Cross-correlation of human alpha activity: Normative data

429

Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands

C R O S S - C O R R E L A T I O N OF H U M A N A L P H A ACTIVITY: N O R M A T I V E DATA E. LISKE, M.D., HARRY M. HUGHES, PH.D. AND DARWELLE. STOWE,B.S. Neurology and Biometrics Branches, U.S.A.F. School of Aerospace Medicine, Aerospace Medical Division (A.F.S.C.), Brooks Air Force Base, Texas (U.S.A.) (Accepted for publication: November 21, 1966)

INTRODUCTION

The timing of bilateral alpha waves with respect to each other has long interested electroencephalographers. Adrian and Yamagiwa (1935) in the report of a study on human alpha rhythm stated " . . . b u t evidently the two sides are so closely linked that the phase relation cannot vary". Cohn (1948) employed a more sensitive apparatus and demonstrated phase changes in parieto-occipital alpha rhythm between the two sides. Cooper and Mundy-Castle (1960) studied the spatial and temporal characteristics of the alpha rhythm and found that "... absolute synchrony ... between the hemispheres was rare". The illuminating essays of Walter (1959, 1962) point out the complexity of the functional, geometric, frequency and phase aspects of human alpha rhythm. The averaged phase relation of left and right brain wave activity has been studied in humans by means of cross-correlation (Brazier and Casby 1952; Barlow 1959; Barlow et al. 1964). Personal communication with Barlow (1966) confirmed what is implied in these reports; i.e., the alpha activity sampled from the parieto-occipital areas of normal human subjects, tends to be essentially synchronous when averaged over a minute or two. Walter et al. (1966) in a recent study also stated "reference to the phase angle calculations (not reproduced) showed that P3-O1 and P4-Oz have their alpha waves essentially in phase . . . " Recently, cross-correlation analyses on base line EEG tape recordings taken from a small group of asymptomatic subjects (Liske et al. 1966)

unexpectedly revealed a tendency for the rightsided alpha generator to lead the left by a few milliseconds. The group of normal individuals has been enlarged to further measure and substantiate this phase shift. The aims of this paper are: (1) to report the averaged phase relation of the right and left alpha activity found in each of 42 asymptomatic subjects; (2) to establish the norm for the group; and (3) to measure the range of deviation about the norm. It is hoped that such normative data may aid in the interpretation of correlation studies on various clinical disorders now appearing in the literature (Karashima 1960; Yamamoto 1960; Yuzuriha 1960; Grindel' et al. 1965). METHODS

1. Data gathering on human subjects

Two separate but nominally identical data acquisition systems (A and B) were employed. Each was made up of a Grass jack box, shielded cable, III-D Electroencephalograph, Sanborn balanced-to-single-ended coupler, and Ampex FR-1300 Tape Recorder/Reproducer operated at 17/8 in./sec in FM mode. Grass E-1 durable disc electrodes (silver) and Grass needle electrodes (stainless steel) were used exclusively The Grass E-1 discs were "cured" in the electrode jelly for 48 h and never polished afterward. The needle electrodes received special handling only in that they were sterilized after each use. Both the disc and needle electrodes were randomized within their proper groups from subject to subject as regards their scalp and jack box tiepoints. The procedure of leaving the electrode Electroenceph. clin. Neurophysiol., 1967, 22:429-436

E. LISKEet al.

430

leads inserted in the same jack box locations (for storage between subject recordings) was specifically avoided during this study. On System A, 20 neurologically normal Air Force male subjects between the ages of 18-23 years were recorded in an acoustically paneled, air-conditioned, dimly lit room, supine with eyes closed. The patients were encouraged to remain awake with their minds inactive. Disc electrodes were affixed by collodion to carefully measured sites of the 10/20 International System and a 3min recording made on both paper and magnetic

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derived from P3-O1 and P4-O2 were filtered, using a Spectrum Instruments active low-pass filter at 25 c/sec cut-off frequency and simultaneously digitized. The Consolidated Systems Co. Microsadic digitizer sampled each channel simultaneously at a rate of 500 samples/channel/sec, recording the digitized values to an accuracy of 11 bits plus sign on digital magnetic tape. Two cross-correlograms, one of the reference signal and the other of the scalp EEG were subsequently generated for each subject on a Philco-2000 digital computer by the formula:

