The relationship between saccadic eye movements and the alpha rhythm in attentionally handicapped patients

Neuropsychologia, 1974, Vol. 12, pp. 209 to 218. Pergamon Press. Printed in England.

THE R E L A T I O N S H I P B E T W E E N S A C C A D I C EYE M O V E M E N T S A N D THE A L P H A R H Y T H M IN A T T E N T I O N A L L Y H A N D I C A P P E D PATIENTS GERALD LEISMAN Department of Neurology, The University of Manchester, England (Received 21 August 1973)

Abstract--The investigation is concerned with the relationship between electro-oculographic potentials (EOG) and the alpha rhythm in hemiplegic attentionally handicapped subjects. It is thought that the alpha rhythm is temporally related to the EOG. Twenty-eightnormal and 36 spastic-hemiplegic subjects with attentional handicaps were studied. Alpha rhythm and the EOG were measured and experimentally varied by changes in illumination and by stabilized retinal image techniques. The results are consistent with the hypotheses and indicated that deviant patterns of scanning and fixation saccadic eye movements may be important components in attentional handicaps. THE CLASSICALtheory of the origin of the alpha rhythm is that during states of restful wakefulness, the occipital cortical neurons beat at an average frequency of 10 Hz in unison. It is in this area that phase reversal points are supposedly found and here that the amplitude is at a maximum [1, 2]. If the alpha rhythm arises from a single source, its amplitude should vary from moment to moment to the same degree wherever it is recorded, which it frequently does not. Alpha activity manifests complex changes with time depending upon the variable rates of frequency change from one cycle to the next. Alpha activity may, therefore, consist of different components [3]. The importance of saccadic eye movements in the manifestation of the alpha rhythm for attention states and for visual perception in general has been well documented [4, 5, 6, 7, 8,9, 101. GR~Y WALTER [3] and CALLAWAYand YAEGER[1 1] thought that the alpha rhythm could reflect, in part, a triggering and pairing of information processing in the brain. GAARDER et al. [9] have shown a relationship between saccadic eye movements and the averaged occipital evoked response. The assumption was that a component of the alpha rhythm was phase-locked with the onset of saccadic eye movements. GAARDERet al. [10] provided further evidence in support of this contention. It is well known that attentional handicaps often accompany conditions of brain damage. It has been demonstrated that attentionally handicapped patients manifest saccades of greater velocity and shorter duration than do normals [12]. It has also been shown that with stabilized retinal image procedures, subjective reports of attention state as well as the ability to condition the alpha blocking response improve in attentionally handicapped subjects [13].

Present address: Diagnostic Center, Board of Education of the City of New York, 218th Street and 67th Avenue, Bayside, New York, 11364, U.S.A. 209

