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Electroencephalography and Clinical Neurophysiology, 1976, 41 : 513--529 513

© Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands

AUTOMATIC R E C O G N I T I O N AND Q U A N T I F I C A T I O N O F INTERICTAL


EPILEPTIC ACTIVITY IN THE H U M A N SCALP EEG *

J. G O T M A N ** and P. G L O O R
Department of Neurology and Neurosurgery, McGiU University and the Montreal
Neurological Institute, Montreal, Quebec H3A 2B4 (Canada)

(Accepted for publication: March 19, 1976)

The value o f the traditional EEG interpreta- od, we will try to demonstrate that the results
tion in the diagnosis of various types of epi- are reliable and not misleading, when com-
lepsy has been clearly demonstrated. But the pared to the traditional interpretation.
primarily qualitative and impressionistic na- Systems aimed at the recognition of actual
ture of the EEG interpretation has motivated seizures, including 3/sec spike and wave dis-
several workers to a t t e m p t a quantification of charges, will not be reviewed here since these
the EEG manifestations of epilepsy, in order events are, from a signal processing point of
to make more accurate the correlations view, very different from the interictal spikes
between EEG and clinical or pharmacological and sharp waves. Some attempts have been
conditions. The relationship between the made to give quantitative definitions of spikes
number of interictal epileptiform events in and sharp waves, from the paper record.
the EEG and the occurrence of actual seizures, Jasper and Kershman (1949) divided focal
for instance, has n o t been clearly established; epileptiform activity into spikes (10--50 msec
the effect of anti-epileptic medication on duration) and sharp waves (50--500 msec
background and interictal epileptic activity is duration). Chatrian et al. (1974) presented
n o t well documented. slightly different numbers: spikes from 20 to
The morphology of interictal activity in the 70 msec duration and sharp waves from 70 to
EEG is used as a diagnostic tool b u t its rela- 200 msec duration. The remaining parts o f
tionship to the possible focus of seizure ac- the definitions are purely qualitative, and the
tivity is still n o t completely known. These m e t h o d of measurement of the duration was
problems can be better approached if a quan- never stated. But the definitions remind us
tification m e t h o d is available. It is our pur- that interictal epileptiform activity does n o t
pose to present here a m e t h o d for the auto- only include sharp transients of short dura-
matic recognition and quantification of inter- tion, since sharp waves m a y last up to several
ictal epileptiform activity in the scalp EEG of hundred milliseconds. Kooi (1966) has con-
epileptic patients. After describing the meth- cluded, from a study of paper records, that
*This work was supported in part by Research epileptic activity was characterized b y seg-
Grants MT-3140 and MA-3821 of the Medical Re- mental velocities of more than 2 pV/msec.
search Council of Canada. The compute r system This is an interesting finding, b u t it clearly is
was purchased through Major Equipment Grant n o t a sufficient one.
ME-3822 of the Medical Research Council of Cana-
Automatic methods, analog or digital, are
da.
** Supported by a Scholarship from the I.W. Killam usually based on the "sharpness" feature of
Memorial Fund of the Montreal Neurological In- the epileptic activity. The most obvious
stitute. correlate of sharpness is the second derivative
514 J. GOTMAN, P. GLOOR

of the signal. It was first used in EEG analysis non-stationarities in the signal. When EEGs
by Saltzberg et al. (1967). Walter et al. (1973) were recorded from the scalp and from under-
describe an analog implementation of this lying subdural electrodes, this m e t h o d ap-
idea, Variations o f this m e t h o d are given by peared to detect m a n y events on the scalp not
Hill and Townsend (1973) and Smith {1974). looking like traditional spikes, but occurring
Carrie (1972) presents a m e t h o d where a at the same time as spikes in the subdural
measure of amplitude complements the sec- electrodes. This is a potentially very powerful
ond derivative; both measures are taken m e t h o d since it might reveal epileptic activity
relative to a running average of the back- n o t seen by the human observer. But much
ground activity, removing the necessity to more work needs to be done using the EEGs
adjust thresholds for each subject. Gevins et of epileptic and non-epileptic subjects in
al. (1975) also use a measure of curvature at order to distinguish the non-stationarities
the peak of a wave, relative to a fixed 4 sec which are definitely of epileptic origin, from a
calibration period; the drawback is to make variety of other non-stationarities which ap-
the results of the analysis dependent on the pear in scalp EEGs. If such a distinction can
choice of t h a t section, but the combination of be made reliable, this method will be very
curvature with other features (duration o f useful. At present the autoregressive model
following wave, presence of spikes in other has the disadvantage of requiring a relatively
channels, artifact rejections) makes this large a m o u n t of computation.
system quite complete. Goldberg et al. (1973) The m e t h o d to be described is an a t t e m p t
present a m e t h o d based only on the amplitude at incorporating several of the ideas mentioned
and duration of individual waves and their above and some original ideas into a system
relationship to background activity, after capable o f reliably giving quantitative informa-
high-pass filtering of the data. The authors tion about the interictal activity of a subject.
conclude that the system is efficient for spike The design criteria are the following: (1) the
detection, but t h a t sharp waves are not de- system, to be implemented on a small com-
tected a n d t h a t muscle artifacts greatly de- puter, should be able to process 16 channels
crease the performance. This is true of most in real time in order to allow the analysis of
of t h e above methods. From these various prolonged recordings (up to several hours);
examples, it may be concluded t h a t the sec- (2) the system should not be disturbed by the
ond derivative is n o t a sufficient measure to most c o m m o n artifacts (EMG and eye move-
detect epileptiform activity, but that it ments) as they usually appear in clinical
characterizes one of its most important as- recordings; (3) the system should give, as its
pects. final result, a relatively simple picture, with
Saltzberg et al. (1971) used a matched quantitative information, regarding the spatial
filtering technique to detect, in the scalp of distribution and the type of epileptiform ac-
monkeys, particular wave shapes which tivity which occurred during the period of
appeared within the cortex. This is a very analysis; (4) a classification of events detected
powerful m e t h o d when a wave shape is according t-'o" clinical significance should be
known in advance and only this wave shape is included if possible. These criteria follow the
to be detected, However, such is obviously basic ideas described in a previous work on
n o t the case in clinical electroencephalog- slow wave abnormalities (Gotman et al. 1973).
raphy, where the same subject may present a The approach is a heuristic one, whereby
variety of interictal wave shapes, and none empirically derived features are incorporated
are clearly known in advance. More recently into as efficient a computer program as possi-
Lopes da Silva e t a l . (1975) have used an auto- ble. In the following text, spikes and sharp
regressive model to represent a section of waves will be referred to jointly as SSW.
EEG; by reverse filtering, it is possible to find
RECOGNITION OF INTERICTAL EPILEPTIC EEG ACTIVITY 515

