INTERNATIONAL JOURNAL OF PSYCHOPHYSIOLOGY

ELSEVIER

International

Journal of Psychophysiology

23 (1996) 145-153

EEG coherence or EEG correlation?

Miguel Angel Guevara, Maria Corsi-Cabrera
Facultad de
Psicologia, Posgrado, Unirersidad National Autdrzoma de M&co, AC,. Urkersidad

*
D.F. 04510, M&co

3004, M&co,

Instituto de Neurociencias, Received 21 November

Universidad

de Guadalajara,

Guadalajara,

Jalisco, Mexico 19 March 1996

1995; revised 16 March 1996; accepted

Abstract In view of the widespread use of electroencephalographic correlation (Y) and coherence (Co/z) analyses in studying brain functional relationships, it seems important to illustrate results yielded by both methods. Although they are considered as equivalent, they show important differences. Results obtained from r and Coh were compared using: (a) 2 Hz sinusoidal signals, where phase and amplitude were artificially manipulated and, (b) Coh and r spectra obtained between each pair of derivations (C3, C4, F3, F4, T3 and T4) from wakefulness, stage 2, stage 4 and paradoxical sleep (n = 8). The following results were obtained: significant Pearson product-moment coefficients were obtained between r and Coh spectra in the range of 0.86 to 0.96 for interhemispheric and 0.60 to 0.90, for intrahemispheric pairs; as a result of principal component analyses, the same three frequency bands were formed for r and Coh spectra with the exception of one single bin; similar results for Y and Coh were obtained by two-way ANOVAs (physiological stages by derivations). In conclusion, as expected, a high degree of comparability between r and Coh was observed under normal physiological conditions and with the use of good quality recordings.
Keywords:

EEG coherence;

EEG correlation;

Sleep; Wakefulness;

Interhemispheric;

Intrahemispheric

1. Introduction The study of functional relationships between two brain regions has been one of the key issues since the development of the electroencephalogram. As early as 1951, the cross-correlation function was used to study the similarity between two EEG signals (Brazier and Casby, 195 1, 1952). Its application in a number of different areas of research in several species including men, on the assumption that the higher the correlation, the stronger the functional

* Corresponding author. Tel.: +52 25-60; e-mail: corsi@servidor.unam.mx 0 167.8760/96/$15.00 Copyright PII SOl67-8760(96100038-4

622-22-51:

Fax: +52 550-

relationships between both regions (Shaw, 198 1, 19841, includes the study of interrelationships between different cortical regions in relation to sensory stimulation, voluntary movements, effect of drugs and a wide range of clinical problems (for a review of early literature, see: Barlow, 1973; Matousek, 19731, and at different levels of alertness and sleep (Barcaro et al., 1986; Corsi-Cabrera et al., 1987, 1988, 1989, 1992; Guevara et al., 1995). It has been used in animals to investigate the mechanisms by which EEG waves are generated through the study of relationships between unit discharges and EEG waves and of the relationships between the cortex and subcortical structures (Bland, 1985; Steriade et al., 1996), and, also to investigate interrelationships be-

0 1996 Elsevier Science B.V. All rights reserved.

146

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23 (1996)

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tween multiunit (Moiseeva, 1979) and single unit activity (Wilson and McNaughton, 1994). With the development of digital computation and of new computational algorithms, such as the Fast Fourier Transform, the use of correlation was gradually put aside and replaced by an alternative mathematical method, the coherence spectrum. This method gives similar information as correlation, but has the advantage of showing the covariation between two signals as a function of frequency and in a rather short time. Coherence studies have been successfully conducted in many fields, including those dealing with cognitive functions and psychiatric disorders (for a review, see: French and Beaumont, 1984). The calculation of correlation for the same number of frequencies involves filtering of the signal through the desired number of bands or frequency bins, either by means of analog devices or by digital filtering. When using analog devices, either separate analog filters are needed for each frequency or the signal must be replayed as many times as bands are desired. These procedures have some disadvantages in that they are time and memory consuming. Both methods, correlation (r) and coherence (C&z), are considered as equivalent in that they evaluate the degree of similarity between two signals but through different mathematical calculations (Shaw, 1981, 1984). The EEG represents a set of continuous voltage/time values and may therefore be considered as a multivariate time series that belongs to the category of stochastic processes which cannot be described by deterministic mathematics rather they can be described only by probability distributions. The concept of temporal stochastic process may be extended, in the case of the EEG, to the spatial domain (Nunez, 1995). The stochastic nature (temporal and spatial) of the EEG allows the use of correlation and coherence analyses which presuppose independence between successive points in time. The coherence function (C&j at each given frequency x is defined by:

