The EEG as a measure of cerebral functional organization. J C Shaw, K P O'Connor and C Ongley BJP 1977, 130:260-264. Access the most recent version at DOI: 10.1192/bjp.130.3.260

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Brit.J. Psychiat. (i@@7),530, 260—4

The EEG as a Measure of Cerebral Functional Organization J.

Summary.

C.

SHAW,

K.

P.

O'CONNOR

and

Evidence suggests that anomalies

C.

ONGLEY

of functional

organization

brain may be presentin some psychiatricdisordersand that EEG

in the

differences

between psychiatric patients and appropriate control groups may depend on them. It is therefore of practical importance to develop further ways of examin

ing the association between the EEG and such organization. The change in inter-hemisphere coherence(a measure of EEG synchronicity) in the alpha frequency band when carrying out a task is shown to discriminate a group of i i right from i i left preferent normal individuals. Since right and left preference is associated with differences in cerebral functional organization, the coherence measure

may

be a useful

way

of studying

IN'rRonucrrloN or non-specificallyabnormal

when

patients with obviously organic or epileptic causes for illness are excluded and the records are assessed by

visual interpretation.

well established methods

This conclusion

of psychiatric

illness.

schizophrenicpatientscompared with a control

The EEG records of psychiatric patients tend to be normal

this feature

of

is implicit

group.

An

abnormal

distribution of cerebral

blood flow in schizophrenics has been found by Franzen and Ingvar (i97@), and these authors suggest that ‘¿the primary disorder in schizo phrenia is not caused by a loss of function... but by an abnormal distribution of function

in Ellinson's review of 1954, and was reached by Gale in a recent review (Gale, 1976). Nevertheless, as these reviews indicate, there are

within

many

cerebral dominance and disorders of behaviour. These findings have been reviewed by Galin (1974), by Lishman and McMahon (1976) and by Gruzelier and Hammond (1976). Lishman

reports of group

differences when

the

EEG's of psychiatric patients are compared with appropriate control groups. This is particularly

evident when

quantitativemethods are used

(Goldstein et al, 1965; Shaw, 1976). If a way of explaining these group differences can be found, it may be possible to develop appropriate EEG measures giving useful information about the individual patient. In recent years there have been reports suggesting that defects or anomalies of cerebral functional organization may be present in some psychiatric disorders. For example, Beaumont and Dimond (i@73) found impaired inter hemisphere integration in schizophrenic patients on a visual matching task, when compared with non-schizophrenic psychiatric patients and nor mal controls. This followed the finding of Rosenthal and Bigelow (1972) that the width of the corpus callosum is significantly larger in s6o

a

and suggest

and

brain

with

metabolism'. a

an

relationship

McMahon

intact

Finally,

morphology

several

between

found

a small

studies

variables

of

but significant

shift towards left preference in patients with functional psychiatric disorder, as measured by a laterality questionnaire. Gruzeier and Ham mond, using several psycho-physiological mea sures, obtained results from schizophrenic patients implying that ‘¿the dominant hemisphere of schizophrenics displays “¿weak― nervous system dynamics', and demonstrated that ‘¿on some measures chlorpromazine reverses a lateralized deficit'. There is some evidence that the EEG indi cates laterality differences in psychiatric dis order (d'Elia and Perris ‘¿974,Serafetinides, 1973).

suggest

Shaw

(1976)

a hypothesis

has

reviewed

that

EEG

evidence

to

differences

J. C. SHAW, K. P. O'CONNORAND C. ONGLEY between psychotic patients and control groups are a measure of differences of cerebral func

tional organization. Although these differences might be explained in other ways, this hypo thesis has considerable heuristic value and is one we are pursuing. This paper describes a pilot experiment to examine

the

relationship

between

the

EEG

and cerebral functional organization. It is part of an investigation to develop EEG measures suitable for further study of the above hypothesis, and itcompared groups of rightand leftpre

ferent individuals. There is abundant experimental and patho logical evidence that in right handers the left hemisphere is specializedfor language and

information processing involving serial coding generally, while the right hemisphere is con cerned with spatial perception and other parallel coding. In the left preferent individual this lateralization of function is less specific and Beaumont (@7i@) has suggested a model in which right handers have a few large units each of high functional specificity, whereas left handers have many small units of relatively low specfficity. If EEG differences were also dependent on the size of such functional units, group EEG differences would be expected. Studies in which these differences have been demonstrated are reviewed by Butler and Glass (1976). Because our experiment involves computer analysis of multi-channel EEGs, a large number of results are obtained. Since our aim is to introduce this different approach to the possible application of the EEG in psychiatry as a basis for further reports, only a small subset of these results are presented here. METHODS