Method A Original EEG

1. Data acquisition and c o m p u t e r system

Sixteen channels of EEG are recorded,


after being filtered at 70 c/sec with a 4-pole
analog filter, on a 7-track analog tape recorder
b y 4 : 1 time-division multiplexing. The signal
is sampled at 200 samples/sec/channel and
B - Representation
either analyzed on-line or written on digital by segments F
magnetic tape for later use. The c o m p u t e r
system consists of a PDP-12 with 28K of
m e m o r y , disk, magnetic tape, and Tektronix B H
4002 storage terminal with hard copy unit.

2. The basic features

SSWs are detected through a sequential I


pattern recognition technique. The signal is C - Representation
first broken d o w n into simple features. A
simple test on these features allows for the
k
rejection of a large proportion o f the data
(the rejected sections have a high probability
of n o t containing any epileptic activity). The
sections which are kept are tested with more
refined features and possibly rejected. The
analysis proceeds in this fashion, making more A
1
and more refined measurements on less and
Fig. 1. A, B, C: Segments, sequences, waves: upgoing
less data. This allows for both a fast processing sequence A F terminates at F because downgoing seg-
and a detailed analysis of meaningful sections. m e n t FG cannot be included, being larger than prece-
ding segment EF. Downgoing sequence FI terminates
a. Segments and sequences at I because upgoing segment IJ cannot be included,
According to the classical m e t h o d of wave being followed by downgoing segment JK of smaller
amplitude. Upgoing sequence IL terminates at L be-
analysis, the EEG signal is broken d o w n into cause it cannot include a downgoing segment of very
segments: a segment is the section between large amplitude, LM. Waves: ABC, BCD, EFG, GHI,
t w o consecutive extrema of amplitude. It is HIJ are examples of waves composed of 2 segments;
characterized by its duration, amplitude and AFI, FIL are waves composed of 2 sequences; A F G ,
EFI, FIJ are waves composed of a segment and a
direction. Hence segments alternate in direc-
sequence.
tion. An example is given in Fig. 1, B. This
m e t h o d causes difficulties when small ampli-
tude " n o i s e " (beta, muscle) is superimposed
on waves o f longer duration, as the latter do have designed a w a y of regrouping segments
n o t appear as a single segment in the decom- into sequences of segments, recreating the
position. Leader et al. (1967) eliminated over- slow frequency wave in the presence of low
riding waves b y imposing a minimum differ- amplitude fast activity. A sequence ends when
ence between consecutive maxima and minima. a segment which may n o t belong to that
Gevins et al. (1975) used a digital filter at sequence is found. A sequence of direction X
20 c/sec to eliminate the fast activity. We (up or down) may n o t include a segment S of
516 J. GOTMAN, P. GLOOR

direction --X larger than either of the two seg- background amplitude at every instant as the
ments immediately adjacent to S. Further- average amplitude of the sequences from the
more, a sequence of direction X may not in- 5 sec directly preceding that instant. (A sec-
clude a segment of direction --X of duration tion comprising activity before and after that
equal to or larger than 30 msec or of relative instant might be preferred, but this presents
amplitude equal to or larger than 2 (see below technical difficulties of implementation.}
for relative amplitude). This is to ensure t h a t The need for a constantly updated back-
a sequence of direction X only includes small ground, as opposed to a fixed calibration
segments of d i r e c t i o n - - X (superimposed fast period, is demonstrated by the fact that the
activity). Fig. 1 gives examples of the re- value of the background activity of one sub-
grouping of segments into sequences. ject, c o m p u t e d over 5 sec, was found to vary
frequently by 100% and occasionally by
b. A wave 400% over a 2 min period. Such variations are
A wave is defined here as a set of two seg- present in normal subjects and in patients. A
ments, two sequences or a segment and a se- duration of 5 sec is a compromise: a stable
quence; both elements must be adjacent and background is required but it is also necessary
of opposite direction. As it becomes part of a to adapt rapidly to a slowly changing back-
wave, a segment or sequence is called a half- ground {onset of alpha activity or of drowsi-
wave. Fig. 1 gives examples of different types ness, for instance}.
of waves. By allowing waves to be composed In practice the background amplitude is
of segments or sequences, both the underlying not updated at every sample point, as this
slow wave and the fast activity may be ex- would require important amounts of m e m o r y
amined, It should be noticed that in the case and computation, but every 1/3 sec. Further-
of a simple rhythmic activity, delta or alpha more, the amplitude of the background ac-
for instance, sequences and segments will be tivity is not a true average of the amplitudes
identical (every sequence having one segment), of sequences over a 5 sec interval. It is biased
and the waves as defined here coincide with towards a smaller value in the presence o f
the traditional waves. R~mond and Renault slow wave activity, because SSWs of similar
(1972) and Schenk (1973) have proposed amplitude can more easily be distinguished in
related m e t h o d s for the decomposition of a predominantly delta background than in a
EEG into waves. faster one. If N is the number of sequences in
an interval of 320 msec and A is the sum of
c. A m p l i t u d e o f background activity the amplitudes of these sequences, A/{N + 6)
One EEG channel is a voltage v ~ i n g with is computed; the constant 6 achieves the
time. Some time characteristics have b e e n desired bias (N is usually between 1 and 15).
defined and are ~ e e d upon, such as the fre- The 16 numbers from 16 consecutive 320
quency o f the alpha activity. But the ampli- msec sections are truly averaged to constitute
tude characteristics are n o t defined in absolute the background amplitude (16 × 0.320 =
terms (in pV) but only relative to a back- 5.12 sec}. Because of the addition of the con-
ground. Chatrian et al. (1974) define back- stant 6, the background amplitude is smaller
ground activity as " a n y EEG activity re- than the true average: about 25% if the ac-
presenting the setting in which a given normal tivity is mostly fast, 2 or 3 times if it is
or abnormal p a t t e r n appears and from which mostly delta and theta activity.
such pattern is distinguished". Since a spike The amplitude of a half-wave (segment or
or a sharp wave is "clearly distinguished from sequence) m a y now be defined in relative
background activity" (Chatrian et al. 1974), terms, as the ratio of its absolute amplitude to
a precise definition of the background ampli- the background amplitude. It is an integer
tude is required. We therefore define the number ranging from 0 to a rare maximum of
RECOGNITION O F I N T E R I C T A L EPILEPTIC E E G A C T I V I T Y 517

