Folia Psychiatrica et Neurologica Japonica. Vol. 13, No. 1, 1959.

STUDIES ON MODIFICATION OF CORTICAL ELECTRI- CAL POTENTIALS BY OVERLYING STRUCTURES AND SUBSTANCES, WITH SPECIAL REFERENCE

TO SUBDURAL HEMATOMA

BY Kunikazu Suhara and Kazuki Sakata

Second Surgical Division, Gifu Medical College, Gifu (Director: Prof. Dr. T a k a o Take tomo)

Focal flattening, or focal reduction in amplitude of EEG, is one of the EEG abnormalities seen in cases of unilateral chronic subdural hematoma. As to its cause, some authors (Jasper et al. 1940, Motokawa 1947, Matsuzaki 1957) insist upon the short-circuiting effect of the hematoma on cortical electrical potentials while others (Ulett 1945, Sullivan et al. 1951) suppose the responsible factor is the reduction in amplitude of cortical electrogram per se. From viewpoint of common sense, presence of the short-circuiting effect may well be supposed, irrespective of whether the latter opinion is right or wrong, provided that the hematoma is cmsiderably large and thick enough.

However, 2 cases of unilateral chronic subdural hematoma were recently encountered by us in which scalp EEGs showed normal symme- trical alpha waves despite of extensiveness and thickness of the hematoma. This made us feel the necessity of experimental inquiry into the last view- point mentioned. The problems to be solved center here on whether the short-circuiting effect is actually present or not, and further, if present, on whether it is really negligible as compared with modifying effects of the skull and scalp on cortical electrical potentials or not. To solve the latter problem of modifying effects of the skull and scalp, of complicated volume conductors, of the normal adult on cortical potentials, they need quantitative estimation aforehand, but with reports on the theme quite scarce up to date, it wants certainly an inquiry anew.

This report includes presentation of the 2 clinical cases and results of experiments done in craniotomized adult patients to solve above problems.

Materials and Method

Experimental studies were carried out in various clinical cases, in which relatively large bone flaps were made, before intracerebral operative procedures began. I n these cases neither distinct scar tissue nor tumor could be observed on the cortical surface exposed. Electrode used in the experiment consisted of a silver plate with a diameter of 9 mm. Electrode placements and leading patterns will be shown in the figures. Monopolar records were taken in relatively monopolar way generally. Distance between the centers of two electrodes put in a pair was routinely made 3 cm, a relatively small distance as compared with diameter of the bone flap. ~_________ ~~ __ ~ - ~

Received for publication, November 2, 1958.

82 K. Suhara and K. Saka ta :

All the resordj excepting EEG of Case 1 were obtained by a San&i 12 channel electroencephalograph. while EEG of Case 1 was recorded by a n Ediswan 8 channel electroencephalograph. The standard electrode plazements (Jasper , 19-11) were routinely used to obtain scalp EEG.

Presentation of Cases

S. S., a 40 year-old man, complaining of headache. He received a head injury about 4 months before EEG recording. A subdural hema- toma thoroughly encapsulated was found covering wide areas of the left cerebral convexity, as thick as about 3 cm (cf Fig. 1 ) . In the presence of such a large and thick hematoma, scalp EEGs led bipAarly as well as monopolarly gave symmetrical alpha waves (Fig. 1 ) .

Case 2. T. I., a 35 year-old man, with generalized convulsive seizure as chief complaint. He suffered from a head injury 12 and a half years before EEG recording. The subdural hematoma enveloped in a calcified capsule was found covering wide areas of the left cerebral convexity, as thick as about 2 cm (cf. Fig. 2). Scalp EEGs led bipdarly as well as monopolarly showed symmetrical alpha waves (Fig. 2) .

The mean peak-to-peak amplitudes of alpha waves were measured in the above cases. The ratios of those on the hematoma side to those on the intact side gave ( 1 ) C?-Al/C4-A2 = 1.01, F3-C3/F4-C4 =0.98, C?-P3/C4- P4=0.99 in Case 1 and (2) C3-Al ,'C4-A2=0.93, FS-C?/F4-54= 1.05, C3- P3/C4-P4=0.92 in Case 2. These values do not always indicate a lower amplitude on the side of the lesion. Moreover, they may not be significant as compared with errars on the side of the recording apparatus.

