COMPUTERS
Automatic
AND
BIOMEDICAL
Detection
RESEARCH
8,393-404
(1975)
and Resolution Movements*
of Synchronous
Rapid
Eye
H. EDWARD DEGLER, JR Concept Inc., St. Petersburg, Florida 33732 JACK R. SMITH Department of Electrical Engineering, University of Florida, Gainesville, Florida 32611 AND FRANK 0. BLACK Division of Otolaryngology, School of Medicine, Pittsburgh University, Pittsburgh, Pennsyfoania I52I3 Received July IO,1974 An electronic system is described which is capable of discriminating among horizontal, vertical and oblique synchronous rapid eye movements (REMs). A simplified model expressing the voltages recorded on the electrooculogram as a function movement angle is presented. A computer solution of the equations was used to provide parameter values in the design of a special purpose hybrid hardware system for the detection of eye movement direction. The system analyzes two electrooculogram (EOG) channels to tirst determine if a REM is present, and secondly the eye movement direction is then categorized as being either horizontal, vertical or oblique.
In 1849, duBois-Reymond discovered a potential difference between the cornea and the retina of the human eye (the cornea-retinal potential). The cornea was found to be positively charged with respect to the negatively charged retina, permitting the eye to be electrically characterized as a rotating dipole. This dipole imposes an electric field on the surrounding anatomical structures, and whenever the dipole changes position the surrounding electric field is altered. The cornea-retinal (CR) potential (electrooculogram-EOG) has been used to monitor eye movements (1) and is currently finding extensive clinical application in nystagmography (2) and in the diagnosis of vision abnormalities (3). Also, Aserinsky and Kleitman’s (4) use of electrooculography led to the discovery of rapid eye movements (REMs) during some sleep epochs, and the observation that REMs tended to occur during epochs * This research was supported by Mental Health Grant MH 16960. 393
Copyright 0 1975 by Academic Press, Inc. AU rights of reproduction in any form reserved. Printed in Great Britain
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when dream recall was greatest was a major contribution to sleep research. Electrooculography has been incorporated into most sleep research protocols. Attempts to dimensionally quantitate the electrooculogram have created the need for a method to distinguish the direction of eye movements. The need arises in the quantitative analysis of electronystagmograms where the calculation of the components of eye movement velocity and distance may give inaccurate estimates of the overall velocity and distance if the eye movements are not in or near the electrode plane. There is also interest in observing the patterns of eye movements during sleep (5, 6). These studies have relied on the manual determination of the eye movement direction, a subjective and time-consuming task. What is needed is an automatic system for detecting and determining the direction of eye movements. Several such systems have already been proposed for detecting eye movements. Chouvet et al. (7) applied amplitude plus amplitude of the first time derivative criteria to a filtered, single channel of EOG data to detect rapid eye movements. Minard and Krausman (8) using two data channels, required that the signals be out of phase and the leading slope be above a certain magnitude to be detected as rapid eye movements. McPartland et al. (9) have also reported satisfactory results using similar criteria. Smith et al. (10) used two filtered EOG channels with amplitude criteria to detect REMs and distinguished between in-phase and out-of-phase movements. Padovan and Pansini (II), using three EOG channels. formulated a computer algorithm for determining the eye movement angle. Their work demonstrated that any detector which used two or less derivations for eye movement detection, will miss certain eye movements. This paper utilizes the detection techniques of Smith et al. (f0) and Padovan and Pansini (II) in the development of an eye movement analyzer which detects and categorizes synchronous ocular dipole movements as either horizontal, vertical, or oblique.
METHOD
Data. The electrode montage used to record eye movements is illustrated in Fig. 1. This arrangement has been utilized for several years in the Department OfPsychiatry’s Sleep Research Laboratory at the University of Florida (IZ). Since the long-range plans for the detector include analysis of human sleep data, this study utilized the same montage. The EOG channels, left outer canthus to nasion (L&N) and nasion to right outer canthus (N-RE), are first amplified (the low frequency time constant is .l set) and then recorded on magnetic tape. Horizontal and vertical synchronous movement directions are defined to be within 20 degrees of the horizontal or vertical plane, respectively. Oblique synchronous eye movements are defined as those neither in the horizontal or vertical movement areas.
REM
DETEC-fION
AND
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RESOLUTION
N 8
FIG.
