Automated morphological analysis of spikes and sharp waves in human

Electroencephalography and clinical Neurophysiology , 1983, 55:45-50 Elsevier Scientific Publishers Ireland, Ltd.

45

A U T O M A T E D M O R P H O L O G I C A L ANALYSIS OF SPIKES AND S H A R P WAVES IN H U M A N ELECTROCORTICOGRAMS JOHN F. LEMIEUX and WARREN T. BLUME

Epilepsy Unit, Department of Clinical Neurological Sciences, University Hospital, London, Ont. N6A 5A5 (Canada) (Accepted for publication: August 23, 1982)

Kooi (1966) considered the 'segmental velocity' or slope to be the aspect which best distinguished spikes and sharp waves (SSWs) from background activity. Gloor (1977) listed several criteria by which the electroencephalographer may separate true SSWs from other potentials which also have a sharp apex and a 'paroxysmal amplitude increase.' He considered asymmetry of wave form to be the most characteristic feature with the slope of the first half-wave exceeding that of the second halfwave. Gotman (1980) measured slope near the apex, amplitude and duration of first and second halfwaves of SSWs in 317 EEG channels from 49 patients. In contradistinction to Gloor's criteria, Gotman found that the SSWs of the majority of EEG channels failed to show a slope asymmetry. Moreover, among the 30% of channels with a slope asymmetry, the second slope was more frequently the steeper. Gotman also found that the amplitude and duration of the second half-wave usually exceeded that of the first half-wave for the SSWs of most channels. We initiated our studies of SSW morphology by measuring those appearing on electrocorticograms as their form is usually less obscured by background activity and artefact.

Method

Spikes and sharp waves (SSWs) from 20 electrocorticograms (ECoGs) were analysed. These 20 patients, aged 3-49 years (mean 20.5 years) were undergoing cortical resection for uncontrolled partial seizures. ECoGs were recorded from the temporal lobe in 13 patients, the frontal lobe in 6

patients and the occipital lobe in 1 patient. Ten patients had tumours (all gliomas) and ten had gliotic lesions of several types. Recordings were made using silver ball electrodes referred to a collodion-applied reference on the contralateral scalp. The electroencephalograph was set at a high frequency cut-off of 70 with a 60 Hz notch filter; the low frequency cut-off was usually 0.3. Sensitivity ranged from 20 to 50 # V / m m depending on the amplitude of SSWs and background. In addition to paper write-out, the data was fed to a 14-channel tape recorder for off-line analysis. These recordings were subjected to an automated spike recognition program using slope, amplitude and duration (Vera and Blume 1978) only as a way of harvesting the SSWs for later analysis. This program allowed the researcher to dynamically adjust the recognition parameters until they were set low enough to ensure that no possible SSWs were missed. Thus, many false SSWs were purposely recognized. The computer stored 500 msec epochs (digitized at 1 kHz) whenever an SSW was recognized. A marker under each channel to be analysed indicated all 500 msec epochs containing possible SSWs. The ECoG tracings containing the program-generated markings were then presented to two electroencephalographers independently for their visual selection of SSWs. All SSWs marked by both EEGers comprised the data set for further analysis. For this study only the most actively spiking channel (as determined by one electroencephalographer at the time of the electrocorticogram) was used in estimating the SSW morphology of that patient. We then studied the morphological parameters of slope, amplitude and duration for this set of selected SSWs (Fig. 1). Each SSW was first di-

0013-4649/83/0000-0000/$03.00 © 1983 Elsevier Scientific Publishers Ireland, Ltd.

46

J.F. LEMIEUX, W.T. B L U M E

dl d2 B= Midpoint from --£--, D= Midpoint from -E"

SLOPE

DURATION

S L P I = Ol

dl SLP 2 = ° z (do/z)

SLP :5 = F = Max. |=

dn3

=i ~

d2

AMPLITUDE

DUR I = d l

AMP I = o I

DUR 2= do2

A M P 2 = 2(o~, )

DUR 3= dis

=',

i

FIRST HALF WAVE (FHW)

I

SECONDHALF WAVE (SHW)

Fig. 1. Parameters of SSWs.