There will be no need to show any example of EEG displaying typical

Case 1.

A-P

I 1 I I A A A A h 4 Fig. 1. Grossly symmetrical EEG (bipolarly led) in the presence of a large unilateral subdural hematoma. Inset is a sketch of an antero-pos- terior arteriogram.

Modification of Cortical Potentials by Subdural Hematoma 83

Fig. 2. Grossly symmetrical EEG (monopolarly led) in the presence of a large unilateral calcified hematoma. Inset is a sketch of a lateral roentgenogram showing calcified area.

focal flattening in the presence of a unilateral subdural hematoma. Ratio of mean alpha amplitude on the side of the lesion to that on the intact side was, for example, 0.6 in a case with a hematoma 1 cm thick i. e. less thicker, and never wider than in Cases 1 and 2. Thus reduction in EEG amplitude over the hematoma stands little proportional to its dimensions.

Fig. 3 shows corticograms recorded immediately after removal of a hematoma in a case in which typical focal reduction in EEG amplitude had been defined formerly. It can be said in general that the electrogram of the cortical area previously underlying hematoma is not flat as compared with that of the normal cortical areas (as is to be seen in the figure, strip 1-2 is flatter than strip 2-3, but strip 3-6 is flatter than strip 1-4).

Results of Experiments

1. Modifying effects of the skull and the scalp on cortical electrical potentials.

By using electrode placements as shown in Fig. 4 A, spontaneous electrograms on the dura, on the skull (i. e. on the periosteum) and on the scalp were recorded bipolarly as well as monopolarly. An example of records under nitrous oxide anesthesia is shown in Fig. 4 B. In general, the electrogram on the dura was similar in wave form to the corticogram, though amplitude tended to be somewhat lower in the former. On the

K. Suhara and K. S a k a t a :

Fig. 3. Electrocorticogram obtained immediately following removal of il

subdural hematoma with its capsule. T h e area surrounded by a broken line was covered by the hematoma. T h e patient was ucder mixed ether and nitrous oxide anesthesia. Further explanations appea r in the text.

other hand, the electrogram on the skull and that on the scalp resembled each other in their amplitude as well as in wave form. However, striking difference in amplitude as well as wave form was often observed between the electrogram on the dura and that on the skull. In most of the cases examined, amplitude of the electrogram on the skull as well as on the scalp was about 4 to 8 times lower than that of the corticogram in bipolar records and about 4 times lower in monopolar records. This fact must denote the maximal modifying effect of the skull on cortical potentials among other structures.

In Fig. 5 an example is shown of variation in wave form of electrogram under pentothal sodium and nitrous oxide anesthesia, by varying positions of the electrodes from cortical surface to scalp surface. Fast waves are found much exaggerated in the electrograms on the skull and scalp, while slow waves behave just in reverse. The tendency is especially marked in monopolar records. Slow waves seen exclusively in the corticogram monopolarly led from either one of a pair of electrodes, i. e. slow waves with a relatively small distribution, are likely to disappear in the Fcalp electrogram. Such a difference in frequency spectrum between the

Modification of Cortical Potentials by Subdural Hematoma 85

Fig. 4. A. Electrode placements used to obtain the record shown in B. Four layers shown in the left figure are the scalp, the skull, the dura and the brain from u p to down.

B. A record obtained with electrode placements shown in A. G. 2, G. 5, etc. indicate the gain of the amplifier in each channel, and the calibration shown in the right lower corner should be referred to. Lower 7 strips are monopolar records. In this case, the skull was 4 mm thick and the scalp 5 mm thick.

R : a reference needle electrode.

Every 1 / 1 0 second is recorded at the top.

cxtical and the scalp electrogram may pxsibly be due to electrical characte- ristics of the skull and the scalp, though only to be decided by experi- mentation.

2. Modifying effects of the skull and the scalp on extraneous potentials applied to the dural surface.

86 K. Suhara and K. S a k a t a :

Fig. 5. A record obtained with the same electrode placements as in Fig. 4. I n this case the skull was 7 mm thick and the scalp 6 mm thick. For explanations see in the text.