The correlation function quency x is defined by: r(x) = C,a(x)/(C,,CF3a)

(r)

at each given

fre-

Coh( x) = IS.4,( X>I/&A(

x)&3(

x))

where IS,,1 is the cross-spectrum between the signals A and B; S,, is the autospectrum of the signal A; S,, is the autospectrum of the signal B.

between the sigwhere C,, is the cross-covariance of the nals A and B; C,, is the auto-covariance signal A; C,, is the auto-covariance of the signal B (Bendat and Piersol, 1980; Shaw, 198 1, 1984). However, there are important differences between them. Coherence is calculated by dividing the numerical square of the cross-spectrum by the product of the autospectra. Therefore, it is sensitive to both a change in power and a change in phase relationships. Consequently, if either power or phase changes in one of the signals, the coherence value is affected. Another important difference is that the value of coherence for a single epoch is always one, regardless of the true phase relationship and the differences in power between the two signals. Over successive epochs the coherence measure is dependent on power and phase of the two signals along the epochs. If there is no variation over time in the original relationship between the two signals, the coherence value remains unity. This means that coherence does not give direct information on the true relationship between the two signals, but only on the stability of this relationship with respect to power asymmetry and phase relationship. Correlation, on the other hand, may be calculated over a single epoch or over several epochs and it is sensitive to both, phase and polarity, independently of amplitudes. The calculation of coherence involves squaring the signal, thus producing values which go from 0 to 1, and a loss in polarity information. By contrast, correlation is sensitive to polarity and its values go from - 1 to 1. However, under normal physiological conditions, no strong and abrupt power asymmetries would be expected to occur. Thus, the influence of power on coherence should be negligible and results similar to those produced by correlation also would be expected for the coherence measures. In contrast to correlation coherence is a very complex measurement and is not easy to understand, whereas correlation is based on a simple method, which requires no specialized mathematical knowledge. Although, for a trained mathematician the similarity between both techniques is obvious and the con-

M.A. Guevara, h4. Corsi-Cabrera /International Journal of Psychophysiology 23 (1996) 145-153

147

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Fig. 1. This figure illustrates the differences and similarities between correlation and coherence using four epochs of a pair of 2 Hz sinusoidal signals. The Pearson product-moment coefficients at 0 lag (r) and coherence (Cob) values for each l-s epoch, and the mean r (on), and Coh for the successive four epochs are given for each pair of signals. Voltage and phase were manipulated in one of the signals of each pair. Voltage was multiplied by 3 in A, C, D, F and G. Phase was delayed by 90 degrees in B, C, E, F and G. Observe the effect of amplitude manipulations of the lower signal of each pair on r and Coh in A, C, D and G, and the effect of phase delay in B, C, E, F and G.