vided into first and second half-waves. The first half-wave (FHW) is the part of the wave from trough (A) to peak (C) and the second half-wave (SHW) that part from peak (C) to trough (E). The peaks and troughs were determined by the method of segments and sequences of Gotman and Gloor (1976). For each half-wave, slope (#V/msec) was measured by 3 methods. The first measurement (SLP1) was calculated by dividing the amplitude from the trough to the peak (a 1) by the duration from the trough to the peak (dj). SLP2 was calculated by dividing the amplitude (a 2) from the midpoint to the peak by one-half the duration from the trough to the peak (d 1 - 2). The midpoint is that point on the wave form (B, D) at half the duration from trough (A, E) to peak (C). SLP3 was the point of maximum slope (F, G) as determined by a 5-point least-squares method (Vera and Blume 1978). Points F and G on Fig. 1 were located for clarity only. Three measures of duration were performed. The first (DUR1) was the duration (d~) from the trough to the peak. DUR2 was the duration (d~2) from the pseudotrough to the peak. The pseudotrough is the point of intersection of a line extrapolated from the peak through the midpoint

and a line tangent to the trough. DUR3 was the duration ( d l 3 ) from another pseudotrough to the peak. This pseudotrough is calculated by extrapolating from the peak through the point of maximum slope to the point intersecting a line tangent to the trough. 500

375

A 25O > :~ v

SD,

W

Q

e_

125

J ,,~

ME.AN 0

BASELINE

S.D

-125

-2500

50

I00

150

200

250

TIME (msec)

Fig. 2. Mean morphology of SSWs: this SSW most closely approximates the average of the mean values of all patients for slope, amplitude and duration. The shaded area represents I S.D. of this patient's SSWs.

MORPHOLOGY OF CORTICOGRAM SPIKES AND SHARP WAVES We measured amplitude in two ways. The first (AMP1) measured the vertical distance (a]) from the trough to the peak. A M P 2 was twice the vertical distance (2a2) from the peak to the midpoint. These 8 calculations were also applied to the second half-wave. Means and standard deviations of all the above parameters were determined for the SSWs of each channel. Paired t tests of the first half-wave values of all calculations of all parameters at a 95% confidence level determined asymmetries. In addition, the percentage of first half-wave values which exceeded second half-wave values for each parameter gave an additional measure of symmetry. A n o t h e r algorithm displayed each SSW on a C R T scope to assure that the intended aspect of each SSW was being properly analysed. Thus, identification of the peak (C) and trough (A, E) by the algorithm could be visually verified. The display also indicated whether the analysis of an SSW would have been rendered incomplete or false because of situations such as a portion of the spike falling outside the 500 msec epoch and overriding wave forms unrelated to the SSW.

47

~oo

SLOPE

V'~J SLP I

m ,SLP2 L~-~ ,SLP3 0

IO0 I DURATION

[ ] ouR, Iml DL~R2 DUR 3

ii!i!iiii!ii,

0

NSD

I GT 2

[]

AMP I

I~

AMP 2

L

2GT I

Fig. 3. First half-wave-second half-wave comparisons. NSD = no significant difference. 1 GT 2 = first half-wave significantly greater than second half-wave (95% confidence level).

rejected because (1) associated artefact would have distorted parameter measurements or (2) a portion of the wave form resided outside the 500 msec analysis epoch. This left an average of 23 SSWs per channel for analysis. Slope

Results

The mean slope value for all first half-waves ( F H W ) taken together exceeded that for the seco n d half-waves (SHW). This applied to all 3 calculations of slope (SLP1, 2, 3). Using paired t tests, we found that the n u m b e r of patients in w h o m there was no significant difference between the slopes of the first and second half-waves approximately equaled the n u m b e r in w h o m the F H W slope significantly exceeded the

The mean m o r p h o l o g y of the SSWs in the most actively spiking channels of the 20 electrocorticograms is depicted in Fig. 2 and Table I. The program recognised an average of 84 SSWs per channel. Of these an average of 35 SSWs 'per channel were selected as definite by both EEGers for analysis. A n average of 12 SSWs per channel were TABLE I

Slope values in p.V/msec; duration in msec; amplitude in ~V. S.D. equals 1 standard deviation. SLPI

SLP2

SLP3

DURI

DUR2

DUR3

AMP1

AMP2

12.7 5.4

14.0 4.8

25.0 8.0

29.6 9.5

26.9 11.5

27.4 8.9

337.7 92.4

392.1 132.8

12.7 4.1

19.5 5.8

42.4 14.1

33.8 10.5

34.9 11.6

372.7 94.2

483.2 150.3

First half- wave

Mean S.D.

Second half- wave

Mean S.D.