1. Electrode montage for eye movement recording. LE : left eye ; RE : right eye ; N : nasion .
Analysis. In Fig. 2 the electrode planes are shown along with an x-y axis system and three voltage channels. The angle II/ is the angle measured between the nasion and horizontal electrodes. Channels 2 and 3 are the two EOG potential channels which ire amplified and analyzed. It will now be shown that the eye position may be determined from these two voltages assuming that only conjugate synchronous
CARTESIAN COORDINATE SYSlEM
CHANNEL 2
//
/ /-
-\ \
‘\
CHANNEL 3
‘\\
u2 / I’ ,/ -._e__CHANNEL 1
FIG.
‘\
u3
L+E
2. Electrode plane arrangement and vectorial representation of electric potentials.
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eye movements occur, and that both CR potentials are of approximately equal magnitude. The eye position may be represented by the vector U in the following equation : U = u(u, cos (4) + a, sin (4)).
(1)
where a, and a,, are unit vectors in the x and y directions, respectively, u is a scalar and 4 is the eye movement angle. Unit vectors in the directions defined by channels one, two and three are:
a2 = a, cos (I)) + a, sin ($),
(2)
a3 = -a, cos (I)) + a, sin ($). In order to obtain the voltage recorded on channels 2 (N-RE), and 3 (LE-N). the dot product must be taken between the unit vector of the desired channel and U. U2 = -U *a, = -u(cos ($) cos (4) + sin ($) sin (4)),
(3)
U3 = U*u, = u(sin ($> sin (4) - cos ($) cos (fj)),
(4)
where U2 and U3 are the voltages recorded on channels 2 and 3, respectively. Equations (3) and (4) can be simplified to the following : u2 = -u(cos (II/ - 4)). u3 = -u(cos (I) + $)). Each of these equations depends on the deviation of the eye, u, from some starting position. By dividing these two equations, the dependence on the amplitude of movement, u is completely eliminated. The resulting division yields the following ratio : U2jU3 = [cos ($ - 4)]/ [cos (II/ + +)I.
(5)
Once the electrode angle, $, has been established, the ratio U2/U3 is dependent only on the angle 4. Moreover, the eye movement angle can be determined from a knowledge of the ratio of the two channel voltages (U2 and U3). By the use of a computer program, values for the angle 4 were substituted into the above equation (with the electrode angle tj known) yielding the ratio U2/U3. Eye movement can be directly related to the ratio U2/U3. When the ratio U2/U3 is plotted versus the angle 4 (Fig. 3) the horizontal, vertical and oblique eye movement areas correspond to specific range of the ratio U2/U3 as summarized in Table I. Instrumentation. The U2/U3 voltage ranges given in Table 1 are used to establish threshold levels on each of four analysis comparators, where there is a one-to-one
REM
DETECTION
AND
397
RESOLUTION
4
“2/u,
I
5.0 4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0 -0.5 -1.0 -1.5 -2.0 -2.5 -3.0 -3.5 -4.0 -4.5 -5.0
FIG. 3. Angle 4 vs U2/U3, when the electrode angle tp is 35”. TABLE
RANGESOF~AND
1
U2/U3 CORRE~PONDINGTOHORIZONTAL,VERTICALANDOBLIQUEEYEMOVEMENTS
Movement of eye
Eye movement angle, 4
Range of ratio U2/U3 (v = 35”)
-20‘<4<20” 160” < I < 200”
0.64 < U2/U3 < 1.7
Vertical
70” < q5< 110” 250’ < I#Ic. 290”
-3.15 < U2/U3 < -0.34
Oblique
20” 140” 200” 290”
Horizontal
< < < <
q5< 70” q5< 160” 4 -=c250” (b 4 340”
All other ranges not included in vertical or horizontal movements
or
(N-M)
U
u
2
3
,O,OO VOLT COWPARATOR
or
(LE-h)
-
I,
FILTER
FI LTEB
1
TTL IWERTER
I
-
-
’
NEGATIVE ABSOLUTE VALDE
NEGATIVE ABSOLUTE VALUE
-
SUMMER
-
I =
MINIbfUM THRESHOLD DETECTOR
1
REM
DETECTION
AND
RESOLUTION
399
correspondence between the values of U2/U3 and the threshold voltage level. Figure 4 illustrates the block diagram of the system designed to resolve synchronous conjugate rapid eye movements into one of three possible movement directions. The input filters are designed to greatly attenuate signals that are not in the desired frequency range. The two filtered input signals pass into the detection and analysis circuits as illustrated in the block diagram. Equation (5) suggests that the eye position can be continuously monitored. However, because of large dc potential shifts caused by the electrodes, subject movement, or slowly changing position of the eye, subject recording systems usually utilize ac recordings. Thus the dc voltage is not available to continuously monitor the eye angle. However eye movements can be detected with ac recordings if CR dipole movements are rapid enough to create sufficiently large changes in the recorded ac voltages. This system is only concerned with detecting rapid eye movements which are manifested by changes in the recorded EOG ac potentials. The basic function of the absolute value circuits, summer, and minimum threshold