ditions under which similar results would occur are predictable, this is not the case for all readers interested in EEG. Therefore, in view of the widespread use of both methods in studying brain activity, we felt it would be useful to illustrate the results yielded by each method and to demonstrate the extent to which the results are comparable. In the present communication our intention is not to discuss coherence and correlation from a mathematical point of view, but simply to facilitate the understanding of these techniques and to statistically compare these two methods by presenting the results obtained by both methods, using two kinds of signals: (a) artificially generated signals in which phase, polarity and amplitude are manipulated in order to illustrate and make comprehensible the similarities and differences between correlation and coherence. For this purpose, l-s epochs of 2 Hz sinusoidal signals were used and (b) true EEG signals, in order to compare the statistical results obtained under different behavioral and physiological conditions with each method, using the same EEG information. Fig. 1 illustrates the differences between correlation and coherence with respect to phase and voltage using a pair of 2 Hz sinusoidal signals. The r and Cob values for l-s epochs, and the mean r and Coh for the successive four epochs were calculated at 0 lag. Thus, Cob was always unity for the first epoch and it increased or decreased as a function of the stability over successive epochs. 1. In the first comparison, voltage was multiplied by 3 in one of the channels along the four epochs. Phase delay was 0 (Fig. 1A). Mean r and Cob values are unity. 2. Voltage was kept the same in both channels, but phase was delayed 90 degrees in one of the channels over the four epochs (Fig. IB). Mean r is=Oand Cob is= 1. 3. Voltage was multiplied by 3 and phase was delayed 90 degrees over the four epochs in one channel (Fig. 1C). Mean r is = 0 and Cob is = I. 4. Voltage was multiplied by 3 in one channel, but only in two of the four epochs. Phase delay was 0 (Fig. ID). Mean r is = 1 and Cob is = 0.8. 5. Voltage was kept unaltered and phase was delayed 90 degrees, but only in two of the four epochs (Fig. 1E). Mean r is = 0.5 and Cob is = 0.5.

6. Voltage was multiplied by 3 and phase was delayed 90 degrees in two of the four epochs (Fig. 1F). Mean r is = 0.5 and Coh is = 0.5. 7. Voltage was multiplied by 3 in two epochs in both channels (Fig. lG), or phase was delayed 90 degrees in two epochs in both channels (Fig. IH) where r and Cnh were unity. Correlation was not affected by changes in voltage (1 and 4) and was sensitive only to changes in phase (2, 3, 5 and 6) between the two signals. In contrast, coherence was not sensitive to differences in phase (2 and 3) or in voltage (1 and 3) between the two channels as long as the same relation between the two signals was maintained. However, when either voltage or phase were changed in one channel and in one or several epochs, coherence changed as a function of the stability of the relationship between the two signals (5, 6 and 7). The details and calculations of the results illustrated above are available on request. These results illustrate that correlation gives information on the time coupling and waveform similarity between the two signals independently of amplitudes whereas, coherence gives information on the stability of the similarity without knowledge as to whether a given Cob value is the result of changes in power or changes in morphology. When the interest is to know the stability of the relationship between two recording sites including both power asymmetries and morphology, coherence is the better method. When the main interest is focused on waveform and time coupling between two sites, correlation is a better choice. However, it is important to realize, as already mentioned, that under normal physiological conditions, no strong and abrupt power asymmetries are to be expected. Therefore, the influence of power on coherence can be considered to be negligible, and results obtained by both methods should be similar. To illustrate this, the results obtained from the classical correlation technique for inter- and intrahemispheric relationships during wakefulness, slow wave sleep and paradoxical sleep, are compared with the results obtained from coherence for the same EEG signals. Subjects and EEG recording procedures were exactly the same as those described by Guevara et al. (1995) for EEG correlation. Briefly, the EEG signals were taken from nine adult males between 22 and 30

M.A. Guerlara, M. Corsi-Cabrera/International

Journal of Psychophysiology 23 (19961 145-153

149

years old considered free of sleep and neurologic complaints during the second uninterrupted night spent at the laboratory under the following conditions: wakefulness (W) with eyes closed before going to sleep, stage 2 sleep (S2), stage 4 sleep (S4) and paradoxical sleep (PS) occurring during the second sleep cycle. EEG was recorded at F3, F4, C3, C4, T3 and T4 referenced to the ipsilateral earlobe with a Grass Model 16-E polygraph with bypass filters set at 1-35 Hz. Electrode impedance was kept below 10 kOhm. The same ten 2-s artifact-free epochs, digitized at 128 Hz, used for EEG correlation in Guevara et al. (1995), were used here for coherence analysis and for the statistical comparisons between both meth-

