik, Kantonsspital, 8006 Ziirich,
Switzerland.
Other studies dealt with the number and location of generators which could model the EEG. The typical finding of two phase reversals in occipital chains of electrodes indicated the existence of a generator in each hemisphere (Walsh 1958). A four-generator model which could account for averaged alpha in parietal areas was developed from EEG data sampled from electrodes in chain or cross arrangements (Joseph et al. 1969; R6mond et al. 1969). Application of Fourier transformation to the EEG yielded constraints about the minimum number and the location of postulated EEG generators (Walter et al. 1966; Larsen 1969). The present paper gives a phenomenology of typical EEG alpha field distributions on the human scalp, using a 48-channel recording system for off-line mapping of the scalp EEG fields. Some preliminary results were reported earlier (Lehmann et al. 1970). METHOD Five adults, 22-33 years of age, served as subjects. The subjects were taken at random from a subject pool. In conventional recordings, wellorganized alpha occurred frequently in three subjects, and less frequently in two subjects. The data presented here were obtained after a series of experiments which explored characteristics of the recording system, electrode placements and data handling strategies. The subject sat in a comfortable chair in a shielded darkroom, with his head in a chin and forehead rest. An intercom system provided communication with the experimenter. The scalp EEG was recorded from 38 to 45 Grass gold cup electrodes attached to the scalp with Grass electrode paste at approximately equal inter-electrode distances. The number of Eh,ctroenceph, clin. Neurophysiol., 1971, 3•:439 449
440
D. LEHMANN
electrodes is determined by several factors: the number of recording channels, the desired placement geometry (symmetrical around midline electrodes), the space on the scalp available for conventional electrodes and the time required for the attachment of the electrodes. The area covered by the electrode array differed slightly from experiment to experiment and is generally described by a line from the inion to the ears to approximately Fz. The inter-electrode distances were between 3.5 and 4.2 cm, depending on the subject's head dimensions and the number of electrodes, [ c~ocK60°°c / , ~ - ~ [ ,o s,~s
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The data collection was performed with an average reference (see Fig. 1). A 48-channel system was used for recording. The system was designed and built in our laboratory by Mr. Julius M. Madey. Fig. I illustrates the principal components of the system. The pre-amplifiers have a gain of 5000, a bandpass of 0.5-100 c/see (half amplitude) with 12 dB down per octave, 1.8 /~V noise peak-to-peak (0.23 /~V root mean square), an input impedance of 100 MfL and a common mode rejection ratio of 1:50,000. The output of each pre-amplifier was sampled at a rate of 750/see; the sampled output was multiplexed in 6 groups of 8 channels, post-amplified and recorded on 6 tracks of an instrumentation tape recorder as amplitude-modulated signal.
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Electroenceph. clin. Neurophysiol., 1971, 31 : 439M49
441
MULTICHANNEL TOPOGRAPHY OF ALPHA EEG FIELDS
ofskull-brain relations. The distortion inherently necessary for the projection of a three-dimensional surface into two dimensions is of no consequence in the present study. In a given map, the arithmetic mean of the instantaneous potential values recorded from all channels (which is in fact the value of the average reference) was used as zero level. The sampling interval between maps was 1-8 msec. If necessary for survey of the map series, equipotential lines were sketched in by hand as shown in Fig. 2. The computer output also identified theelectrodes which had recorded the positive and negative maximal values in each map. Further, the average, absolute amplitude per electrode was computed for each map. The average, absolute amplitude per electrode is the sum of the absolute potential differencesbetween the local potential recorded by each electrode and the mean of the potentials recorded by all electrodes in a given map, divided by the number of electrodes used. Given equidistant electrodes, the value "average, absolute amplitude per electrode" is an indicator of the degree of relief or "hillyness" of the field distribution. From each subject, at least 30 min of spontaneous EEG were recorded during relaxation with closed eyes; after editing for accessability and artifacts, approximately 10-15 min of alpha EEG were available for processing. From this material, well-organized alpha EEG epochs of 500-1000 msec duration were selected for further analysis. For each subject, 2-7 see of alpha were analyzed. RESULTS
Examination of a series of equipotential maps obtained during alpha activity shows that some fielddistributions occur repeatedly with the same or opposite polarity. For instance, during the alpha cycle mapped in Fig. 3 we find similar field distributions with inverted polarities at 425 and 465 msec, and at 449 and 505 msec. The interval between similar distributions of inverted polarity is approximately 50 msec, i.e., one-half of one alpha cycle. Generally, the field distributions are simple, centering around one or two positive and negative maximal values in each m~p (Fig. 3). This suggests the location of the
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The upper number indicates the a m o u n t of relief in each m a p (average, absolute amplitude per electrode in microvolts); the lower number is the time in milliseconds, referring to Fig. 5, of which Fig. 3 illustrates a portion.