detector shown ‘in the Fig. 4 detection circuitry is to determine whether the EOG signal shifts meet a minimum amplitude criterion. At the instant the EOG signals first meet the amplitude criterion, the occurrence of an eye movement is denoted, and it is at this moment that the determination is made on the type of eye movement which has occurred. The amplitude criterion is arbitrary: here it was decided that the sum of the absolute values of both EOG signals excede 80 pV. This criterion resulted in close agreement between the automated detection and the manual detection of rapid eye movements occurring in sleep. Different recording time constants would probably require different amplitude criteria. The strobe pulse can occur at a maximum rate of two times a second. The maximum rate is limited by the inhibit pulser which disables the strobe pulser for 0.5 set after the strobe pulser emits a pulse. This 0.5 set inhibit time was chosen to reduce false alarms since rapid eye movements did not appear to occur within .5 set of each other (10). The second part of the system, the analysis circuitry, establishes the ratio U2/U3 by the use of a four-quadrant analog divider. At the time of this study only twoquadrant dividers were available, and it was necessary to realize a four-quadrant divider utilizing a two-quadrant divider, two dual SPST analog switches, and a positive-negative discriminator (Fig. 5). Once the ratio U2/U3 has been determined by the four-quadrant divider, U2/U3 is then inputed into four analysis comparators through a signal conditioning network which is basically a noninverting buffer. The four amplitude comparators in combination with logic circuitry allow the ratio to be discriminated into three ranges. Each of these three ranges corresponds directly to each of the three possible movement directions. This process is illustrated by the following example. Example. Using the described electrode montage, a horizontal movement to the left will result in an increase in the potential on both EOG channels. The ratio (N-RE)/(LE-N) of thesetwo “in phase” signalswill be approximately + 1. Since the
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DEGLER,
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?”
J
REM quotient is equal to the ratio as the output of the artalog If the input voltage level will change from a high to
DETECTION
AND
401
RESOLUTION
U2/U3, the detection will be on the horizontal channel voltage divider (U2/U3) lies between 0.64 and 1.7 V. of the 0.64 V comparator exceeds 0.64 V, the output a low logic level. This signal is then inputed into an
1 8\ I x 5
i 6
\
4
5 FIG. 6. Eye movement chart used in evaluating the system.
inverter and the output of the inverter is connected to one of the inputs of a dual NAND gate. The other input of this dual NAND gate is connected to the output of the 1.7 V comparator. Since both inputs are high at this time the output of the NAND gate is at a low logic level. Then the output of the NAND gate is inverted, thereby constructing an AND gate.
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The remaining step is to strobe the output of the AND gate with the minimum amplitude criterion. This is accomplishedby the use of another AND gate in which one input is the output of the previous AND gate and the other input is the strobe pulse. When the first input is high, denoting a horizontal eye movement. and when the strobe pulse is high, a horizontal rapid eye movement has occurred. A similar process occurs for a vertical eye movement, except the ratio 113113 is in the range -0.34 to -3.15 V. The negative sign occurs becausethe signals arc out of phasewith each other. The vertical logic is similar to the horizontal movement logic. The only exception is the behavior of the comparators. The comparator5 change from a low logic level to a high logic level when the threshold is exceededin the negative direction. An oblique eye movement occurs when the minimum amplitude requirement is met but the ratio U2/U3 is not in either the horizontal or vertical eye movement categories. Eduation. In order to evaluate the accuracy of the system, it ib necebsary 10 know the input eye movement direction. Figure 6 shows a visual field target chart constructed to guide human subjects during eye tracking from the center to a specified direction and visual field arc and back to center position. Each number corresponds to a specific movement direction; vertical ( I. 5). horizontal (3. 7! and
s”“Li;;;
I
I
I
I
1
I
I
I
FIG. 7. Systemevaluation. Channel 1: N-LE. Channel 2: RE-N. Channel 3: Horizontal detectron. Channel 4: Vertical detection. Channel 5: Oblique detection. Channel 6: Minimum amplitude criterion. Numbers correspond to subject’s eye movements.