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tape. System A utilized approximately 1 min of EEG machine calibration signal for a phase reference on all channels before and after each subject's 3-min EEG was taken. All subjects in the A group were right-handed by natural preference. On System B, 22 neurologically normal Air Force military and civilian male subjects (all different from the System A group), aged 22 to 47 years, were recorded in a similar manner except for these notable exceptions: (1) all 22 subject runs were preceded and followed by a 10 c/sec micro-source sine wave reference signal introduced into the jack box and recorded on all channels in addition to the 1-min recording of the EEG machine calibration signals; (2) ten of this B group utilized disc electrodes (group B-l) while the remaining twelve were recorded with needle electrodes (group B-2). The B-2 subjects were all right-handed whereas two of the B-1 subjects preferred their left hand for skilled acts. All 42 subjects were studied in serial fashion and no selection was allowed after the EEGs were taken. Thus, "dominant alpha" subjects and those with "poor alpha" were accepted indiscriminately. Hand preference (suggesting contralateral cerebral dominance) was ascertained by both history and actual demonstration.

2. Data handling The magnetic tape recordings of both the phase reference signal and the subjects' EEG

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The phase reference correlogram was generated from 10 sec of data while the EEG correlogram utilized 150 sec of data. The correlogram program was allowed to run for 20 lags in each case with lag interval of 2 msec. The results were plotted on a digital Cal-Comp plotter (Fig. 1). Additionally, the correlation values at each lag were printed out and subsequently used in computing more accurate estimates of the phase relationship between correlated channels. Determination of the relative phase relationship between data channels may be resolved to the nearest millisecond by reference to the printed output of correlation values for each 2 msec lag. It was possible to further refine these determinations without decreasing the lag interval by employing a parabolic fitting technique. Those correlation values chosen on either side of the maximum were used to interpolate a new maximum, which at the very worst, differs from the true shift by less than 0.2 msec. When analyzing the correlograms generated from the reference signals which were known to be in phase.~ similar parabolic fitting techniques were employed to improve the resolving power. The final computed phase shift for each subject, reported and discussed below, was obtained by subtracting the fitted shift of the reference signal (known zero phase input) from the fitted shift of the EEG correlogram to remove the effect of all systemintroduced shifts.

Electroenceph. clin. Neurophysiol.,

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ALPHA RHYTHM CROSS-CORRELATION IN NORMALS

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Fig. 1 These cross-correlograms, accurate to the nearest millisecond, show that n o r m a l subjects can have appreciable phase shift. Subsequently these data are c o m p a r e d to a reference signal of k n o w n zero phase shift to obtain the values used in the text. Finest divisions along abscissa equal 2 msec.

3. Calibration Two methods were employed to calibrate our instrumentation from the jack box to the computer print/write-out devices; viz., (1) a microsource 10 c/sec sine wave signal was injected into all channels at the jack box with the reference cross-correlogram between pertinent channels generated. With this reference correlogram we demonstrated that: (a) phase shift measurements utilizing the raw data from our system cannot be made more accurately than +__ 0.5 msec (regardless of lag interval) without the reference correlogram; and, (b) the accuracy of 4- 0.5 msec is obtainable only if tape recording is performed in channels adjacent within the same head stack; and, (c) care is taken to match the low-pass filters. However, in every subject a zero-phase reference signal was cross-correlated from pertinent channels and used to correct the raw, phase-shift measurements of the subjects' brain waves. This corrected measurement was then treated mathematically to increase the resolving power as described under "Data handling". (2) A linear resistive load of 5000 ~ was inserted

into both Pa-O1 and P4-Oz of the jack box to simulate a non-generating source. The system noise was at a power less than 1/100 that of the EEG signal. Secondly, a comparison between reference signals was carried out; i.e., the square wave generated in the EEG machine calibration circuit and the exogenous l0 c/sec micro-source sine wave. Their relative phase shift as compared by cross-correlation was found to be immeasurably small by available technique. Thus, although the l0 c/sec sine wave signal has some theoretical advantage, for the purposes of this experiment the square wave and the sine wave were of equivalent fiduciary value. Thirdly, consideration was given to the circuit from the subjects' scalp to the jack box. In the electrode application room, the DC resistance was measured and any electrode pair showing a value greater than 5000 f~ was reapplied. The effect of the time constant of different electrodes has been demonstrated by Cooper 0963) and might at first suggest an explanation for the needle subgroup (B-2) giving actual Electroenceph. clin. Neurophysiol., 1967, 22:429~,36