ods. The second cycle of the night was chosen for these comparisons, because results from principal component analysis and from ANOVAs between sleep stages and wakefulness obtained for EEG correlation of cycle 2, were similar to those obtained when the first three cycles of the night were analyzed (Corsi-Cabrera et al., 1996). The EEG signals were digitally filtered by means of a Fast Fourier Transform using rectangular windows, and correlation and coherence spectra were calculated for every condition and pair of derivations at every 0.5 Hz (INTER: C3-C4, F3-F4 and T3-T4 and INTRA: C3-T3, C4-T4, F3-T3, F4-T4, F3-C3 and F4-C4). Spectra were limited from 1.5 to 15 HZ, because the digitized higher frequencies were com-

0.a

Fig. 2. This figure illustrates the correlation (r) and coherence (Co/t) spectra between the EEG activity at F3 and F4 of one subject during wakefulness with eyes closed (A), stage 2 (B), stage 4 (C) and paradoxical sleep (D) of the second sleep cycle of the night. EEG signals were digitally filtered for every 0.5 Hz using rectangular windows. Pearson product-moment coefficients were calculated in the time domain between the pair of signals for every 0.5 Hz. The similarity between both spectra can be observed.

150

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Table 1 Pearson product-moment correlations (I) between coherence and correlation spectra for every pair of derivations, sleep stages 2 (S2), 4 (S4), paradoxical sleep (PS) and wakefulness (W) s2
r

s4
r

PS
r

W
r

F3-F4 c3-c4 T3-T4 F3-C3 F3-T3 C3-T3 F4-C4 F4-T4 C4-T4

0.95 0.96 0.86 0.73 0.77 0.68 0.74 0.80 0.88

0.95 0.96 0.88 0.64 0.74 0.76 0.86 0.8 1 0.89

0.92 0.94 0.90 0.64 0.81 0.60 0.65 0.69 0.46

0.94 0.94 0.90 0.80 0.80 0.88 0.73 0.84 0.90

p < 0.05 = r 0.38; p < 0.01 = r 0.44 (df = 28).

prised of a very few points and may render inaccurate results (i.e. 6 points at 21 Hz). Correlation spectra were obtained by means of Pearson productmoment correlation coefficients calculated in the time domain for every narrow band, and coherence was derived from the cross-spectrum amplitudes and the two corresponding power spectra (Shaw, 198 1, 1984) using a program developed by one of the authors for this purpose (Guevara et al., 1992). Calculation time for 10 epochs for both correlation and coherence spectra was similar (0.40 and 0.41 s for coherence and for correlation respectively in a 486, 33 MHz PC). Coherence and correlation values were trans-

formed to Fishers Z scores before statistical analysis to guarantee a normal distribution. Fig. 2 shows an example of the correlation and coherence spectra for the same pair of derivations and condition. It can be seen that they follow a very similar pattern. A peak of r and Cub can be observed during wakefulness in the alpha range compared to other frequencies. Also, higher r and Coh values can be observed during sleep than during wakefulness. To evaluate the degree of similarity between correlation and coherence spectra, Pearson product-moment correlations were calculated between the correlation and the coherence spectra of the same condition (W, S2, S4 and PS) and the same pair of derivations (Table 1). The r values between interhemispheric r and Coh are above 0.85, indicating that the percentage of shared variance by both methods was very high. In the case of intrahemispheric derivations, the proportion of variability shared by the two methods was lower. The r values can be seen to range from 0.90 to 0.60, except between C4-T4 during PS where the value drops to 0.46. However, all of the values are beyond the 0.05 significance level. With the purpose to determining which frequencies covaried together and which were independent, correlation and coherence spectra were separately subjected to principal component analysis with the EEG frequencies as variables, using Varimax rota-