210

GERALD LEISMAN

It is t h o u g h t t h a t a t e m p o r a l r e l a t i o n s h i p exists b e t w e e n t h e a l p h a r h y t h m a n d t h e e l e c t r o - o c u l o g r a m ( E O G ) r e f l e c t i n g s a c c a d i c eye m o v e m e n t s . A c o - v a r i a n t r e l a t i o n s h i p is a l s o e x p e c t e d b e t w e e n t h e E O G a n d t h e a l p h a r h y t h m o n t h e s a m e side o f t h e h e a d o f e a c h s u b j e c t ; b y - p a s s i n g t h e s a c c a d i c eye m o v e m e n t v a r i a b l e (by e l i m i n a t i n g t h e effects of deviant patterns of scanning and fixation) t h r o u g h stabilized image techniques should c a u s e c h a n g e s in b o t h t h e a l p h a r h y t h m a n d in t h e a t t e n t i v e recall o f p e r c e i v e d e v e n t s presented for short durations. METHOD Subjects Twenty-eight normal subjects were studied. The group consisted of final year medical and psychology students as well as hospital secretarial and administrative staff. There were 16 males and 12 females with an age range of 18.9-36.8. The mean age was 22-7 with a S.D. of 8.6. All of the subjects had no evidence of neurological or psychiatric disorder and had no history of such in their families. All of the subjects had a normal attention span as rated by the Continuous Performance Test [14]. Thirty-six congenitally spastic-hemiplegic subjects were investigated. The group consisted of 18 males and 18 females with an age range of 13.8-42.1. The mean age was 18.1 with a S.D. of 6.10. The subjects were patients who had been seen at the out-patient clinic over the course of the past eight years, residents at special training centres for "spastics" and pupils at a council school for children and adolescents with neurological handicaps. Ten of the subjects reportedly had right predominant lesions and 26 had left predominant lesions. The subjects had no history of epilepsy and no epileptic activity was noted on their EEG records. Each of the subjects suffered from some form of attentional handicap as rated by the £'ontinuous Performance Test. Apparatus and procedure The EOG was recorded while the subjects gaze was rapidly switched between two fixation points using the method suggested by ARDEN and KrLSEV [15] and KRIS [16, 17]. Eye potential changes were recorded binocularly and measured by ordinary skin electrodes placed equidistantly from each cornea over the lateral and medial canthi and superior and inferior orbital rims. With d.c. coupling of the vertical and horizontal components, the potential difference between electrodes changed as a result of eye movement. Two llford X-ray viewing screens were separated at a subtense of 30 °. The subjects were required to change fixation rapidly from a mark on one screen to a mark on the other. One eye or the other was occluded with light-tight goggles. Fluid contact from the eyes onto the electrodes was avoided. Although this method leaves a good deal to be desired, it is useful for recording with closed eyes and most of the possible sources of artifact can be obviated by calibration. Also head movements are not much of a problem with this method. Both the EOG and the alpha rhythm were recorded on a Galileo E-10b eight channel electroencephalograph (T.C. = 0.3 sec; Gain -- 50 uV/5 mm; H.F. cut = 25 Hz). Alpha rhythm was measured from each side of the head using scalp pad electrodes placed 10 Cln in either direction from arcs struck from a point 5 cm. above the inion and 5 cm. to both the right and left of that point [18, 19]. When the potentials from both the right and left eyes were recorded, a switching circuit separated movements to the right and to the left for both eyes. After movements to the left for both eyes, the circuit would only be triggered by movements to the right for both eyes and vice versa. A relay also switched the amplified EEG signal from one channel to another so that when the Ampex FR-1900 FM tape recorder received a message from the electroencephalograph, it would alternately store the EEG message on one channel or the other. In other words, the circuit automatically collected samples alternately triggered by movements of both eyes to the left in one channel and movements of both eyes to the right in another channel [9, 13]. The mean alpha and EOG amplitudes of each group of subjects were computed for each minute interval over the course of each run which lasted for two hours. The digital conversion of the analogue data provided a ready means of measuring the amplitude of both EOG and the alpha rhythm. D.c. coupled record of the subjects' saccadic eye movements of the left eyes were obtained on the EEG apparatus. The output of the channels recording eye movements drove a spot on a Telequipment S51E cathode ray oscilloscope at the same amplitude, duration, velocity and direction as the saecadic eye movements of the subjects' left eyes. This achieved a condition of stablized retinal image when the subjects' heads were held immobile in a chin rest [13, 20]. The subjects were tested for the effects of perceptual fragmentation by subjective reports of fading images. The oscilloscope screen was placed 0.25 m from the subject's coronal plane subtending an angle of 28 °. The relationship between the EOG and the alpha rhythm was examined when the subjects of both groups viewed the oscilloscope target under stabilized and nonstabilized retinal inaage conditions.