432

E. LISKE et al. TABLE I Statistical summary of mean phase shifts for various subject subgroups

Group

N

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*Positive values indicate right phase lead; negative indicates phase lead by the left alpha generator.

values closest to synchrony. H o w e v e r , a statistical analysis revealed t h a t there was no significant difference in the p h a s e shifts between the two e l e c t r o d e groups. C o o p e r (1963) a n d G r e a t b a t c h (1966) give t h e o r e t i c a l a n d p r a c t i c a l reasons w h y the A g - A g C I e l e c t r o d e usually has electrical advantages in certain instances for e l e c t r o p h y s i o logical recordings. F r o m their discussions we can see no source o f e l e c t r o d e - i n d u c e d p h a s e shift in o u r d a t a g a t h e r i n g system. The p r o b l e m o f e l e c t r o d e effects on c r o s s - c o r r e l a t i o n studies in h u m a n E E G has n o t been s y s t e m a t i c a l l y s t u d i e d to o u r knowledge. Finally, the use o f two s e p a r a t e b u t n o m i n a l l y identical i n s t r u m e n t a t i o n systems for d a t a gathering a n d the use o f two s e p a r a t e g r o u p s o f h u m a n subjects for a l p h a g e n e r a t i o n with b o t h situations leading to essentially t h e same values, further tend to v a l i d a t e the results.

g r o u p s A a n d B-1. ( S t u d e n t ' s t is 1.55 with 40 d.f. giving P > 0.10.) Thus, we m a y c o m b i n e all 42 subjects. This results in a m e a n right p h a s e shift o f

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RESULTS The s p r e a d o r v a r i a t i o n o f the d a t a was extremely c o n s i s t e n t as i n d i c a t e d by the calculated s a m p l e s t a n d a r d d e v i a t i o n s in T a b l e I a n d Fig. 2. It is u n u s u a l for o b s e r v e d s t a n d a r d deviations to be so close to each o t h e r in groups o f this size. The m e a n o f the A g r o u p (l.1 msec) is significantly different f r o m zero at the 3 level (see final c o l u m n T a b l e I). T h e m e a n o f B-1 g r o u p is a l m o s t identical to t h a t o f A g r o u p ; t o g e t h e r they establish the significance o f the 1.1 msec phase shift at the 0.01 level because o f the increased n u m b e r o f subjects. G r o u p B-2 has a s a m p l e m e a n very close to zero b u t still n o t significantly different f r o m the c o m b i n a t i o n s o f

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Fig. 2 (,4) Distribution of 20 subjects employing the EEG machine calibration signal for a phase reference. (B) Twentytwo different subjects using an exogenous sine wave for phase reference. (C) A group of normal subjects using needle electrodes. (D) Re-combination of 30 subjects using disc electrodes. Negative milliseconds on the abscissa mean that the left alpha generator is leading. The arrow indicates mean phase value for the group. Electroenceph. clin. Neuroph.vsiol., 1967, 22:429-436

ALPHA RHYTHM CROSS-CORRELATION IN NORMALS

0.83 msec that is significantly non-zero at the 3 ~o level. Our results then, apply to what can be expected when choosing a subject at random and should have applicability in the clinical setting. Attention is invited to the shape of the curve of distribution (Fig. 3). While the mean shift is of the order of 1 msec, note that subjects vary from 4 msec left shift to 7 msec right shift and that there is "crowding" just to the left of zero and a "trailing out" to the right. Of the total 42 subjects, eighteen exhibited left alpha phase lead while the remaining 24 subjects showed phase

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Fig. 3 Phase distribution ofaU subjects in the study. The "trailing out" of the curve to the right is of interest and suggests that in some normals there is a " d o m i n a n c e " for phase-lead residing in the fight cerebral hemisphere. Negative values mean left alpha generator is leading. Arrow locates mean value o f + 0 . 8 3 m s e c for the group.