9.9 3.5

48

J.F. LEMIEUX, W.T. BLUME

S H W slope; this held for SLP1 and SLP2 (Fig. 3). A significantly greater F H W m a x i m u m slope occurred more commonly than equal m a x i m u m slopes. A significantly greater SHW slope occurred for only one patient in a single category (SLP3). The SLP1 for the F H W was 50.8% of its SLP3 value (maximum slope). The SLP1 for the SHW was also 50.8% of its SLP3 value. The SLP2 value for the F H W was 56% of its SLP3 value while the SLP2 value for the SHW was 65% of its SLP3 value. We calculated the cross-correlations among the 3 slope calculations for the first and t h e second half-waves taken separately. The mean values for each slope measurement for each patient were correlated giving 3 correlation pairs per half-wave. The lowest of these 6 cross-correlation pairs was 0.93. This means that any of the 3 slope calculations would be equally reliable in comparing slopes of groups of SSWs. For each slope calculation, the correlation coefficient between the first and second half-waves exceeded 0.90, reflecting the expected close relationship between slopes of first and second half-waves. Combining the SLP1 and SLP2 calculations (Table I) gave a range of about 8 - 1 8 / x V / m s e c for the F H W and 7 - 1 5 / t V / m s e c for the SHW with 1 S.D. The ranges for 2 S.D.s were 3-23 /~V/msec for the F H W and 2-21 /~V/msec for the SHW.

Duration For all calculations of duration, the mean of the S H W exceeded that of the F H W by 20-30%. Using paired t tests, Fig. 3 shows that patients had either no asymmetry or that the SHW exceeded the FHW. Asymmetry was slightly more c o m m o n using measurements DUR1 and D U R 3

than using DUR2. Taking all calculations together, the F H W duration within 1 S.D. ranged from 16 to 39 msec while that of the SHW ranged from 23 to 55 msec. Durations within 2 S.D.s were 4 - 4 9 msec for the F H W and 12-71 msec for the SHW. Therefore, an SSW duration would range from 39 to 94 msec with 1 S.D. and from 16 to 120 msec with 2 S.D.s. For each half-wave, the correlation coefficients between calculations DUR1 and D U R 3 exceeded 0.9. Calculation D U R 2 had a correlation coefficient of 0.7 with both DUR1 and DUR3. As with slopes, there was a high inter-half-wave correlation (exceeding 0.75) for each duration calculation.

Amplitude The SHW was 10.3% greater than the F H W using the AMP1 calculation and 23.2% greater using AMP2 calculation. Using paired t tests as for slope and duration we found that about an equal number of patients had larger SHWs as had virtually equal half-waves and that few had larger FHWs. Using both calculations an estimated range of amplitude within 1 S.D. would be 245-525 #V for the F H W and 278-634/~V for the SHW. The ranges within 2 S.D.s would be 127-658/~V for the first half-wave and 183-784 /~V for the second half-wave. The correlation coefficient between AMP1 and AMP2 calculations for each half-wave exceeded 0.93 while inter-half-wave correlations were 0.87 for AMP1 and 0.89 for AMP2.

lnterparameter correlations Taking each half-wave group separately, all slope-amplitude calculation pairs had a correlation coefficient of at least 0.8 for the F H W and at least

TABLE II For each calculation, percent of all SSWs of all patients in which first half-wave(FHW) value was greater than (GT) second half-wave (SHW) value. Percent of FHW GT SHW (all SSWs). SLPI

SLP2

SLP3

DURI

DUR2

DUR3

AMPI

AMP2

72

61

79

23

32

32

35

33

MORPHOLOGY OF CORTICOGRAM SPIKES AND SHARP WAVES 0.72 for the SHW. Similar pairings for slope-duration clustered about - 0 . 4 while duration-amplitude clustered at about -0.08. Another calculation of half-wave symmetry appears in Table II. This gives the percentage of all SSWs of all patients in which the FHW exceeded the SHW for each parameter of measurement. This type of analysis gives results similar to that described above and in Fig. 3 in that FHW slopes were usually greater than SHW slopes while SHW durations and amplitudes were usually greater than F H W values. This type of analysis may be less reliable than those described above as spikes were more abundant in some patients than others. Cfinical correlations No significant difference in any SSW parameter appeared between the discharges of the 10 patients with tumours as opposed to the I0 with nonneoplastic lesions. Similarly, the SSW morphologies of the 8 patients under general anaesthetic did not differ from those of the 12 patients under local anaesthetic in any parameter.