SACCADIC

EYE

MOVEMENTS

AND

THE

ALPHA

211

RHYTHM

Active vision implies a considerable amount of attention to the visual stimuli. The lack of fixation on a particular stimulus seems to be found amongst many brain damaged subjects with attentional handicaps. This was investigated by examining the differences between perception in normal viewing situations and perception with the eye movement variable manipulated by stabilized image techniques. The normal and hemiplegic subjects were given a chart resembling the oscilloscope screen. The subjects were required to reproduce and recall the last position of the target on the screen under both normal viewing and stabilized image conditions. To prevent a learning set from affecting the results, random positions were assigned to the moving targets and were substituted between trials under normal viewing and stabilized image conditions. The descriptive features of the reproductions were noted. Ten reproductions of the last positions of the oscilloscope targets were made by each subject. The experimenter, at the appropriate time, also noted the final position of the target on the screen. The reproductions were then sorted into three categories: those most accurately reproducing the original stimulus, those reproductions intermediate in position and those which were inaccurate. Three judges independently rated the reproductions and the concurrence of two was necessary for selection for the appropriate category. RESULTS The amplitude of the E O G varies with the level of illumination. For each of the groups, the m e a n amplitude/wave of the alpha r h y t h m a n d E O G was c o m p u t e d a n d a correlation of 0'92 existed for the n o r m a l group (P < 0"0001) and 0"97 for the hemiplegic patients (P < 0-0001), with rapid alternate fixation between the two screens. It is interesting to note that in the hemiplegic group, the amplitude of the alpha r h y t h m is significantly lower (t = 2"12; P < 0"05) t h a n it is for the normal. A co-variant relationship was noted between the E O G a n d the alpha rhythm in both groups of subjects.

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FIG. I. The mean electro-oculographic (EOG) and alpha amplitudes as a function of time during periods with and without illumination amongst (a) normal and (b) hemiplegic subjects. The time intervals indicate random periods during the course of the experiments. The EOG was recorded binocularly and the alpha rhythm bilaterally. The ratio of the alpha amplitude on each side of the head was compared with the ratio of the amplitudes of the E O G in both eyes which was varied by occluding one eye.

212

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indicate the time during which the right eye remained in total darkness and the left in illumination. The non-indicated periods refer to an occluded left eye and an illuminated right. The E O G was measured for each eye separately and illumination was altered independently by using light-tight goggles.

In Figs• 2(a) and 2(b), alpha amplitude is highly correlated with the EOG on the same side of the head (r = 0"91; P < 0"001) for normal and hemiplegic subjects (r 0"92; P < 0'001). Little correlation was found between the alpha amplitude and the EOG when one was recorded on a different side than the other. When the subjects in the normal and hemiplegic groups were asked to follow a target moving independently of their eye movements, the data summarized in Figs. 3(a) and 3(b) resulted. A significant relationship was found between the mean EOG and alpha rhythm as a function of time among both normal (r ~ 0"78; t -: 2'04; P 005) and hemiplegic groups (r 0"86; t -- 2"70; P < 0"01). Significant differences were also noted in the mean amplitude of both the EOG and alpha rhythm between the normal and hemiplegic groups. The hemiplegic group had an overall lower mean amplitude of both the EOG and alpha rhythm than did the normals (t ~- 2"93; P < 0"01). When the target was stabilized on the retina, the EOG and alpha rhythm still co-varied in each group. However, there were no longer any significant differences in the mean amplitudes of both dimensions between normal and hemiplegic groups. The general electrical changes related to attention, active vision and recall were now investigated. The normal and hemiplegic subjects were given a chart which duplicated the oscilloscope screen and were asked to recall and reproduce the last position of the target on the screen under both stabilized and non-stabilized retinal image conditions. The results presented in Table 1 show that among hemiplegic subjects, under normal viewing conditions, attention to stimuli seems to produce a significantly lower mean alpha

213

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FtG. 4. Co-variance of the mean alpha and EOG amplitudes among (a) normal and (b) hemiplegic subjects while viewing an oscilloscope target driven by the subjects' saccadic eye movements. amplitude than found for normals (t = 2"79; P < 0"01). It was also f o u n d that the hemiplegic patients exhibited an alpha potential amplitude lower than that found for normal subjects during attempted recall. Significant differences were also noted with both active vision and attempted recall between stabilized and non-stabilized retinal image conditions for both groups. Attempted recall does not produce the same degree o f suppression o f alpha activity (in all cases) as does active vision under both normal viewing and stabilized image conditions. A n analysis of variance of the mean potentials for attempted recall and active vision indicated significance in both the normal and hemiplegic groups respectively (F ----- 2'41; P < 0-01; F = 1"84; P < 0'05).

214

GERALD LEISMAN

Table 1. The reduction of potential with active vision and attempted recall of stabilized images (S) and non-stabilized images (NS) in normal and hemiplegic-attentionally handicapped subjects

Subjects and conditions

.'~ potential alpha (in uV) for 10 sec

S.D.