lead to the right. None were precisely synchronized over the averaged 150 sec. DISCUSSION

Previously published displays ofcross-correlograms with lower resolution would make it difficult to detect a small difference in phase such as reported in the present study.Comparison with the preliminary calculations of phase angle reported by Walter et al. (1966)cannot be made because all of the present results were calculated in terms of milliseconds of shift. We used time displacement rather than phase angle because the correlogram is a mixture of several frequencies and the phase angles probably cannot meaningfully be related to any particular frequency. Even using the average period of the correlogram for establishing a frequency from which phase angles can be calculated may help

433

little because phase angles can change in a nonlinear fashion (Corriol 1951; Downs and Liebman 1966). To appreciate how infrequently the.alpha generators are in true synchrony, one has only to repeat the method of Corriol (1951) or Andrew (1956) recently revived by Levine et al. (1963). By observation of the Lissajous figures, one can show that the alpha waves from either side move into synchrony only briefly, then fall out of zero phase. From previous cross-correlation studies (see Introduction) it was suggested that the average phase relation was close to true synchrony, implying that one alpha generating system tended to lead the other by a certain amount and then fall behind by an approximately equal quantity. Such symmetrical competition for phase lead between two anatomically symmetrical hemispheres suggested a deep, midline cerebral pacemaker to Aird and Garoutte (1958), Garoutte and Aird (1958) and Garoutte et al. (1961). The present study failed to demonstrate that the competition for phase lead by the two alpha generating systems in any of our 42 normal subjects was symmetrical. Averaging over 2.5 min always revealed that either one or the other hemisphere was dominant in this regard. At times the dominance was surprisingly great: in one instance the right hemisphere exerted a 7 msec average phase lead. In no subject did the left hemisphere maintain a phase lead greater than 4 msec. Although those subjects exhibiting extreme phase lead were "right hemisphere alpha dominant", enough subjects were to the left of the zero-phase point so that the group of 42 subjects as a whole exhibited 0.83 msec rightsided phase lead. This distribution may support certain textbook statements describing the tendency for some normal subjects to generate more prominent alpha rhythm over the right hemisphere (Cohn 1949, p. 9; Hill and Parr 1963, p. 238). Rarely, the left-sided alpha activity is reported dominant, such as the base line alpha of one study by Lansing and Thomas (1964). Although in theory, the cerebral hemispheres are identical in anatomy and functional capacity, the latter is not always bilaterally equivalent in humans. In these the left hemisphere often tends to exercise its capacity for the memory of language symbols and skilled movement patterns Electroenceph. clin. Neurophysiol., 1967, 22:429-436

434

E. LISKEet al.

to a greater degree. The left hemisphere showed dominant photic driving in the study by Lansing and Thomas (1964). On the other hand, Glanville and Antonitis (1955) found no relationship between occipital alpha rhythm and hand preference. Giannitrapani and Darrow (1963) studied phase relationships between homologous scalp areas in 10 left-handed and 10 right-handed subjects. Scoring phase differences on a momentary wave per wave basis, they found a reliable tendency for central areas contralateral to preferred hands and eyes to lead corresponding homolateral areas, especially during sleep. They did not report on the phase of the right- and left-sided alpha activity, however. In the present study only two subjects preferred their left hand for skilled motor patterns. One of these had 1.8 msec left phase lead and the other exhibited 3.6 msec right side phase lead. No correlation was demonstrated between the hemispheres which were alpha dominant or motor skilled dominant in the group. Some instances of right hemisphere dominance have been reported. Piercy and Smyth (1962) conclude that the right cerebral hemisphere is normally dominant for the functions impaired in constructional apraxia. In a photic driving study on humans, Freedman (1963) found "the right hemisphere always showed greater following". Fig. 3 in the report by Aird and Garoutte (1958) shows a strong right occipital phase lead in a patient with agenesis of the corpus callosum, suggesting an alpha dominance for pacing residing in the right hemisphere. Further discussion emphasizing clinical differences in the functional capacity of the right and left human cerebral hemispheres is made by Denny-Brown (1962). That the great cerebral commissure is necessary to coordinate the higher functions of the hemispheres is well known (Sperry 1964). Visually evoked potentials and reaction time at least are dependent on the phase of alpha brain waves (Dustman and Beck 1965). Thus it may be that, although the deeper midline structures of the brain exert a coarse control over bilateral alpha generation (bioelectric scale of alertness), a vernier control exists transcallosally to aid in the finer coordination of phase-dependent responses between the cerebral hemispheres. Participation of the corpus callosum in the mechanism of the bioelectric synergy of the cerebral