Sine wave p3tentials of various frequencies and insulated from the earth were applied to the dural surface. Records were obtained from various loci as shown in Fig. 6 A, an example being recorded in Fig. 6 B. In this case amplitudes of waves of various frequencies recorded at various loci were measured and compared with the control record led bipolarly from the electrodes 1 and 2, which were separated from the source electrodes only by very thin cotton layers. The result is shown in Fig. 7 A (bipolar records) and B (monopolar records). It can be seen that waves belonging to the fast wave range of EEG are more attenuated by the skull and the scalp than waves belonging to the slow wave range. However, relationship between attenuation and frequency is not linear and maximum attenuation is at 26 cps (or thereabout) in the bipolar scalp record. Tendency of forming a trough becomes more marked when the pxition of leading electrodes deviates laterally from the source. Relative attenuation of fast waves is more pronounced in monopolar records. Absolute values of attenuation in the 1.5 cps wave are shown at the right end of each curve. Similar experiment as above was carried out in a model consisting of cotton layers soaked with physiological saline solution, where similar relative attenuation of fast waves as above was observable, but in this case the attenuation showed relatively linear relation to frequency without

Modifi cation of Cortical Potentials by Subdural Hematoma 87

A

R

B

I I I I I I

I

I.5C.p.S. I UIUI I &ZCFS 1 I Icbs. I 2 6 0 s I 4Ws. 1 66-

Fig. 6. A. Electrode placements used to obtain the record shown in B. Four layers shown in the left figure are the scalp, the skull, the dura and the brain from U P to down. Small layers seen between the skull and the dura are thin cotton layers soaked with normal saline. E: electrodes to which sine wave potentials were added.

B. Record obtained with electrode placements shown in A. In this case the skull was 5 mm thick and the scalp 5 mm thick, too. For explanations see in the text.

R : a reference needle electrode.

forming marked trough. Such a difference between the human head and the cotton layer indicates, of course, the complexity of electrical characteristics of the skull and the scalp. In view of these results, the exaggeration of fast waves in the scalp record shown in Fig. 5 must be

88 K. Suhara and K. S a k a t a :

11-12 1. Zlllff I

8

I10 c

PI 1.5 ’ 1.8 6.2 11 26 h9 64 4’

B Fig. 7. Amplitudes of waves in the record shown in Fig. 6 B were mea- sured, and changes in amplitude according to changes in wave frequency in each bipolar (A) or monopolar (B) record were calculated and compared with the standard record “ 1-2”. Amplitude of 1.5 cps wave in each strip is put to the same value as that of the record “1-2” for the sake of clearness, hut actual values relative to the standard record are shown on the right extreme, below the numbers indicating electrode leads,

ascribed to invasion of potentials originating from surrounding cortical areas.

3. Modifying effects of substances inserted between the cortex and the skull on cortical electrical potentials and on extraneously applied potentials.

A case is shown in Fig. 8, which demonstrates changes in electrograms on the skull and the scalp induced. by insertion of a cotton layer of 5 x 6 x 0.7 cm3 between the dura and the skull. The cotton layer had previously been soaked with normal saline solution. Its electrical resistance was similar to that of hematoma content. Definite attenuation in ampli- tude of bipolar electrograms on the skull and the scalp was observed following insertion of that layer. Monopolar electrograms, however, showed no distinct change in amplitude. When extraneous potentials applied to the cortical surface were recorded on the surfaces of the skull and the scalp, they were remarkably reduced in their amplitude by insertion of the cotton layer. A case in which a thin cotton layer about 0.5 mm thick was inserted showed no distinct attenuation of electrograms on the skull and the scalp.

If the attenuation of electrograms on the skull and the scalp by insertion of a cotton layer is due to its short-circuiting effect on the potentials originating from the cortex underlying the layer alone, electrical insulation of the same cortical area to overlying structures may result in more marked attenuation of the skull and the scalp electrogram. A case is shown in Fig. 9, in which a thin rubber sheet of 7x8cm2 was inserted between the cortex and the dura. Surprising is the fact here that the

Modification of CorticaI Potentials by Subdural Hematoma 89

Fig. 8. Changes in electrograms induced by insertion of a cotton layer be- tween the dura and the skull. The electrode placements are the same as in Fig. 4. Left half: before insertion. Right half: after insertion. This case is the same as in Fig. 5.

scalp and the skull electrograms, either bipolarly or rnonopolarly led, showed no distinct reduction in their amplitude following insulation from such a wide cortical area. The reliability of the insulation is clearly shown by the flat record on the surface of the dura. When extraneous potentials applied to the cortical surface were recorded on the skull and the scalp, pronounced reduction in their amplitude was induced by the above insula- tion. In a case in which a rubber sheet of 9 x 1 1 cmz was inserted between the dura and the skull a little attenuation was seen in the scalp record, but it is not so marked as in the case of insertion of a cotton layer.