~ Reduction of potential

Normal (N = 28) Eyes closed Active vision (NS) Active vision (S) Attempted recall (NS) Attempted recall (S)

27.5 16-4 12-5 19.8 19.2

3.76 2.72 3'69 2.79 2.65

-41 65 28 31

Hemiplegic (N = 36) Eyes closed Active vision (NS) Active vision (S) Attempted recall (NS) Attempted recall (S)

19.3 8.2 13.1 11.4 18.3

3.09 3.47 2.69 3.25 2.87

58 33 41 6

Frequency changes of the usual 8-13 cycle/sec to 13-15 cycle/sec and lower voltage activity were observed in 60 per cent of the tracings in the stabilized-image active vision condition among brain damaged patients. A comparative group of 67 per cent of the normal subjects achieved similar results. However, under the normal viewing active vision condition, 29 per cent of the hemiplegic subjects exhibited increased frequency and lower voltage activity compared with 59 per cent of the normal individuals. During recall by normal subjects under non-stabilized image conditions, a complete suppression of the alpha rhythm was infrequent, a simple amplitude diminution being more usual. On the other hand, during normal viewing conditions in brain damaged patients complete suppression of the alpha rhythm was more common than just the simple amplitude diminution found for normals (t = 3'27; P < 0"001). No significant differences were noted between the normal and hemiplegic groups during attempted recall under stabilized image conditions. Under the conditions of this experiment, the induced electrical changes were fairly constant for periods of longer than 10 sec. The factors found to be significantly correlated with reduction in potential with active vision under stabilized image conditions are listed in Table 2. Variables found to have no significance in the reduction o f potential were the age and sex of the subjects, the presence or absence of abnormality in the E E G tracing, the rate of return of the alpha rhythm following eye closure and the type of frequency change occurring during active vision. Among the normal subjects, the reduction of potential with recall seemed to be associated with the same factors resulting in a reduction with active vision. However, the greater reduction of potential with large degrees of rhythmicity was not signficant by the %~ test. An attempt was also made to study the relationship between the features of the EEG and attentive behavior. The subjects were requested to reproduce the last position of the oscilloscope target on a sheet of paper with a reproduction of the screen printed on it.

215

SACCADIC EYE MOVEMENTS A N D THE A L P H A R H Y T H M

Table 2. Factors correlated with potential reduction with active vision under stabilized image conditions in normal and hemiplegic-attentionally handicapped subjects

Groups and criteria Normal (N = 28) alpha resting potential 9.8-24.5 gtV 24.6-77.0 IxV rhythmicity* I + 2

3 + 4 reduction with recall 0-27 ~ 28-78 ~ Hemiplegic (N = 36) alpha resting potential 9.8-24"5 laV 24.6-77.0 gtV rhythmicity* 1 -I-2 3 q- 4 reduction with recall 0-27 ~ 28-78 ~

reduction with active vision

3-50 42

51-82 9

11

38

35

10

16

39

34

15

13

38

69

2

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*Rhythmicity is based on a 4 point qualitative scale with 1 = little or no rhythmicity and 4 = nearly continuous sinusoidal activity.

Table 3 illustrates that under normal viewing conditions, the number of adequate reproductions of perceived targets was significantly less for hemiplegics than for normals (t ---3"14; P < 0"001). However, no significant differences were found in the adequate target reproductions between hemiplegic stabilized image and normal non-stabilized image subjects.

Table 3. Active recall and reproduction of targets under stabilized image (S) and non-stabilized image (NS) conditions amongst normal and hemiplegicattentionally handicapped subjects

Group

accurate drawings

~ intermediate drawings

~o poor drawings

Normal (NS) Hemiplegic (NS) Hemiplegic (S)