positiveand negative maximum in each map as descriptor of the dominant characteristics of the distribution. Plotting of the location of maximal field values shows that they tend to occur within relatively small scalp areas, which we call preferentialareas. A case of three preferential areas is illustrated in Fig. 4, where the entries indicate the frequency of occurrences of positive and negative maxima at the different electrode positions during a 640 msec epoch of alpha activity (including the sequence of Fig. 3) sampledin intervals of 8 msec. The maxima Electroenceph. clin. Neurophysiol., 1971, 31:439~t49
442
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Fig. 4. Location of maximal values of the fields during 640 msec of alpha (including the epoch shown in Fig. 3). Sampling in 8 msec intervals. Each dot or number represents one electrode. The numbers give the percentage of time that the maximal value occurred at the indicated electrode location. The most anterior (first) midline electrode was approximately 7 ~ of the distance nasion-inion behind Fz, the second at Cz, and the sixth at the inion. Values in A are not always the mean of corresponding values in B and C, and the totals are not equal to 1 0 0 ~ , because of rounding to multiples of 1'~. Electrodes with 6 or more percent time of occurrence are shaded. Dotted lines in A delineate the three preferential areas {see text) used in Fig. 5.
occurred preferentially
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7 of t h e 3 8 electrodes during appr6~ximately 6 3 ~ of the time, and at the remaining 31 electrodes during approximately 40 ~ of the time (rounding to multiples of 1 ~ brings the total to 103~). The results are largely similar when positive and negative maxima are treated independently (Fig. 4, B and C). The three clusters of preferred electrode locations for the maxima are located over anterior, left occipital and right occipital areas. For further data reduction, the three preferential areas were 'defined as the electrode sites with 6 ~ and more time incidence of occurrence of positive and negative maxima, plus all neighbor electrodes unless contested by an adjacent preferential area. Demarkation lines of these preferential areas are dotted in Fig. 4, A. The anterior area is larger than the occipital areas. This is a typical finding, and more detailed examination of the data shows
Fig. 5. A : Location of positive (POS.) and negative (NEG.) maximal field values as a function of time, in the three preferential scalp areas of Fig. 4: anterior (ANT.), occipital left (OC.L.), and occipital right (OC.R.), B: Concomitant changes of the amount of relief of the whole field (average, absolute amplitude per electrode). C: Changes of local field values as a function of time at the three electrode locations in Fig. 4, A with highest percent time of occurrence of the field maxima: l=anterior, 11 ~ ; 2=occipital left, 11 ~,/,; 3 =occipital right, 13 ~o. Sampling in 8 msec intervals. Fig. 5 is based on the same data as Fig. 3 and 4.
that the maximal value drifts over time within the anterior area, i.e., the maximum occurs at neighbor or next neighbor electrodes during successive alpha cycles. The time of occurrence of the maxima in the three preferential areas of the sample epoch is illustrated in Fig. 5, A. There is a repetitive, rotational sequence ofthe location ofthe positive and negative maxima, in the following order: anterior, left occipital and right occipital area. In each preferential area, positive and negative maxima alternate, each at approximately 10 c/sec. The magnitude of the phase lags between waves recorded from the three preferential areas is illustrated in Fig. 5, C, which demonstrates the large phase difference anterior-posterior, and Electroenceph. clin. Neurophysiol., 1971, 31 : 439 449
MULTICHANNEL TOPOGRAPHY OF ALPHA EEG FIELDS the m u c h smaller lags between hemispheres, Fig. 5, C also shows the typical variance in phase lags from cycle to cycle. It should be noted that in Fig. 5, A, only information on the direction of phase lags of the field fluctuations in the three areas is represented ; there is no information on the m a g n i t u d e of the phase lags, since only one positive and one negative field m a x i m u m was determined for each time slot. The a m o u n t of relief of the field (the average, absolute amplitude per electrode) is shown as a function of time in Fig. 5, B. A periodic fluctuation of the field relief is evident at a rate of a p p r o x i m a t e l y 20/see, twice the alpha frequency, During successive peak times of the relief curve, the field m a x i m a are found alternately in the anterior area or in the occipital areas (see also Fig. 3). N o t e w o r t h y is one missing "beat" of the fluctuations of the relief at a p p r o x i m a t e l y 370 msec in Fig. 5, A, an event that was observed in
443 three records; the cyclic sequence of locations of field m a x i m a was not interrupted, merely the relief of the distribution remained low. Let us now consider another alpha sequence recorded from a second subject. Sample m a p s are shown in Fig. 6. The general features of the fields are similar to those in Fig. 3, but four preferential areas for location of field m a x i m a can be distinguished (Fig. 7). Electrodes frontal to the anterior preference location were included in the anterior preference area in Fig. 7, A. The sequence of the occurrence of the field m a x i m a (Fig. 8, A) now is anterior, right occipital, left occipital and left ear, contrary to the previous example. However, toward the end of the alpha spindle, at a p p r o x i m a t e l y 700 msec, there is a reversed sequence, a c c o m p a n i e d by declining organization of the relief cycles (Fig. 8, B) which change to slower frequencies and disappear. Fig. 8, C demonstrates that the alpha spindle starts and ends at s o m e w h a t varying times in t
ed.n
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Common characteristics in all subjects The location of the scalp preference areas for
B. pos. MAXIMA
Fig. 6. Sequence of equipotential maps of alpha EEG. Time of each map is indicated in milliseconds, referring to Fig. 7 and 8, of which Fig. 6 illustrates a portion. For other explanations, see Fig. 3.