From the above results, it is considerable that the short-circuiting effect of the cotton layer acts not only on the potentials originating from the cortex covered by the layer, but also on the potentials originating from surrounding cortical areas and distributing in the structures overlying the layer. Now, correctness of this consideration has been proved by an experiment shown in Fig. 10 A and B. It is to be noted that, in contrast to faster waves which are reduced in their amplitude, the 1.5 cps waves recorded on the scalp surface regain their amplitude when the upper rubber sheet in Fig. 10 A is removed.

K. Suhara and K. Sakata:

Fig. No marked change in amplitude of the scalp electrogram despite insertion of a rubber sheet between the dura and the skull. Left half: before insertion. Right half: after insertion. This case is the same as in Fig. 4.

I)iscussion

1 . Modification of cortical electrical potentials by overlying structures. When cortical electrical potentials are recorded on the scalp surface,

the potentials recorded have been modified by the dura, the skull and the scalp in three ways : spatial diffusion, reduction in amplitude and changes in frequency spectrum. Striking extensiveness of spatial diffusion has well been demonstrated by the case described above in which no distinct change in amplitude of scalp EEG was induced by insulation of considerably wide cortical area from overlying structures. Thus, it seems likely that a certain scalp EEG in some case is mainly composed of potentials originating from cortical areas outside the area underlying the electrodes. Multiplicity and some ambiguity in localization study by EEG may be partly due to such an extensive and complicated diffusion of potentials. Such a diffusion of potentials seems to be mainly produced by the skull.

Attenuation of spontaneous as well as extraneous potentials also seems to be mainly produced by the skull.

As to changes in frequency spectrum relative attenuation of fast waves was found to be produced by the skull and the scalp, but the relationship between the degree of attenuation and frequency is not simple by far. In recording cortical electrical potentials on the scalp surface, an equivalent

Modification of Cortical Potentials by Subdural Hematoma 91

A

B

_. .o 3’ -4’ ,...

...a

Fig. 10. A. In the left figure 7 layers are the scalp, the skull, a n upper rubber sheet, a cotton layer soaked in normal saline, a lower rubber sheet, the dura and the brain from up to down. E : electrodes to which sine wave potentials were added.

B. Difference in wave amplitude according to the presence (continuous lines) or absence (broken lines) of the upper rubber sheet is shown. Chan- ges in amplitude according to changes in wave frequency are expressed by relative values as compared with the standard record “1-2” in Fig. 7 B, since the same case as in Fig. 7 was used in this experiment. The amplitude of 1.5 cps wave in the record “3-4” is taken as 100%. T h e actual relative values of amplitude in the record “3-4” are 2 6 times larger than those indicated here.

Electrode placements used in B.

This case is the same as in Fig. 6.

circuit as shown in Fig. 1 1 A will be considered to exist there. Relative attenuation of fast waves seems to be caused by dominant action of condensers put parallel to lead, and complexity of the relationship between the degree of attenuation and wave frequency seems to denote complicated

92 K. S u h a r a and K. S a k a t a :

A

Bra In

E

Fig. 11. A. A n equivalent circuit postulated to exist in recording scalp EEG.

B. A simplified equivalent circuit postulated to exist in recording scalp EEG.

For explanations see in the text.

For explanations see in the text.

action of all the components of the circuit. A well known fact that sharp cortical spike discharges often change into lesser sharp ones when led from scalp surface icf. Jasper, 1949) may be related to the relative attenuation of fast waves.

2. Focal flattening and normal EEG in case of unilateral subdural hematoma.

As to presence or absence of flattening of the corticogram under hematoma p e r se, we have had no opportunity to compare corticograms of symmetrical areas with each other in case of unilateral hematoma, but the fact that no definite difference in amplitude was observed between corti- cogram under hematoma and that outside hematoma does not lend support to flattening of the corticogram p e r se .