REM DETECTIONANDRESOLUTION
403
oblique (2, 4, 6, 8). The two input channels (U2, U3) were simultaneously inputed into both the eye movement detection system and a Grass Model III Multichannel Recorder. The corresponding eye movement detections were displayed simultaneously beneath the two EOG channels. The subject was told to move her eyes in a given direction, and the eye movement detection system response was immediately verified as to being a correct or incorrect detection. Figure 7 gives an example of the system performance. The system was able to determine the direction of the eye movements. DISCUSSION
The system fidelity depends on the accuracy with which it detects eye movements and also the precision with which it resolves the input angles. The detection accuracy has been previously evaluated (10). This accuracy could be improved using a digital discriminator (13). The resolution accuracy is mainly a function of the threshold detectors and the divider. The quality of instrumentation described here will suffice for resolving rapid eye movements in sleeping subjects, but several other problem areas must first be clarified before such a procedure is feasible. A major problem is the detection of nonCR field potentials caused by other facial muscle movements, head movements, and slow wave EEG activity. Furthermore it is not known how the amplitude and direction of the two dipole potentials change during the night. Ocular deviation from the horizontal plane is another problem, although the eyes return to a nearly horizontal position during REM sleep (6). The system described here is suitable for resolving rapid eye movements in an awake subject and has immediate application possibilities for nystagmus analysis. If future research indicates some of the assumptions are not valid for sleeping subjects, the model and detector described here, with appropriate modifications, will still be useful for rapid eye movement resolution. SUMMARY
This article describes an electronic system which is capable of discriminating among horizontal, vertical and oblique synchronous rapid eye movements. A mathematical model is developed which describes the movements of the eyes for various eye movement angles. A computer simulation of the mathematical model provides the parameter values used in the design of an electronic hardware system. The electronic hardware system analyzes two electrooculogram (EOG) channels to first determine if a rapid eye movement (REM) is present, and secondly the direction is then categorized as being either horizontal, vertical or oblique. REFERENCES 1. MOWRER, 0. H., RUCH, T. C., AND MILLER, N. E. The cornea-retinal potential difference as the basis of the Galvano-metric method of recording eye movements. Amer. J. Physiol. 114, 422 (1936).
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2. ASCHAN, G., BERGSTEDT, M., AND STAHLE, J. Nystagmography. Acta Otolaryng. Suppl. I29 (1956). 3. ARDEN, G. B., BARRADA, A., AND KELSEY. J. H. New clinical test of the retinal function based upon the standing potential of the eye. Brit. J. Ophthai. 46,449 (1962). 4. ASERINSKY, E. AND KLEITMAN, N. Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science 118,273 (1973). 5. GABERSEK, V. AND SCHERRER, J. Les mouvements oculaires pendant la phase paradoxale du sommeil. Acta Neural. Latin0 Amer. 14, 40 (1970). 6. JACOBS, L., FELDMAN, M., AND BENDER, M. Eye movements during sleep. I. The pattern in the normal human. Arch. Neural. 25, 151 (1971). 7. CHOUVET, G., VERCHERE, G., MOURET, J., JEANNEROD, M.. AND JOUVET. M. Analyse sequentielle des mouvements des yeux au tours du sommeil paradoxal chez I’Homme. Comptes rendus des seances de la Societe de Biologic. 165, 1654. (1971) 8. MINARD, J. G. AND KRAUSMAN, D. Rapid eye movement definition and count: an on-line detector. Electroenceph. clin. Neurophysiol. 31, 99 (1971). 9. MCPARTLAND, R. J., KUPFER, D. J., AND FOSTER, F. G. Rapid eye movement analyzer. L&cf,w-
enceph. clin. NeurophysioI. 34, 3 I7 (1973). IO. SMITH, J. R., CRONIN, M. J., AND KARACAN, I. A multichannel hybrid system for rapid eye movement detection. Comput. Biomed. Res. 4,275 (1971). II. PADOVAN, 1. AND PANSINI, M. New possibilities of analysis of electronystagmography. Acfa Otolaryng. 73, 121 (1972). 12. WILLIAMS, R. L., AGNEW, H. W., JR., AND WEBB, W. B. Sleep patterns in young adults: An EEG study. Electroenceph. clin. Neurophysiol. 17, 376 (1964). 13. SMITH, J. R., AMBUEHL, R. A., AND FLJNKE, W. F. Recognition of phasic events in sleep EEC’s. Proceedings of 25th ACEM3, p. 237 (I 972).