C. NEG, MAXIMA
Fig. 7. Location of maximal values of the fields during 1024 msec of alpha (including sample shown in Fig. 6). The most anterior (first) midline electrode was approximately 5 },; o4 the nasion-inion distance in front of Fz, the third electrode at Cz, and the seventh electrode at the inion. Dotted lines delineate preferential areas used in Fig. 8. For other explanations, see Fig. 4. Electroenceph. c/in. Neurophysiol., 1971, 31 : 439 449
444
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Fig. 8. A : Location of positive and negative maximal field values as a function of time in the four preferential scalp areas of Fig. 7: anterior (ANT.), occipital right (OC.R.), occipital left (OC.L.), and left ear (L.E.). B: Changes of the amount of relief of the whole field (average, absolute amplitude per electrode). C: Changes of local field values as a function of time, at the four electrode locations in Fig. 7, A with highest percentage of time of occurrence of field maxima : 1 = anterior, 9 ~ ; 2 =occipital right, 16 %; 3 =occipital left, 14 %; 4 = left ear, 8 %. Sampling in 1 msec intervals. Fig. 8 is based on the same data as Fig. 6 and 7.
Electroenceph. clin. Neurophysiol., 1971, 3l: 439 449
MULTICHANNEL TOPOGRAPHY OF ALPHA EEG FIELDS
A
445
B
Fig. 9. Average distribution of maximal values of alpha E E G fields on the scalp. Mean of five subjects. Values in percentage of time per electrode. For visualization, contour lines were interpolated linearly between the values at the electrode positions. Percentage levels are differentiated by shading, as illustrated below Fig. 9, B. A : Electrode array includes ears. B : Electrode array with scalp electrodes only; ear values were substituted by secondary maxima on the scalp. The insets indicate the electrode positions. The circled electrode is at the vertex, the most posterior midline electrode is at the inion. Dots indicate electrodes with less than 3 ~ occurrence, open circles with more than 3 ~ occurrence.
field maxima during EEG alpha exhibited a considerable similarity in the five subjects. Fig. 9, A demonstrates topographically the frequency of occurrence (in percentage of time) of the scalp field maxima during alpha activity, averaged over the five subjects. The average frequency of occurrence was computed for each electrode, using the frequency-of-occurrence data of the first alpha epoch which had been selected for analysis in each subject. Electrode positions that had not been used in all subjects were excluded from the average. In maps where the maximum occurred at one of the excluded electrodes, the next lower value in the remaining electrode array was used, thus covering 100~ time for each analysis epoch. Fig. 9 shows that the field maxima occur preferentially in a well-defined area. Seen from the occiput, this area has the shape of an inverted Y over the sagittal midline. Peak frequencies of occurrence are found near the vertex, at the left occiput, and particularly at the right
occiput. In addition, both ears frequently record maxima. The inspection of original maps suggests that an ear electrode often is nearly equipotential with distant electrodes. To clarify this impression, the data of three subjects who had a row of electrodes just frontal to Fz were examined. Data collected from the left ear electrode were excluded from the determination of maximum values: in each map which originally showed a maximum at the left ear, the location of the next highest field value (secondary maximum) was plotted as maximum in Fig. 10, A. The secondary maxima tended to a distribution along the circumference of the electrode array, especially preferring the contralateral ear. This contrasts with the distribution of the secondary maxima after the exclusion of a left occipital electrode (Fig. 10, B), where these substitute values are reasonably centered around the original location; there is some spread to the right occiput as Electroenceph. olin. Neurophysiol., 1971, 31:439 449
446
D. LEHMANN
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dominated in each subject. However, the limited material does not allow us to decide whether individuals preferentially show one direction of progression of field maxima. The field reliefs of all subjects exhibited 20/sec fluctuations consistently during alpha EEG.