Discussion

Two measurements (SLP1, 2) suggest that about half of our patients have electrocorticogram SSWs with symmetrical slopes. Similarly, Gotman (1980) found no significant SSW slope asymmetry in a majority of scalp recording channels. He and Ktonas et al. (1981) each found that SHW slopes exceeded F H W slopes more often than the converse for scalp-recorded SSWs. In contrast, when our electrocorticogram SSWs were asymmetrical for slope, the F H W was almost always the steeper. In this later aspect our findings support Gloor's (1977) impression that epileptiform potentials are usually asymmetrical, the first slope being the steeper. Our results for amplitude and duration differ little from those of Gotman (1980) and Ktonas et al. (1981) in that those studies found second halfwave values to be more often larger than first half-wave values. However, a higher percentage of our patients had no significant inter-half-wave differences in these respects.

49

Our slope values far exceeded those obtained by Kooi (1966) whose hand measured slopes for scalp SSWs ranged from 0.5 to 3.3 ~V/msec. The higher amplitude of our electrocorticogram SSW first half-waves than his scalp first half-waves (10-90/~V), but almost equal full-wave durations produced this difference in slope. In the absence of any other study of morphological parameters of electrocorticogram epileptiform potentials of which we are aware, we have had to compare our results with the few measurements of scalp recorded potentials. The impression of earlier authors (Gloor 1975; Ajmone Marsan 1976; Celesia and Chen 1976) has been that substantial morphological differences do not exist between scalp and electrocorticogram epileptiform potentials beyond those consequent to amplitude differences. Careful correlative studies are needed.

Summary We studied the morphological parameters of slope, amplitude and duration of visually selected electrocorticogram epileptiform potentials from the most active channels of 20 patients. First half-wave slopes either equaled or exceeded second half-wave slopes. Amplitude and duration of second halfwaves usually exceeded or equaled those of first half-waves.

R6sum6

Analyse automatique de la morphologie des pointes et des ondes pointues de I'ECoG humain On a 6tudi6 les paramrtres morphologiques de pente, d'amplitude et de dur6e de potentiels 6pileptiformes srlectionnrs h vue, h partir des drrivations les plus actives chez 20 patients. Les pentes des premirres demi-ondes 6talent 6gales ou sup6rieures h celles des secondes. L'amplitude et la durre des secondes demi-ondes 6taient en grnrral plus 61evres ou 6gales h celles des premirres demiondes.

50 This research was supported by grants from the Physicians' Services Incorporated Foundation, the Richard and Jean Ivey Fund, and John Labatt Limited. Mr. D. Kent McNeill assisted in spike identification.

References Ajmone Marsan, C. Part C: Electrocorticography. In: A. R6mond (Ed.), Handbook of Electroencephalography and Clinical Neurophysiology, Vol. 10. Elsevier, Amsterdam, 1976: 1-46. Celesia, G. and Chen, R. Parameters of spikes in human epilepsy. Dis. nerv. Syst., 1976, 37: 277-281. Gloor, P. Contributions of electroencephalography and electrocorticography to the neurosurgical treatment of the epilepsies. In: D.P. Purpnra, J.K. Penry and R.D. Walter (Eds.), Neurosurgieal Management of the Epilepsies. Advances in Neurology, Vol. 8. Raven Press, New York, 1975: 59-105.

J.F. LEMIEUX, W.T. BLUME Gloor, P. The EEG and differential diagnosis of epilepsy. In: H. van Duijn, D.N.J. Donker and A.C.V. Huffelein (Eds.), Current Concepts in Clinical Neurophysiology. Drukkerij Trio, The Hague, 1977: 9-21. Gotman, J. Quantitative measurements of epileptic spike morphology in the human EEG. Electroenceph. clin. Neurophysiol., 1980, 48: 551-557. Gotman, J. and Gloor, P. Automfitic recognition and quantification of interictal epileptic activity in the human scalp EEG. Electroenceph. clin. Neurophysiol., 1976, 41 : 513-529. Kooi, K. Voltage-time characteristics of spikes and other rapid eleetroencephalographic transients: semantic and morphological considerations. Neurology (Minneap.), 1966, 16: 59-66. Ktonas, P.Y., Luoh, W.M., Kejariwal, M.L., Reilly, E.L. and Seward, M.A. Computer-aided quantification of EEG spike and sharp wave characteristics. Electroenceph. clin. Neurophysiol., 1981, 51: 237-243. Vera, R.S. and Blume, W.T. A clinically effective spike recognition program: its use at electrocorticography. Electroenceph. clin. Neurophysiol., 1978, 45: 545-548.