20. The m e t h o d of detection of a SSW will Pseudo-Duration


be given below, but it is important to notice Y2 duration duration
t h a t a SSW is n o t included in the c o m p u t a t i o n i
I
of the background activity. This makes it
possible to detect SSWs even when t h e y are
frequent. 1
Ic
d. The sharpness
The second derivative of the signal is the I
I I
simplest measure o f the sharpness of a wave.
E B e~
Since the second derivative is measured in p V / T Pseudo- D- ~r T dTT
sec/sec it is necessary to normalize it in order I duration i I Pseudo.duration i~I
I-
to have a measure independent of the subject. I I
I
I
!~ Duration I!, Duration 1,~
The background amplitude, derived from the
past 5 sec of signal, is used for the normaliza- Fig. 2. Computation of the pseudo-duration of seg-
tion of the second derivative as it was used for ment AB with respect to A: the line joining A to the
that o f the amplitude. To reduce the computa- point at middle duration (C) intersect the horizontal
tion, the second derivative is c o m p u t e d only line passing through B in D. The pseudo-duration of
for the apex of a wave (using 15 msec before segment AB is ED, and similarly that of segment ab is
ed.
and after the apex), and n o t for every sample
point. The relative second derivative is called
the relative sharpness. It is scaled (in arbitrary
units) and ranges from 0 to a rare m a x i m u m than the duration, while remaining easy to
of 5. compute.

e. Pseudo-duration f. The basic attributes o f wave


It is now necessary to define the duration We have seen t h a t a wave is a set of two
o f a half-wave (made of a segment or a se- half-waves (segments or sequences). The attri-
quence). The simplest choice is of course to butes o f a wave are the relative amplitude and
use the actual duration of the half-wave. But the pseudo-duration of its two half-waves, the
for the purpose of spike recognition, it is easy relative sharpness at its apex, and its total
to define a simple measure which will be more duration (the sum of the durations of the
efficient than the duration in distinguishing half-waves). To these features are added the
between spike or sharp waves and other waves. relative amplitude and the duration of the
The definition of the pseudo-duration of a third half-wave; the latter is defined as the se-
half-wave relative to its beginning point is quence directly following a wave. Its use
given in Fig. 2. The amplitude of the point at originates in the importance given, for the
middle duration is used in order to incorporate visual interpretation, to the presence of a
information a b o u t the convexity of the half- slow potential following a SSW. Having defined
wave. Fig. 2 illustrates t h a t two half-waves of the attributes of a wave, it is necessary to
same duration and amplitude can be differen- explain their use in the detection of SSW.
tiated: ab has a larger pseudo-duration and is
less likely than AB to be part of a spike or a 3. Detection algorithm
sharp wave (notice t h a t the curvatures at A
and a on one hand, B and b on the other hand The channels are first processed inde-
are similar). By incorporating some informa- pendently o f each other. The signal is decom-
tion about the shape o f the half-wave, the posed into segments and sequences. When a
pseudo-duration appears more appropriate segment or sequence is complete, the following
518 J. GOTMAN, P. GLOOR