hemispheres has been suggested by others, such as Bremer (1956), Bremer and Stoupel (1957), and Enomoto (1959). That the corpus callosum might play some role in coupling the alpha generating mechanisms and perhaps control phasing has been more recently suggested in humans by Green and Russell (1966) and in animals by Berlucchi (1966). Many of the subjects in this normative study possessed an alpha generator on the right seemingly capable of entraining and phase-leading the alpha generator on the left long enough to shift the average phase lead to the right. To discover how clinical conditions might correlate with these normative data, a series of patients has been studied with various clinical disorders ranging from cardiac arrhythmias to spatial disorientation and will be the subject of a separate report. SUMMARY AND CONCLUSIONS

1. Forty-two asymptomatic adult males were studied by history, physical examination and EEG. Cross-correlograms were generated from the EEG data derived from Pa-O1 and P4-O2. 2. Twenty-four subjects exhibited phase lead to the right and eighteen to the left. None were exactly in zero phase. 3. Average phase shift for the group was 0.83 msec to the right. 4. The range of the phase shifts was from 4 msec left to 7 msec right. 5. This report emphasizes that not all normal subjects are essentially synchronized with respect to their alpha activity, although in most normals there is clearly some imperfect neurological mechanism operating to phase align the alpha activity. 6. In a number of normal subjects a surprising degree of right-sided alpha phase leading was seen; a degree not approached in those subjects in which left-sided alpha activity was phase leading. 7. These findings tend to support textbook statements that cerebral dominance for alpha rhythm more often resides in the right hemisphere of normal humans in the sense that it more often exerts an average phase lead over the alpha activity generated in the left hemisphere. Electroenceph. clin. Neurophysiol., 1967, 22:429-436

ALPHA RHYTHM CROSS-CORRELATIONIN NORMALS RI~SUMI~ CORRELATIONS CROISI~ESDE L'ACTIVITI~ALPHA HUMAINE 1. Q u a r a n t e - d e u x sujets adultes m~les sains ont 6t6 6tudi6s par: anamn6se, examen physique et EEG. Des corr61ations crois6es sont f a r e s p o u r les donn6es E E G obtenues h partir des d&rivations P3-O1 et P4-O2. 2. Vingt-quatre sujets m o n t r e n t une avance de phase /t droite et dix-huit /t gauche. A u c u n n ' e s t exactement en phase z6ro. 3. La v a r i a t i o n de phase m o y e n n e p o u r le groupe est de 0.83 msec en faveur de la droite. 4. Les d~phasages s'6tendent de 4 msec fi gauche/~ 7 msec ~ droite. 5. Ce r6sultat m o n t r e que t o u s l e s sujets n o r m a u x ne sont pas a b s o l u m e n t synchronis6s en ce qui concerne leur activit6 alpha, puisque chez la p l u p a r t des sujets il y a u n m~canisme nerveux de s y n c h r o n i s a t i o n de l'activit~ alpha imparfait. 6. U n taux s u r p r e n a n t d ' a v a n c e de phase /t droite est observ6 chez de n o m b r e u x sujets normaux. U n m o i n s grand n o m b r e de sujets m o n t r e une activit6 alpha gauche en avance de phase. 7. Ces donn6es confirment les publications qui s o u t i e n n e n t que la d o m i n a n c e c&6brale p o u r l'activit6 alpha est le plus s o u v e n t h6misph6rique droite chez les h u m a i n s n o r m a u x , en ce sens que cet h6misph~re i m p r i m e en m o y e n n e u n e avance de phase sur l'activit6 alpha de l'h6misphbre gauche. Mr. A. Pellacani, research EEG technician, provided valuable assistance to the authors throughout this study. REFERENCES ADRIAN, E. D. and YAMAGIWMK. The origin of the Berger rhythm. Brain, 1935, 58: 323-351. AIRD, R. B. and GAROUTTE,B. Studies on the "cerebral pace-maker". Neurology (Minneap.), 1958, 8: 581589. ANDREW, A. M. Lerner's polar analyzer applied to EEG. Electroenceph. clin. Nearophysiol., 1956, 8: 162-163. BARLOW, J. S. Autocorrelation and crosscorrelation analysis in electroencephalography. IRE Trans. reed. Electron., 1959, ME6: 179-183. B~,RLOW, J. S., ROVIT, R. L. and GLOOR, P. Correlation analysis of EEG changes induced by unilateral intracarotid rejection of Amobarbital. Electroenceph. clin. Net, rophysiol., 1964, 16: 213-220. BERLUCCrU, G. Electroencephalographic studies in "split brain" cats. Electroenceph. clin. Neurophysiol., 1966, 20: 348-356.