2
DISCUSSION
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Fig. 10. Distribution of second highest field values, average of three subjects. Numbers indicate percentage of time of occurrence of secondary maxima. A: Original maxima were at left ear (x), Note the high incidence at the contralateral ear. B: Original maxima were at left occipital electrode ( x ).
Circle indicates vertex electrode. For further discussion see text. expected with the usual small phase lag between the oscillations in the two occipital areas. The average distribution of the field maxima of the whole population (Fig. 9, A) changed only slightly when the values at both ears were excluded and substituted by secondary maxima (Fig. 9, B). Next, we examine the difference between the occurrence of maximal values in preferential and non-preferential areas. Electrode positions showing 3% and more time of occurrence in Fig. 9 were considered preferential. There were 15 (14) preferential and 21 (20) non-preferential electrode positions in the averaged map. (Values after the exclusion of the earlobe data are in parentheses.) The mean frequency of occurrence per electrode over subjects was 5.38 (5.52) % for preferential electrodes vs. 0.92 (1.14)% for nonpreferential electrodes. The difference was significant at P < 0.005 (< 0.005) in paired t tests, Further, preferential and non-preferential electrodes were compared in each subject. The designation of electrodes as preferential or nonpreferential in the population average of Fig. 9 was used also for the individual subjects. The difference between the frequencyofoccurrence of maxima at preferential and non-preferential electrodes was significant for all subjects (P < 0.005 in rank tests), indicating a high consistency of the location of preferential areas between subjects, Progression of the field maxima in clockwise and counter-clockwise direction was seen in all subjects, although usually one direction pre-
Direct plotting of the relatively simple scalp fields was possible because of the number (48) o f available recording channels; a n array of m o r e than 4 by 4 electrodes is necessary t o
detect more than one positive and negative peak in a field. No interpolation was used for the estimation of the location of maximal field values. These maxima were found preferentially in a pre-vertex to parietal midline area, a left occipital, and a right occipital area. In simple Conditions, the maximum of a surface field will be located perpendicularly over its generator. However, the conspicuous extensions of the anterior preference area along and to both sides of the midline raises questions about the anatomical and physiological relevance of the localization. In fact, distortion of the projection of cortical areas onto the scalp is known (Driscoll and Rush 1969), and the central fissure may function as a mediator for distortion. It appears that the assumption of three stationary generator areas, each oscillating at approximately l0 c/sec, can account for the major phenomenological properties of the ohserved alpha fields. The field oscillations are not in phase in different scalp areas (e.g., Walter 1959; Liske et al. 1967), and vary around a center frequency (Garoutte and Aird 1958). Thus, the generators may well be semi-independent under the control or coordination of subcortical (Garoutte and Aird 1958; Andersen and Andersson 1968), or cortical mechanisms (Petsche and Rappelsberger 1970). Contrary to the two small occipital preference areas for field maxima, the anterior area is relatively loosely defined, shows noticeable variation between subjects, and the location of the maximum may drift within the area over time. Occasionally, bilateral preference locations are observed in the anterior area. Contrariwise, the two occipital areas are sometimes close enough to each other to prevent the detection of a trough of frequency Electroenceph. clin. Neurophysiol.. 1971, 3l: 439 449
MULTICHANNEL TOPOGRAPHY OF ALPHA EEG FIELDS
of occurrence of field maxima between them, so that in the most simple case of alpha EEG, the scalp fields center around an anterior and a posterior maximum area, opposite and alternating in polarity, with the field relief waxing and waning approximately 20 times/sec. On the other hand, bilaterally symmetrical field distributions typically are observed during early phases of visually evoked E E G potentials (Lehmann et al. 1969; Lehmann, inpress). Field values at the ears often were discontinuous with values on the adjacent scalp area but close to values along the base of the calvarium and over frontal areas (Fig. i0, A). One may speculate that these locations tend to equipotential values because of a shunting effect of the neck, and further, that the ears cause a distortion in the local field, resulting in a tendency to localize maximal values at the ears. This would account for the minor change of the average distribution of field maxima after exclusion of the ear values (Fig. 9, A and B), since the secondary maxima were distributed