operations take place sequentially (if the TABLE I


answer to any question is no, analysis pro- Relative sharpness and relative amplitude thresholds
ceeds to the next half-wave): for SSW detection. The absolute threshold 4 was sub-
i. Is the relative amplitude of the current tracted from the relative amplitudes.
half-wave and of the preceding one above
Sharpness Amplitude Amplitude Amplitude
preset thresholds? A relative amplitude of 4 is of 1st of 2nd of 3rd
necessary for a half-wave to be considered as a half-wave half-wave half-wave
possible part o f a SSW; this may appear high
but it must be remembered that the back- 0 ~3 >4 --
1 1 ~>4
ground amplitude is smaller than the true
~2 >3
average of sequence amplitudes, giving higher 2 0 l I>4
relative amplitude than otherwise expected. 1 1 i>2
ii. Are the pseudo-durations of both half- 0 2 I>2
waves under t h e appropriate limit? In order to 0 ~-3 --
i>1 I>2 --
belong to a SSW, a half-wave must have its
i>3 0 0 >14
pseudo-duration and relative amplitude satis- 0 I ~2
fying the requirements plotted in Fig. 3. Re- 0 2 --
gion ABCD is the region of validity for a first 1 1
half'wave and region A E F G H is for a second sum/> 3
half-wave. For short pseudo-durations the
amplitude limit is constant b u t it increases
linearly with longer durations. Note that for a
given pseudo.duration, a slightly smaller
amplitude is required for a second half.wave
than for a first one. Note also that longer if its relative amplitude is large enough; a
durations are acceptable for the second half- wave of larger relative sharpness requires a
wave. smaller relative amplitude to be declared a
iii. Given the relative sharpness of the wave, SSW. Table I indicates the thresholds of re-
are the relative amplitudes large enough? A lative amplitude of the first, second and third
wave of small relative sharpness is a SSW only half-waves for a given relative sharpness. The
table is interpreted as follows: to be a S S W , a
wave must h a v e a combination of its 3 relative
amplitudes in agreement with at least one
Relative horizontal line in the section of its relative
amplitude
sharpness. In the table the threshold value 4
ol N has been subtracted from the relative ampli-
2C tudes, leaving values in excess of the threshold.
It may be noticed that: (1) waves of high
s ~ G i sharpness (~>2) with first and second half-
10
waves of small amplitude require a third half-
5 ~ pseudo- wave of large enough amplitude; (2) thresh-
A E duration olds for the second half-wave are often larger
° 0 ;5 '
}00 200 msec than those for the first, reflecting the frequent
Fig. 3. Diagram of the limits of the relative amplitude asymmetry seen in SSWs.
as a function of the pseudo-duration. Region ABCD iv. Is the total duration of the wave larger
is for a first half-wave, and region A E F G H is for a or equal to a minimum value (35 msec.)?
second half, wave. The coordinates are: A(0,4),
B(50,4), C(150,I2), D(150,-), E(60,4), F(150,11), If yes is answered to all the above ques-
G(240,14), H(240,-). tions, the wave is declared a possible SSW. It
RECOGNITION OF INTERICTAL EPILEPTIC EEG ACTIVITY 519

is important to notice that the above features lasts less than 1/3 sec. The autocorrelation
(relative amplitude and sharpness, pseudo- function is then c o m p u t e d , using 1/3 sec
duration) are used in the detection algorithm centered at the apex of the detected wave. It
b u t are also useful after a wave has been de- is possible to define a threshold for the rapidity
clared a SSW: they provide quantification of of decrease of the autocorrelation function
the amplitude, sharpness and duration o f a which differentiates b e t w e e n short muscle
SSW. bursts and genuine spikes (the decrease is
faster for muscle activity). These t w o modes
4. Artifacts of rejection take care of practically all false
detection related to this artifact.
Although n o t frequently, it happens that
a wave being detected following the above b. Eye blinks
m e t h o d is n o t a SSW. It is necessary to do Eye blinks are often of t o o long duration
further processing in order to reject this wave. to be considered as SSWs, but many present
By far the three largest categories of such the characteristics of sharp waves, i.e., very
cases are muscle activity, rapid eye blinks and steep rising phase, slower descending phase,
onset o f sharp alpha activity. For the pur- and a sharp apex. A detected SSW is rejected
pose of this study, alpha activity is treated as as an eye blink if all of the following are true:
an artifact. it occurs in a frontal channel; it is of positive
polarity; it has a duration larger than 150
a. Muscle msec; a wave o f similar amplitude occurs
When muscle activity is on-going, both the simultaneously on the homologous contra-
relative amplitude and the relative sharpness lateral channel. These criteria allow for the re-
of most waves are small. But with a sudden jection of most eye blinks; some are kept,
onset, both sharpness and amplitude become largely because of asymmetry between right
very high relative to the background activity. and left side. It has also occurred that a sharp
Most of these waves have a very short dura- wave was erroneously declared an eye blink.
tion (30 msec or less) and are not detected as
SSW. Occasionally a wave (usually made of c. Onset of alpha activity
several segments) has a longer duration and is During recordings with eyes open or closed,
detected. It is rejected if its immediate sur- it is frequent that alpha activity comes and
rounding (1/3 sec) has a large number of high goes. Since 5 sec of EEG are used to deter-
amplitude segments, indicating onset of mine the background amplitude, a suddenly
muscle activity. This may n o t be sufficient as appearing alpha burst may contain waves
shown in Fig. 4, A, when the muscle burst having the characteristics of SSW, particularly
when the alpha is sharp. An example is given
in Fig. 4, B. Such waves detected as SSW can
A be rejected by determining that they are part
of a section with a dominant frequency of
B 8--12 c/sec. This is done by computing the
correlation functions of 1/3 sec centered at
J;O0 pv the apex of the detected wave, and 1/3 sec
I see centered 100 msec before and after the a p e x
Fig. 4. A : E x a m p l e s o f short lasting bursts of muscle over a lag of 60 msec; a high correlation
activity. Their relat've a m p l i t u d e and sharpness are (above 60%) indicates the presence of alpha
large. S o m e waves m a y last 35 msec o r more. B:
E x a m p l e o f onset o f sharp alpha activity f r o m a low
activity. This m e t h o d allows for an almost
a m p l i t u d e background. Normal subject, e y e s closed, perfect solution of the problem.
channel P4--O2. It should be emphasized that muscle ac-
520 J. GOTMAN, P. GLOOR