Table 2 Principal Hz

component Eigenvectors

analysis

of EEG correlation Hz

for every 0.5 Hz rotated values Eigenvectors 1 2 - 0.205 - 0.285 - 0.256 - 0.325 - 0.272 -0.181 -0.310 - 0.243 3 0.538 0.576 0.555 0.438 0.554 0.684 0.638 0.72 1 11.0 11.5 12.0 12.5 13.0 13.5 14.0 14.5 15.0 Hz Eigenvectors 1 0.245 0.168 0.259 0.224 0.389 0.275 0.219 0.282 0.348 2 -0.531 -0.581 - 0.657 -0.681 - 0.626 - 0.670 - 0.752 - 0.688 - 0.628 3 0.444 0.493 0.223 0.174 0.195 0.273 0.300 0.254 0.313

I
1.5 2.0 2.5 3.0 3.5 4.0 4.5 5.0 5.5 6.0 6.5 0.533 0.525 0.55 1 0.685 0.568 0.644 0.489 0.643 0.66 1 0.570 0.59 1

2 -0.191 - 0.395 - 0.433 -0.281 - 0.296 - 0.378 -0.133 - 0.340 -0.153 -0.131 - 0.226

3 0.289 0.121 0.175 0.234 0.274 0.097 0.370 0.085 0.308 0.288 0.378 variance 7.0 7.5 8.0 8.5 9.0 9.5 10.0 10.5

0.432 0.362 0.35 I 0.418 0.401 0.265 0.082 0.183

Accumulated

percent of explained

44.42

49.38

53.91

M.A. Gueuara, M. Cord-Cabrera/Intemational Table 3 Princiual comaonent Hz Eigenvectors

Journal of Psychophysiology 23 (1996) 145-153

151

analvsis of EEG coherence HZ 2 -0.190 - 0253 - 0.276 - 0.258 - 0.295 - 0.348 -0.231 - 0.274 -0.145 -0.157 -0.183 3 0.100 0.242 0.210 0.215 0.300 0.193 0.411 0.356 0.488 0.39 1 0.494 variance 7.0 7.5 8.0 8.5 9.0 9.5

for every 0.5 Hz rotated values Eigenvectors 1 0.395 0.437 0.373 0.379 0.308 0.174 0.217 0.231 0.267 2 -0.314 - 0.292 - 0.227 - 0.337 - 0.260 - 0.277 - 0.347 - 0.407 - 0.436 3 0.549 0.544 0.632 0.557 0.696 0.723 0.678 0.63 1 0.514 11.5 12.0 12.5 13.0 13.5 14.0 14.5 15.0 HZ Eigenvectors 1 0.199 0.230 0.411 0.24 1 0.27 1 0.285 0.280 0.325 2 0.593 0.645 0.698 0.760 0.744 0.745 0.736 0.647 3 00.479 0.324 0.342 0.233 0.212 0.195 0.279 0.267

1
1.5 2.0 2.5 3.0 3.5 4.0 4.5 5.0 5.5 6.0 6.5 0.725 0.586 0.673 0.684 0.650 0.649 0.596 0.637 0.543 0.563 0.518

10.0
10.5 11.0

Accumulated

% of explained

46.72

52.31

59.3 1

tion (Becker et al., 1982; Kabuto et al., 1993). The results from principal component analysis were very similar for r and Cob spectra as shown in Tables 2 and 3, respectively. The first three components for coherence explained a slightly higher percentage of the total variance (59.31%) than was the case for correlation (53.9 1%). However, the frequencies forming the three components were very similar in both analyses. The first component was formed by slow frequencies from 1.5 to 6.5 Hz and explained 44.42% of the variance in the case of correlation and 46.72% in the case of coherence. The boundaries between the second and the third components were slightly different. In the case of correlation the second component was formed by frequencies ranging from 11.5 to 15 Hz, corresponding to sleep spindle

frequencies, and explained 4.96% of the variance. In the case of coherence the boundary range included 11 Hz and explained 7.00% of the variance. The amount of variance accounted for by the third component was small, being 4.5% for correlation and 5.59% for coherence. It included middle frequencies from 7 to 11 and from 7 to 10.5 Hz, respectively. The raw EEG signals were again digitally filtered, with the new boundaries using square windows. INTER and INTRA hemispheric r and Coh were recalculated for these new bands. In order to compare statistical results between physiological conditions, both, coherence and correlation values were separately submitted to two-way ANOVAs for repeated measurements, with sleep stages and wakefulness as one factor and pair of derivations as the other