Our EEG data have been analysed in twoways. Firstly, power spectra have been computed for individual recording channels. This is a form of frequency analysis in which the total amplitude variance of an EEG signal is ex pressed as components of variance in many small frequency bands. In our case there are 15 bands from 2 to 30 Hz, each 2 Hz wide. Our second method uses the coherence function, a measure of the correlation between the signals recorded

261

in two channels, similarly expressed as a function of frequency (Shaw, Ongley and O'Connor, in preparation). In the present context it may be regarded as a measure of synchronicity between two recording areas. EEGs were recorded with subjects at rest, and while carrying out two mental tasks, from 12 right preferent and 12 left preferent indi viduals classified by a laterality questionnaire

(Humphrey, 1951). The results from one subject from each group were discarded be cause they had low laterality scores and there was positive evidence for an acquired pre ference in one of these. These groups were selected from teacher training college students and hospital nursing staff and did not differ significantly

in

sex

or

age

distribution.

All

subjects had participated in at least one other EEG experiment.

One task was mental arithmetic, the problems being chosen to have equal difficulty and a mean solution time of 5 seconds according to the principle of Thomas (1963). The 5 seconds immediately following presentation of a prob lem constituted one trial of the mental arith metic task. In each problem of the other task the subject had to use spatial imagery to re construct a figure composed of vertical and horizontallinesfrom informationpresented verbally at a constant rate for 10 seconds. These required

an answer at the end of the 10 seconds

and this constituted one trial of the spatial imagery task, but only the first 5 seconds was used for EEG analysis.

These tasks were chosen because of the evidence that in right preferent individuals, mental arithmetic involves the left hemisphere and visuo-spatialprocessing the right hemi

sphere,in accordancewith themodel referred to above. The tasks were pre-recorded and presented from magnetic tape. Ten channels of EEG and a trial marker signal were recorded

on paper and on magnetic

tape, using frequency modulation. The montage was a common reference one using F@to C4, P4, 02, T4 and T6, on the right hemisphere, and to C3, P3, 0,, T, and T5 on the other (Io—2oInternationalSystem). Subjects were

seated room.

on an aircraft

chair

in a darkened

262

THE EEG AS A MEASURE

OF CEREBRAL

Following an initial period of base-line recording, subjects were presented with three conditions in random order over subjects. Two of these conditions were the tasks already described, and trials were presented in each of these at random intervals with a range and mean of 20 seconds. Ten habituation trials were given to make sure the instructions were under stood, and then sufficient trials were presented to obtain io correct answers. This made sure that subjects were mentally active during the trial and also made it possible to compare the levels of difficulty of the two types of task. The number of trials required for xo correct answers were not significantly different for the two tasks and the two groups. They were therefore judged as being in the same difficulty range, and this was supported by subjective reports. The third condition was continuous eyes shut rest, again with io habituation trials. Trial marker signals were recorded at similar random intervals as for the tasks to index the 5 second epochs for analysis in this condition. Eight channels of EEG for 8 trials in each of the conditions were tranferred to digital tape for signal analysis on a PDP ‘¿2 computer. Thus 40 seconds

of eight-channel

EEG

for each

condi

tion for each subject was available for analysis. A comprehensive signal analysis system de veloped by one of the authors (Ongley, in preparation) was used to compute power spectra and coherence functions. These were appropriately averaged over the eight trials in each condition and compressed to give the 15 point spectra with values for 2Hz frequency bands with a 2Hz separation from 2 to 30Hz. The number of possible coherence functions is the number of combinations of 8 channels taken two at a time, namely 28. To reduce this number to manageable proportions, only all possible intra-hemisphere pairs and the four inter-hemisphere pairs between homologous electrode sites, were used. This gives i6 co herence functions.

FUNCTIONAL

ORGANIZATION

electrode), and to give further data reduction, power spectra and coherence values for the alpha frequency band only are considered,by

appropriately combining data from the bands centred on 8, io and 12 Hz. The result of interest is the change in inter hemisphere coherence between a rest and task condition. In the case of the spatial imagery task this inter-hemisphere coherence increased in 8 of the i i right preferent group and de creased in 8 of the i i left preferent. This is illustrated in Fig i, in which subjects are ranked in order of the magnitude and sign of this change. Each bar of the histogram is the difference between the coherence measured during the spatial task and that measured during rest. The clear bars are right handers, the black ones left handers. The Mann-Whitney U test shows the change in coherence to be significantly different for the two groups (Table I). The coherence and power spectra results were compared in the following way. The difference between the alpha band power from the F5-P3 and F2-P4 derivations was found for each condition. The table indicates that the change from rest to task of this inter-hemisphere power difference score did not discriminate the groups. Similar results were obtained for the mental

arithmetic

task,

and

these

are

also

shown in Table I. The right handers all had the same sign of inter-hemisphere coherence change for both tasks, but in five of the left handers the sign of the change differed. Of the six individuals who did not fit the pattern of increase in inter-hemisphere co herence in right handers and decrease in left •¿50

TASK—REST DIFFERENCEIN INTER-HEMISPHERE COHERENCE ALPHA BAND, FZ-P4/FZ-P3

1flh-i-@.., .4.