tivity, e y e blinks and o n s e t o f a l p h a activity Fp2"F8% ~ ~ 1 ~


are difficulties w h i c h are n o t i n h e r e n t t o this
m e t h o d o f SSW r e c o g n i t i o n . B e c a u s e t h e i r
morphology and mode of appearance have
T4-T6 ':c g
m u c h in c o m m o n w i t h real SSWs, t h e y are
12oo~v
likely t o p r e s e n t difficulties t o a n y time- 1 sec

domain or frequency-domain detection meth- Fig. 6. The letters a to h mark the SSWs detected by
od. the system. Phase reversals at electrode F8 are de-
tected by coincidence in time for a--b and e--f, by
computation of the cross-correlation for d and h
5. In ter-channet relations. (since no SSW was found in channel F8--T4 at the
time of d orh).
A s s u m i n g t h a t t h e d e t e c t e d w a v e is a SSW,
its relationships w i t h o t h e r c h a n n e l s are im-
p o r t a n t f o r t h e l o c a l i z a t i o n o f an epileptic
focus. O n l y b i p o l a r m o n t a g e s h a v e b e e n (channels having an e l e c t r o d e in c o m m o n ) or
s t u d i e d here, a n d a l t h o u g h t h e m e t h o d was an e q u i p o t e n t i a l z o n e with p h a s e reversal f o r
also i m p l e m e n t e d f o r o t h e r s , t h e p r e s e n t a t i o n b i p o l a r c h a n n e l s o f t h e s a m e chain n o t
will use t h e m o n t a g e s h o w n in Fig. 5. A m a j o r i m m e d i a t e l y c o n t i g u o u s . E x a m p l e s are given
s o u r c e o f i n f o r m a t i o n lies in t h e relative in Fig. 6 a n d 7.
p o l a r i t y o f SSWs in n e i g h b o r i n g channels. I t m a y also o c c u r t h a t the m a x i m u m o f the
T w o SSWs o c c u r r i n g s i m u l t a n e o u s l y in t w o p o t e n t i a l field is s i t u a t e d in the area o f t h e
c h a n n e l s o f a b i p o l a r chain, w i t h o p p o s i t e first or o f t h e last e l e c t r o d e o f a chain. If, as is
p o l a r i t y , indicate a m a x i m u m o f t h e p o t e n t i a l a s s u m e d h e r e , this is a u n i q u e m a x i m u m in
field o v e r t h e e l e c t r o d e s s i t u a t e d b e t w e e n t h e t h e chain, a SSW will be p r e s e n t in t h e first or
t w o channels. T h i s is r e f e r r e d t o as a p h a s e last b i p o l a r c h a n n e l o f t h e chain, a n d p o s s i b l y
reversal f o r t w o c o n t i g u o u s b i p o l a r c h a n n e l s in an a d j a c e n t channel, b u t n o SSW o f o p p o s i t e
p o l a r i t y m a y o c c u r in the chain. In o t h e r
words, a m a x i m u m o f t h e electrical field is
d e t e c t e d at t h e e x t r e m i t y o f a b i p o l a r c h a i n if
a SSW is f o u n d in the e x t r e m e c h a n n e l o f t h a t
c h a i n a n d if no p h a s e reversal or e q u i p o t e n t i a l
z o n e exists.
~10Z2"NO ~2

F~2(~ £ \

\ -e5%(
\--76% -- \ s

/ ,,e ~f
) c A2 c

jlO0 pv
1 sec

Fig. 7. The letters a to f mark the SSWs detected by


the system. The equipot~ntial zone over F8--T4 is
found by coincidence in time at a--b and d--e, by
computation of the cross-correlation for c and f
(correlation more negative than--50%). Correlations
between channels T4--T6 and F8--T4 were also com-
Fig. 5. Bipolar montage used in this study. puted at c and f, but found positive.
R E C O G N I T I O N O F I N T E R I C T A L EPILEPTIC E E G A C T I V I T Y 521

Although the above cases do n o t include all classic spikes are found in Fig. 6 and 7. Fig. 8
possible configurations of the electrical field shows sharp waves of long duration (180 and
of an interictal epileptic event, they cover the 200 msec). Sharp waves of up to 400 msec
most frequent ones. The actual existence of can be detected, and have been detected in
the opposition of polarity between two SSWs one subject. Fig. 9 shows a section of EEG
is determined by coincidence in time of the with different shapes of SSWs recognized by
apexes (occurrence within 10 msec of each this system. Fig. 4 and Fig. 8 also indicate
other) or by the computation of the cross- that beginning sharp alpha activity and inter-
correlation function between the t w o chan- mittent EMG bursts are usually not recog-
nels. If only one SSW is detected in a chain, it nized as SSWs. This m a y be shown in quanti-
is cross-correlated with all channels of the tative terms by counting h o w often a clearcut
chain. The cross-correlation is also c o m p u t e d spike is declared an artifact and h o w often a
if the apexes o f two SSWs do n o t occur clearcut artifact is declared a spike. Nearly
within 10 msec of each other. A section of 100 subjects (normal, non-epileptic patients
duration equal to twice the duration of the and epileptic patients) were recorded with
only SSW or of the sharpest of the two SSWs eyes closed for a b o u t 2 min (16 channels,
is used in order to incorporate the immediate montage given in Fig. 5). No recordings were
vicinity o f the event. If the cross-correlation is rejected for excess of artifacts after a subject
more negative than --50%, an opposition of had been selected. Table II shows that the
polarity is said to be present. As shown in number of false positives and false negatives
Fig. 6 and 7, this method allows the detection related to artifacts (muscle, eye blinks, onset
of phase reversals and equipotential zones of alpha activity) is small. More details on
even when only one spike is detected (the these results will be given when a systematic
adjacent channel presenting t o o small a wave global evaluation of the method is available.
to be automatically recognized).
2. Display o f final results
6. Events
The results of an analysis are presented in
The analysis proceeds by discrete time units Fig. 10. The picture is meant to present quan-
of a b o u t 1/3 sec. If several SSWs are found
during this time, only the sharpest is retained.
Therefore only one SSW per 1/3 sec per chan-
nel can appear in the final results. If SSWs are
found in one or more channels within the F3 - C 3 .,.~"'~'~~ ~ ~ ~, ~ -
time unit, an event is said to have occurred.
An event is c o m p o s e d of all SSWs and of all C3 - P3 ~ ~ J ~ - ~ ' ~
phase relations which were detected during a
time unit.
P3 - 0 1