over many electrode sites, Well-organized alpha over frontal or vertex regions is not frequent in bipolar and unipolar recordings. Several factors may account for this: the anterior preference area is less well defined than the occipital areas. Therefore, restricted spatial sampling may miss the maximum, or may only intermittently record it, since the maximum tends to drift somewhat within the frontal area. Further, in unipolar recordings (using one or both ears as reference), there is a certain possibility that the recording electrode is near equipotential with the reference, as discussed above. On the other hand, bipolar recordings may show poorer alpha in frontal areas because of flat anterior field distributions; with greater inter-electrode distances, there is a temptation to attribute alpha to the well-known occipital alpha activity, The field maximum showed apparent migration from one preference area to the next. The maximum was recorded at one electrode position for relatively long times in comparison with the time spent in transit from one to the next preference position across several electrodes. Apparent migration of the maximum may occur during approximately one-third of the cycle time,
447
whereas during the other two-thirds, the maximum is found at one of three electrode positions. Thus, unless one assumes discontinuous movement of the generators, it is reasonable to understand the apparent migration of the field maxima as the interaction of the fields of two stationary generators (Rgmond 1968). Stable generators are compatible with the observation of moving fields or waves (Petsche and Marko 1955; Freeman and Patel 1968); for example, three generators oscillating at similar frequencies but with different phase relations can generate a rotating field. The assumption of three generator complexes does not agree well with results of intracranial recordings (DeLucchi et al. 1962; Cooper et al. 1965) which suggest the existence of many EEG generators, an observation which essentially may be extended to the theoretical proposition that there are as many E E G generators as there are active neurons. However, the scalp EEG can be understood as an averaged and smoothed reflection of cortical activity, showing the average tendencies of the underlying neuron population (DeLucchi et al. 1962; Walter et al. 1966). Thus, modelling of the scalp EEG by a minimum number of components will hopefully permit insight into general characteristics of human brain functions. SUMMARY Alpha EEG during relaxation was recorded from the scalp of five subjects, using a 48-channel system. The data were transformed into series of equipotential field maps. The field distributions were simple and showed one to two positive and negative maximal values in each map: These maximal values were located with significant preference in three scalp areas: pre-vertex to parietal, left occipital and right occipital. Preferential areas were similar in the five subjects. The maximal values stepped clockwise or counter-clockwise from preference area to preference area. Field values measured at the ears often were discontinuous with neighbor values on the scalp but tended to be similar at both ears. The amount of relief of the fields waxed and waned 20 times/sec. With successive peak values of the relief, the maximal values of the fields alternated Eh'ctroenceph. clin. Neurophysiol., 1971, 31:439 449
448
D. LEHMANN
between anterior and posterior locations. It appears that the assumption of three stationary, semi-independent generators can acc o u n t for the main features of alpha fields. RESUME TOPOGRAPHIE MULTICANAUX DES CHAMPS DE POTENTIEL ALPHA CHEZ L'HOMME
L'activit6 alpha au repos a 6tb recueillie /t partir du scalp de cinq sujets, grfice ~ un syst6me d'enregistrement fi 48 canaux. Les donn6es ont 6t6 transform6es en s6ries de cartes isopotentielles. Les distributions de champs se sont r6v616es simples et montrent une ou deux valeurs maximales positive ou n6gative dans chaque carte. Ces valeurs maximales sont situ6es de faqon pr6f~rentielle dans trois r6gions du scalp: pr~vertex fi pari6tale, occipitale gauche et occipitale droite. Ces r6gions pr6f6rentielles sont les m~mes
pour les cinq sujets. Les valeurs maximales passent d'une r6gion pr6f6rentielle ~t l'autre dans un sens ou dans l'autre. Les valeurs de champs mesur6es au niveau des oreilles sont souvent discontinues par rapport/~ celles qui sont recueillies sur le scalp voisin mais pr6sentent une tendance/t 6tre semblables des deux c6t6s. Le relief des distributions de champs va et vient 20 fois/
Les valeurs maximales successives du relief alternent d'avant en arri6re, II semble que les principaux aspects des sec.
champs de potentiel de l'activit6 alpha puissent s'expliquer dans le cadre d'une hypoth~se off l'on se
contenterait de trois g6n6rateurs semi-ind6-
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Reference: LEHMANN, D. Multichannel topography of human alpha EEG fields. Electroenceph. clin. Neurophysiol., 1971, 31 : 439-449.