RIGHTPREFERENTSUBJECT

RESULTS

As already indicated, only a subset of the results are presented here. These are from the F2-P3 and F5-P4 derivations (i.e. right and left parietalelectrodesreferredto a mid frontal

LEFT PREFERENTSUBJECT

F:o

1.—The difference

in inter-hemisphere

EEG

co

herence (alpha band) between rest and spatial imagery task conditions. Open bars are right, black bars are left,

preferent subjects.

J. C. SHAW, K. P. O'CONNORAND C. ONGLEY

263

T#@nI2I Test of thjerence between rig/it and left preferent groups bj Mann-Whitney U test

EEG measure

tail)Spatial Task

Mann Whitney U

P (two

imagery

o@oo36

Coherence o.oog6Spatial Mental arithmetic

21

imagery

55

0@72

Power Mental arithmetic [email protected]

6o

IITest testEEC

of contingencybetween laterality score and EEC measures with the Fisher exact probability

scoreTask-rest measure

Laterality

difference

arithmeticHigh Spatial imagery tail)Predicted

Low 13

Mental

P (one tail) High

3

Coherence

Low

12

P (one

3

0@011

Not 5Predicted predicted

I

5

5

2

Power

0@03

2 6

5

6

5

o@@6

Not predicted

10

5

handers, all but one had lower scores on the laterality questionnaire than the remaining subjects. Therefore a prediction was made that right preference coupled with a high dexterity score will show an increase in inter-hemisphere coherence and that left preference with a high sinistrality score will show a decrease. This was tested by the Fisher exact probability test and is shown in Table II. The prediction is upheld for both tasks, and again the power measures show no significant effect. DIscussIoN

The only apparent behavioural feature distinguishing our two groups was their score on a laterality questionnaire. The evidence cited above suggests that this indicates a difference in functional organization in the brain. Our results show that the change in alpha band inter-hemisphere coherence from rest to task discriminated the differences in these experimental groups. Coherence appears to be more sensitive than power measures for

O@33

this purpose, and may have a quantitative relationship to the scores on the laterality questionnaire used to select the groups. The EEG coherence function was chosen as an appropriate measure for this work on the basis of the following postulate. Cortical areas at rest have a high degree of synchronous EEG activity, resulting in high coherence between them. An area involved in processing informa tion becomes desynchronized, so reducing its coherence

with other areas still at rest. It was

anticipated that we would be able to interpret our intra-hemisphere results in terms of this model, but so far this has not proved to be the case. They are therefore being further analysed to see if some other, more appropriate model can be found. In the meantime the inter hemisphere coherence changes reported here are of interest in the context of our study, and we are currently analysing data collected from two new groups* to see if they are confirmed. * This

replication

has

now

been

completed

and

the

re

sults described here confirmed in every respect (in pre).

264

THE EEG AS A MEASURE

OF CEREBRAL

Inter-hemisphere EEG coherence measures have previously been shown to discriminate

dyslexic

children

hyperkinetic

(Sklar

children

appropriate

control

et

al,

1972)

(Montagu, groups,

and

1975) from

and

to

show

dif@

ferences between

right and leftpreferent groups

(Giannitrapani,

1973).

These

studies

support

the results presented here indicating that EEG coherence

measures

functional

may

organization.

relate

If

to

they

are

cerebral

confirmed,

we will develop these measures further to investigate this aspect of psychiatric disorders.

FUNCTIONAL

ORGANIZATION

[email protected],D. (1974)Implications forpsychiatryof leftand right cerebral specialization. Archivesof General Psjchiatrj, 31,572—83. Girrs@m, D. (‘973) Brain areas dominance deter mined by EEG phase-angle and coherence spectra. &c.rpta Medica International Congress Series, 236, 141. GoI.DsTEns,

L.,

[email protected]@i, A. A.,

[email protected], H.,

Mua

piraza, H. B. & PFE1PPER, C. C. (1965) Electro cerebral activity in schizophrenics and non-psychotic subjects:quantitativeEEG amplitude analysis. Electroencephalography and Clinical Xeurop4ysiology, i@, 350—61. GRuZEUER, J. & HAiIMol@m, N. (1976) Schizophrenia:

a dominant hemisphere temporal-limbic disorder? Research Commwzicationsin Psychology, Psychiatry and Behaviour, I.

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4PQ,

(Received 2 June 1976)