Results

1. Examples F7- T3 ~ ~ - v - ~ ' ~ j ~ . ~ ~ ~'~


100 ~v
It is difficult to present a large number o f 1 sec
examples of SSWs detected by the system, Fig. 8. Waves a and b, recognized by the system, are
because a long enough section of background examples of long duration sharp waves (respectively
activity must also be presented. Examples of 180 and 200 msec).
522 J. G O T M A N , P. G L O O R

F4-C4 ~ ~ d

C4 -P4

P4-02

F8,T4'

T4.T6
__ 1S e c I l O o ~ V , ,
T6-02~ .... -'~-,:.,--~'

Fig. 9. This section o f E E G illustrates s o m e e x a m p l e s o f SSWs d e t e c t e d b y t h e system. On-going or bursts o f


muscle activity d o n o t d i s t u r b t h e r e c o g n i t i o n . SSWs d e t e c t e d are m a r k e d a t o e:

38 VALID [UEHTS
/'I F2

I
n .= m
1 1 3 1 1 1

F~ /-2 FZ F¢ f8
CZ>

I Phase.reversals
2 5 2 3 /:afT4
7"3 C3 Ca* C¢
0

L i
1 1 I ? 7 1 16 4 4 2 ~ \
T5 P3 PZ p.¢
7"6 ~Results of
~ channel
T4,T6

z 1 ~ 1 1 7 1 Zi~ z

A O
RECOGNITION OF I N T E R I C T A L EPILEPTIC EEG ACTIVITY 523

PI /'2

Equipotentials between F4-P4


fZ

.r3 C3 CZ C¢--
!

P3 .. S
Equipotentials between C4-P4
T6

B 0./ 02

? VALID EVENTS
J.2
OR fJ
16
END
f7 F3 fZ F~ f@

T3 ~3 C£ C~ T¢

"r "
2
FJ" P3 PZ ~ T~

2 £,4 £ 2
OJ 02
C ~ ~

Fig. 10. Global results for a section of 3 min (Subject 66-5). A : The names of the electrodes of the 10--20 system
are in their usual location (note that F p l and Fp2 are labelled F1 and F2). The number of SSWs found in a bi-
polar channel is displayed between the corresponding electrodes, in the form of 4 columns. From left to right:
the number of SSWs sharp--large, sharp--small, less sharp---large, less sharp--small. No histogram is displayed if no
SSW is found in a channel. The number of phase reversals at one electrode is indicated just under that electrode,
surrounded by as many lines as phase reversals. This subject shows epileptic activity, predominantly in the right
temporal posterior areas, with some spread to the left hemisphere. B: Connecting lines indicate equipotential dis-
tribution between 2 electrodes, and adjacent numbers indicate the number of times each was found. C: Display
obtained by requesting all events having at least a SSW in left occipital channels (channels P3--O1 or T5--O1 ). It in-
dicates that the left occipital region presents activity often not simultaneous with activity in the right hemisphere
(moreover no event presents simultaneous SSWs in P3--O1 and P4--O2).
524 J. GOTMAN, P. GLOOR

TABLE II
Data base and number of SSWs detected. Sixteen channels. (Note that the results are normalized for a duration
of 30 rain.) The number of "real SSWs" not detected by the system is unknown since there is no unambiguous
definition for a SSW.

No. of Total dura- No. of SSWs Artifacts de- SSWs rejected


subjects tion of detected tected as SSWs as artifact
recording (per 30 rain) (per 30 min) (per 30 rain)

Normal subjects 30 63 min 4 3 0


Non-epileptic 20 43 rain 13 1 0
patients
Epileptic patients 43 107 min 605 1 4

titative information and to attract attention in which one might like to know if activity in
to the most active areas. Fig. 10, A gives the the left occipital region occurs simultaneously
number and locations of SSWs, as well as the with activity in the right hemisphere. A possi-
phase reversals. Note that if a potential maxi- ble answer is to ask for the display of all
m u m is located at the end of an electrode evenus which include a SSW in the left occipi-
chain (e.g., frontal or occipital pole) this ap- tal region (channels P3--O1 or T5--O1). The
pears in the display as if a phase reversal had results are shown in Fig. 10, C; the activity in
been detected there. Fig. 10, B presents the the left occipital region is largely, but not
distribution of equipotential zones. This sub- totally, independent from that in the right
ject presents widespread epileptiform abnor- hemisphere; although both active, homologous
mality, with a clear focal maximum in the channels P3--O1 and P4--O2 are not active
right temporal and occipital areas. Because simultaneously (the two maxima at 0 2
the electrodes of the 10--20 system are in originate from SSWs in channel T6--O2).
their usual location, the spatial aspect of the A special syntax m u s t be used to formulate
results is easy to comprehend. the questions: it includes logical variables
One important drawback to the above dis- (with values true or false) and logical opera-
play is that the time scale is almost lost, only tions, which together make a logical expres-
when channels present phase reversals or equi- sion. This expression is evaluated (found true
potential zones do their time relationships ap- or false) for every event and an event is in-
pear. They do not appear for channels not cluded in the display if its value is true. The
belonging to the same electrode chain. When operations available are OR, AND and
several areas show abnormalities, it is impor- ANDNOT (identical to NAND). The variables
tant to know if they are active simultaneously can be a channel number (its value is true if a
or independently. One possibility is to give SSW is present in that channel at a given
histograms on a compressed time scale {Gevins event) or an electrode name (true if a phase
et al. 1975). But the time relationships are reversal is present at that electrode). The ex-
difficult to see for channels which are n o t pression may have any n u m b e r of variables, tn
adjacent on the display, and cannot be seen the above example, the question is formulated
precisely if the time analyzed is beyond a few a s : " 1 2 OR 16" (channel numbers are found
minutes. Instead, we use a system where the in Fig. 5), meaning "all events having a SSW
user asks interactively specific questions for in channel 12 or in channel 16". Other exam-
resolving the particular ambiguities of an ples are: " P 3 " (events having a phase reversal
EEG. As an example, Fig. 10, A shows a case at P3), "1 AND 2 " (events having a SSW
RECOGNITION OF INTERICTAL EPILEPTIC EEG ACTIVITY 525