Table 4 Results of two-way ANOVAs of inter- and intrahemispheric correlation (r) and coherence (Cob) for the three eigenvectors (Eigvl, Eigv2, Eigv3) of the principal component analysis with stage 2, stage 4, paradoxical sleep and wakefulness as one factor (A) and derivations as the second factor (Bl Interhemispheric A df = 5,191 Eigv B df = 3,191 0.00001 0.00001 O.OOQOl 0.00001 0.00001 0.00001 AXB df = 15,191 0.60 0.56 0.82 0.35 0.84 0.76 Intrahemispheric A df = 5,191 0.06 0.001 0.00001 0.00001 0.002 0.01 B df = 3,191 0.001 0.0005 o.oOOQ7 0.00001 0.00008 O.OOOGl AXB df = 15,191 0.87 0.93 0.53 0.70 0.99 0.99

r Coh r Coh r Coh

0.00001 o.OOOQ1 0.00001 O.OOOQl 0.004 0.02

Eigv2

Eigv3

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factor. Tukeys Student-t tests were used for posthoc comparisons between means, when main effects were significant. Table 4 summarizes the statistical results obtained with the two-way ANOVAs for correlation and coherence. All derivation main effects were significant for correlation as well as for coherence, and results of pairwise comparisons were similar. In the case of INTER, correlations between T3 and T4 gave lower values than those obtained for F3-F4 and C3-C4. In the case of INTRA, the correlation values obtained for F3-T3 were lower than those obtained for F3-C3 and C3-T3. In the case of the right hemisphere there were more significant differences for coherence than for correlation. Coh between F4 and T4 was lower than between F4 and C4 and between C4 and T4. However, the correlational analyses did not reveal significant differences within the right hemisphere. The main effects of sleep for the first three components were also very similar for r and Coh. The main effects for slow frequencies and for sleep spindle frequencies were significant for INTER as well as for INTRA. The results from pairwise comparisons showed that r and Coh of slow frequencies were higher during S2, S4 and PS than during W, and that r and Coh of slow frequencies were higher during S2 and S4 than during W. INTER and INTRA r and Coh of middle frequencies were higher during PS than during W. The only difference between both methods was observed in the case of INTRA of the slow frequency band, which in the case of r did not reach statistical significance, although it was near the p 0.05 level. Two main points are supported by the comparisons presented. (a) any advantages of showing the covariation of two signals as a function of frequency and the time saving capabilities of the coherence spectrum calculation are negligible based on the present form for calculation of the correlation spectrum. (b) In spite of some differences between both techniques, the results obtained with EEG signals under normal physiological conditions, as expected, indicate a high degree of statistical equivalence between correlation and coherence spectra. The Pearson product-moment coefficients between both spectra revealed highly significant correlations between correlation and coherence spectra for all conditions and pair of derivations. The principal component

analyses showed that the first three components from each method are formed by the same frequencies with the exception of one single bin (11 Hz). Finally, a high degree of similarity between the results obtained with ANOVAs for correlation and coherence data were found in the comparisons of differences between different normal behavioral and electrophysiological conditions. The results indicate that a large amount of variance is shared by the two methods. Intrahemispheric comparisons showed more differences between the two methods than interhemispheric comparisons. While these differences may be attributed to greater unstability of power within regions of the same hemisphere which is reflected in coherence but not in correlation, further exploration is needed. In conclusion, the present results endorse a high degree of comparability of results obtained with either method, provided normal physiological conditions and good quality of EEG recording exist.

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