As to short-circuiting effect of hematoma, the results described above must have demonstrated its possible presence. Then, the question to be answered is why EEG can be symmetrical in the presence of a large unilateral hematoma.

When alpha waves are recorded on the scalp surface an equivalent circuit as shown in Fig. 1 1 B is supposed to be acting (condensers are omitted here). Each of the potentials A, B and C is divided by respective series of resistance and the voltage between two ends of R is picked up. Thus this voltage may mainly consist of potentials due to C, if the voltage of C is high enough. If, in such an individual, a very chronically developing hematoma, provided with a firmly developed or even calcified capsule having a relatively high electrical resistance, does lie there in a

We may infer as follows :

Morlifi2a:ion of Cortical Potentials by Subdural Hematoma 93

mass as indicated by H, the scalp alpha waves may not be attenuated, just as seen in the case of rubber sheet insertion. But if the voltage of A is high enough, hematoma H may cause reduction in amplitude of scalp alpha waves just as indicated by attenuation of the scalp record of poten- tials applied to dural surface by insertion of a rubber sheet.

On the other hand, when the hematoma is relatively fresh and its capsule is almost absent or very thin, and when it is not so small nor s3 thin the scalp alpha waves over the hematoma may be decreased in its amplitude, whether the highest potential is in A or C, just as seen in the case of cotton layer insertion. But slow waves may behave otherwise and also monopolar records may remain unchanged. Our experiences up to date with cases of subdural hematoma seem to lend support to this inference.

Summary

Two cases have been reported in which normal symmetrical alpha waves were observed in the presence of a large and thick unilateral subdural hematoma.

2. These cases necessitated experimental investigation on short-circuit- ing effect of hematoma on cortical electrical potentials, which had been insisted upon by various authors and could be accepted from the standpoint of common sense. In this connection modifying effects of the structures overlying the brain on cortical potentials were also examined.

3. Modification of cortical electrical potentials by the skull and the scalp consists of spatial diffusion, reduction in amplitude and changes in frequency spectrum. Spatial diffusion was found very extensive and the most responsible structure for causing diffusion and reduction in amplitude was found to be the skull. Relative attenuation of fast waves by those structures was observed, but the relationship between the degree of attenuation and wave frequency was not simple. The cause was discussed.

4. Observation was made on modifying effects of a rubber sheet and a cotton layer soaked in normal saline, each of which was inserted between the cortex and the skull, on cortical potentials as well as on potentials applied to the surface of the cortex or the dura, and following inference has been made. Short-circuiting effect on cortical potentials may be mani- fested when the hematoma is relatively fresh and not so small nor so thin. Normal symmetrical EEG may be observed in the presence of a large unilateral subdural hematoma when it developes very chronically and its capsule much thickly and when main sources of alpha waves participating in the scalp EEG on the hematoma lie outside the cortex covered by the hematoma.

1.

Kef erences

1 ) Jasper, H. H. : Electroencephalography. In W. PenJield and T. C. Erickson : Epilepsy and Cerebral Localization, Springfield, C. C. Thomas, pp. 380-454, 1941.

2) Jasper, H. H. : Electrical signs of epileptic discharge. EEG Clin. Neurophysiol.,

3 ) Jasper, H. H., Kershman, J, acd EZvidge, A. R. : EIectroencephalographic

4)* Matsuzaki , S.: Experimental studies on EEG in case of subdural hematoma.

1: 11-18, 1949.

studies of injury to the head. Arch. Neurol. Psychiat., 44:

Brain and Nerve, 9 : 313-332, 1957.

328-348, 1940.

94 K. Suhara and I<. Sakata:

5>* Motokawa, K. : Electroencephalography. Tokyo, Nanjo Shoten, 1947. 6) Sul l ivan, J. F., Abbott, J. A. and Schwab, R. S. : T h e electroencephalogram in

cases of subdural hematoma and hydroma. EEG Clin. Neurophysiol.. 3: 131- 139, 1951. ULett, G . : EEG of dogs with experimental space occupying intracranial lesions. Arch. Neurol. Psychiat., 54 : 141-149, 1945.

7)

* Written in Japanese.