simultaneously in channels 1 and 2), "9 OR be answered within seconds. This method ap-
10 OR 13 OR 14 A N D N O T 15 A N D N O T 16" pears to resolve most ambiguities about time
(events having a SSW in the left anterior re- relationships in a flexible manner: if the
gion and no simultaneous activity in the left global results are not ambiguous, no further
posterior temporal area). At the end of the processing is performed, but questions, simple
analysis every SSW is available in the com- or complex, may be formulated in difficult
puter memory in the form of a small number cases.
of parameters, and questions may therefore Another example is shown in Fig. 11. The

39 VALID EUENTS
PJ

m B n ~ .

22 11 I I 1
FP /'3 rz P4 .tO

n
2 4 1 1012 1 1 5 1 S
I3 I'3 CZ C~ F4
CD

L
I010 2 1 2 1 1

l~ P3 PZ Pe

An I~ _.~ L
.2.2 ~'/3.4 I 1.1 .11
A ox 02

F,." /'2

PP PZ re ,'*0--

t C3 C¢ F¢

.3

-r-t
,/"S ,,°3 ,o2" 2"6--

a @2
Fig. 11. A and B (see legend o n next page).
526 J. GOTMAN, P. GLOOR

G3 VALID EVENTS

~'~ 411 I ~ ' 3 $ $ fZ E; 4 I 2 PC $ 4 4 3 f'@


0 c~ C~ CD

.L L ,

o
.2.$" ~ P3 1 2 1 P2' 1 PC 3 4 Z Z IS
C <2> ¢-~
$ VALtD EUENTS
F3
AND
d31)J__ gl
END F'..2 3 2 P~ I /'0

• L L
~1 .T3 2 C3 2 1 1~__~ 2 1 1 C$ 2"4 RZ

D .2.5 ,.~ ~z ~. F~

Fig. 11. Global results for two sections of 2 min (Subject 89-3). A : Antero-posterior montage. The display indicates
a generalized abnormality, more prominent in left fronto-central area. B: Equipotentialzones are more numerous be-
tween F3 and C3. C: Coronal montage (upper chain: F7--F8; middle: A1--A2; lower: TS--T6). Results indicate
most intensive activity around CZ, but also bifrontal. D: Answer to question, in coronal montage, "CZ AND F3"
indicates that most phase reversals occurring at F3 are simultaneous with phase reversals occurring at CZ.

results f r o m the analysis o f t w o d i f f e r e n t a r o u n d F3, seen in b o t h m o n t a g e s , o c c u r r i n g


bipolar m o n t a g e s are shown. In Fig. 11, A t h e at t h e same t i m e as t h a t c e n t e r e d a r o u n d CZ?
a n t e r o - p o s t e r i o r m o n t a g e shows a bilateral This q u e s t i o n m a y b e f o r m u l a t e d as " F 3 AND
a b n o r m a l i t y , m o r e p r o n o u n c e d on t h e left C Z " (all events having a phase reversal simul-
side in t h e F 3 - C 3 - - P 3 region. Fig. 11, B t a n e o u s l y at F3 and CZ). T h e answer is s h o w n
shows t h e e q u i p o t e n t i a l zones ( f r e q u e n t at in Fig. 11, D: m o s t o f t h e phase reversals
F3--C3). Fig. 11, C shows the results o f the o c c u r r i n g at F3 (5 o u t o f 7) are s i m u l t a n e o u s
analysis o f the E E G o f the same subject, b u t with phase reversals a t CZ.
with a c o r o n a l m o n t a g e ( e q u i p o t e n t i a l zones
are o m i t t e d for simplicity). T h e a b n o r m a l i t y 3. Classification of SSW
appears n o w to be m a i n l y a r o u n d e l e c t r o d e
CZ and in b o t h f r o n t a l regions. One m i g h t ask It can b e seen in Fig. 9, A t h a t t h e d e t e c t e d
the following question: is the activity c e n t e r e d SSWs have b e e n clMaified in 4 categories
R E C O G N I T I O N O F I N T E R I C T A L EPILEPTIC E E G A C T I V I T Y 527