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BRAZIER,M. A. B. and CASBY,J. U. Crosscorrelation and autocorrelation studies of electroencephalographic potentials. Electroenceph. clin. NeurophysioL, 1952, 4: 201-211. BREMER, F. La synergie interh6misph6rique. Strasbourg todd., 1956, 8: 533-552. BREMER, F. and STOUPEL,N. Recherche d'une participation du corps calleux au m6canisme de la synergie bio61ectrique des h6misph~res c6r6braux. J. Physiol. (Paris), 1957, 49: 66-67. COliN, R. The occipital alpha rhythm: A study of phase variations. J. Neurophysiol., 1948,11 : 3l-37. COHN, R. Clinical electroencephalography. McGraw-Hill, New York, 1949, 639 p. COOPER, R. Electrodes..4mer. J. EEG Techn., 1963, 3: 91-I01. COOPER, R. and MUNDY-CASTLE, A. C. Spatial and temporal characteristics of the alpha rhythm: a toposcopic analysis. Electroenceph. clin. Neurophysiol., 1960, 12: 153-165. CORRIOL,J. Analyse et comparaison de phase en 61ectroenc6phalographie. Electroenceph. clin. Neurophysiol., 1951, 3: 443-448. DENNY-BROWN,D. Discussion. In V. B. MOUNTCASTLE (Ed.), Interhemispheric relations and cerebral dominance. Johns Hopkins Press, Baltimore, Md., 1962: 244. DowNs, T, D. and LIEBMAN,J. The analysis of angular data from vectocardiograms. 4th Ann. Symp. Biomath. Computer Science in Life Sciences, Houston, Texas, 24 26 March, 1966. DUSTMAN, R. E. and BECK, E. C. Phase of alpha brain waves, reaction time and visually evoked potentials. Electroenceph. clin. Neurophysiol., 1965, 18: 433-440. ENOMOTO, T. F. Unilateral activation of the non-specific thalamic system and bilateral cortical responses. Electroenceph. clin. Neurophysiol., 1959, 11: 219-232. FREEDMAN,N. L. Bilateral differences in the human occipital electroencephalogram with unilateral photic drwing. Science, 1963, 142: 598-599. GAROUTTE, B. and A1RD, g. B. Studies on the cortical pacemaker: synchrony and asynchrony of bilaterally recorded alpha and beta activity. Electroenceph. clin. Neurophysiol,, 1958, 10:259-268. GAROUTTE,B., AIRD, R. B. and DIAMOND,M. C. The electroencephalographic pacemaker and function of the corpus callosum. Trans. Amer. neurol. Ass., 1961, 86: 153-156.

GIANNITRAPANI,D. and DARROW, C. W. Differences in EEG time relationships in right and left handed individuals. Electroenceph. c/in. Neurophyslol., 1963, 15: 721. GLANVILLE,A. D. and ANTONITIS,J. J. The relationship between ocopltal alpha activity and laterality. J. exp. Psychol., 1955, 49: 294-299. GREATBATCH,W. Electrochemical polarization of physiological electrodes. Bull. N. Y. Acad. Sci., 1966 (in print). GREEN, J. B. and RUSSELL,D. J. Electroencephalographlc asymmetry with midline cyst and deficient corpus callosum. Neurology (Minneap.), 1966, 16: 541-545. Electroenceph. clin. Neurophysiol., 1967, 22:429-436

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