according to their relative amplitude and their recordings (often more noisy and presenting
relative sharpness (sharp--large, sharp--small, EKG artifacts), study of the possibility of
less sharp--large, less sharp--small). This is merging the results from different montages.
of course a very simple classification, b u t it is However, the ability of the system to rec-
still useful because it is somewhat similar to a ognize only interictal epileptic abnormalities
classification into large and small spikes and and n o t to miss any such abnormalities has
large and small sharp waves. It is anticipated n o t y e t been demonstrated. Only a relative
that a more refined classification will be de- insensitivity to artifacts was shown. The
veloped, based on the morphology of SSWs, absence of a precise definition for an inter-
their spatial relationships and their m o d e o f ictal epileptic event makes the validation diffi-
occurrence (isolated or in bursts). This will b e cult. We hope to demonstrate the validity o f
possible w i t h o u t changing the detection meth- this m e t h o d in a later study, relying n o w on
od, as all the parameters of every SSW de- our firm impression of its validity.
tected are readily available at the end of the What are the potential uses of such a quan-
analysis; they include the durations, pseudo- tification system? In clinical electroenceph-
durations and relative amplitudes of the first, alography, the results may be used in a way
second and third half-waves, the relative similar to that o f the canonogram for slow
sharpness, the values of cross-correlations wave abnormalities (Gotman et al. 1973,
with related channels, the absolute amplitude 1975): to provide the electroencephalographer
of the background activity and its number of with a simple quantitative picture giving
sequences. All of these parameters can be reliable information regarding the interictal
used for classification. epileptic activity, its intensity and spatial
distribution. The task of the interpreter is
simplified since she/he does not have to ex-
amine the record with great attention to find
Discussion SSWs and their inter-channel relationships. It
was found in a few cases that a situation hard
The results may n o w be reviewed in terms to decipher on the paper record because of
of the design criteria stated in the introduc- complex inter-channel relationships, appeared
tion. (1) The system is able to analyze 16 very clearly in the results of the automatic
channels of EEG in real time using a small analysis. The interpretation o f the clinical
laboratory computer. (2) The system is practi- significance of this activity is, of course, left
cally n o t disturbed by the most c o m m o n to the electroencephalographer and would
artifacts (continuous or intermittent EMG, probably be similar to the traditional one.
eye blinks), nor is it disturbed by onset of The system could also be used, for instance,
sharp alpha activity. (3) Final results are given to establish firmly the relationships between
in a simple picture containing quantitative in- interictal and ictal activity. Recordings of sev-
formation. Information not displayed in this eral hours of EEG, including seizures, could
picture, regarding simultaneity of occurrence be analyzed and could possibly clarify the
in different locations, may be obtained if variations o f interictal activity in relation to
needed b y asking simple specific questions. the occurrence of seizures. Similarly the im-
(4) An elementary classification of SSW is portance of the morphology of SSWs could be
provided. Much remains to be done in this studied in relation to the starting point o f
respect, b u t the system was developed in such focal seizures. The influence of plasma levels
a way as to make several potential parameters o f anti-epileptic drugs on the EEG could also
available for classification. Future develop- be studied in a quantitative fashion. These are
ments will also include: increase in the sensi- just a few examples of the possible applica-
tivity of detection, analysis of monopolar tions o f this method.
528 J. GOTMAN, P. GLOOR

Summary I'EEG de chaque d~rivation est d~compos~ en


demi-ondes. Une demi-onde est carac~ris~e
An a t t e m p t was made at using a small com- par sa dur~e et son amplitude relative au
puter to recognize and quantify interictal rythme de fond. Une onde est caract~ris~e
epileptic activity (spikes and sharp waves) in par les dur6es et les amplitudes de ses deux
the human scalp EEG. demi-ondes, par la d~rivde seconde ~ son
To perform the automatic recognition, the sommet, mesurde relativement au r y t h m e de
EEG of each channel is broken down into fond, et par la dur~e et t'amplitude de la
half-waves. A half-wave is characterized by its demi-onde suivante. On a pu ddterminer des
duration and its amplitude relative to the combinaisons particuli~res de ces param&res
background activity, A wave is characterized pour la reconnaissance et ta quantification des
by the durations and amplitudes of its two pointes. L'~limination d'ondes ressemblant fi
c o m p o n e n t half-waves, by the second deri- des pointes rapides ou lentes, tels que les
vative at its apex measured relative to the clignements d'yeux, les potentiels musculaires
background activity, and by the duration and et l'activit6 alpha pointue, se fait par des
amplitude of the following half-wave. Particu- m6thodes sp~cifiques d o n n a n t des r6sultats
lar combinations of these parameters were tr~s satisfaisants. La d&ermination des r~gions
found to characterize spikes and sharp waves d'~pileptogdnicit~ maximale est possible grfice
and are used for their recognition and quanti- fi l'examen d&aill~ des relations entre d6riva-
fication. Specific methods are used for the tions.
rejection of spike-like or sharp wave-like wave Seize d~rivations peuvent &re analys~es en
forms such as eye blinks, muscle potentials temps rdel. Les rdsu]tats sont pr~sentds sous
and sharp alpha activity and were found to forme d'une image simple, d o n n a n t une in-
perform with a high level of reliability. Inter- formation quantifi6e, particuli~rement utile
channel relationships are thoroughly ex- pour la localisation. Des questions sp~cifiques
amined to determine areas of maximal epilep- sur les relations temporelles entre des pointes
togenicity. situ6es sur des d~rivations diff~rentes peuvent
Sixteen channels can be analyzed in real &re posdes d'une manidre interactive. L'utiti-
time. Results are presented in a simple picture sation du systhme en dlectroenc6phalographie
containing localizing and quantitative informa- clinique est envisag~e.
tion. Specific questions regarding the time
relationships of spikes in different channels References
can be asked interactively by the user. The
system is of potential use in clinical electro- Carrie, J.R.G. A technique for analyzing transient
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Chatrian. G.E., Bergamini, L.. Dondey, M., Klass,
D.W., Lennox-Buchthal, M. and Petersen, I. A
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etectroencephalographers. Electroenceph. ctin.
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approach to an automatic pattern recognition of
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