82 30 78

14 14 5

4 56 17

216

GERALD LEISMAN

DISCUSSION A relationship between saccadic eye movements and the alpha rhythm has been found. LINDSLEY [4] thought that stimuli were coded upon input to aid in perceptual clarity. He conceived of a mechanism in which saccadic eye movements are linked with alpha activity. The movements occur during an inexcitable phase to avoid retinal discharge impinging on the cortex. LIPPOLD [21] had pointed out that both sides of the visual cortex are equally innervated from both eyes and the correlation between alpha and E O G on the ipsilateral side, according to Lippold, cannot be mediated by retinal connections. This, however, is not quite the case as both sides of the visual cortex are not equally innervated from both eyes because of the monocular crescent of fibers from the nasal retina. Therefore, one would expect a correlation between alpha and E O G on the contralateral side. This was not found and it was assumed that the effect was mediated by retinal connections. MULnOLLAND and EVANS [7] noted that alpha rhythm was related to rolling the eyes up and its absence with looking straight ahead, independent of illumination and independent of eye opening or closure. Their conclusion was that ocular-motor function may be integrally involved with the mechanisms of alpha activation. DEWAN [8] had also reported that the eyes had to be raised for alpha rhythm to occur and there had to be an absence of fixation and accommodation. KUHKOWSK~ and LEISMAN [22] have found, however, that with partial paralysis of the extraocular muscles achieved by retro-bulbar anesthesia and with bilateral pupil dilation and restriction of accommodation alpha rhythm was still present. I f the alpha rhythm is a rhythm of rest produced by cells in the occipital cortex, inactive from the point of view of vision, then the speed of mobilization of these cells for the purpose of seeing might provide evidence for an intermediate mechanism between the reception of a stimulus and the motor response. ELHNGSON [23] and HARTER [24] had seen the alpha rhythm as reflecting a type of scanning mechanism. PIT~s and McCULLOCH [25] suggested that the sweep of negativity in the cortex constituted a scanning mechanism involving excitation of successive layers by non-specific afferents which lowered the threshold of those layers to the incoming afferents. An average value of the excitations was thought to have been computed in the cortex and released at the conclusion of each scan. GREy WALXER [26] suggested that a spatial pattern is reduced to a temporal one to make information more readily available to analyzers. He thought the amplitude would be greatest in the absence of a signal, when the potentials would be regular and rhythmic. Grey Walter also thought that the effects of photic stimulation on alpha frequency might stem from interference with a scanning mechanism. GAARDER et al. [10] found a component of alpha activity which was time locked to the occurrence of fixation saccadic eye movements. They found a phase relationship prior to the onset of the saccade. It was thought, therefore, that the saccade does not serve as a stimulus which locks the alpha activity into phase, but that alpha activity reflects the driving of saccades. If the alpha rhythm is related to saccadic eye movements [4-10] and if the differences which exist in the duration of saccadic eye movements between normal and hemiplegic subjects [12] are related to the ability to perceive and integrate visual information in the cortex, then manipulating the variable of the influence of saccadic eye movements (i.e. deviant patterns of scanning and fixation) by stabilized image techniques should show

s ACCADICEYE MOVEMENTSAND THE ALPHA RHYTHM

217

c h a n g e s in the a m p l i t u d e o f the a l p h a r h y t h m and i m p r o v e m e n t in the ability o f h e m i plegics to recall i n f o r m a t i o n . T h e results are c o n s i s t e n t with these n o t i o n s .

REFERENCES 1. ADRIAN,E. D. and YAMAGIWA,K. Origin of Berger rhythm. Brain. 58, 323-351, 1935. 2. PENFIELD,W. and JASPER, H. Epilepsy and the Functional Anatomy of the Human Brain. Little, Brown, Boston, 1954. 3. WALTER, W. G. Intrinsic rhythms of the brain. Handbook of Physiology. Section 1 : Neurophysiology. J. FXELD, H. W. MAGOUN and V. E. HALL (Editors). Vol. 1, pp. 279-298, 1959. Washington, D.C.: American Physiological Society. 4. LINDSLEY,D. B. Psychological phenomena and the electroencephalogram. Electroenceph. clh~. Neurophysiol. 4, 443~,56, 1952. 5. MEISTER, R. K. .4 Hypothesis Concerning Visual Alpha Rhythm with Reference to the Perception of Movement. (Unpublished doctoral dissertation, University of Chicago), 1951. 6. GRoss, E. G., VAUGHN, A. G. and VALENSTEIN,E. Inhibition of visual evoked responses to patterned stimuli during voluntary eye movement. Electroenceph. olin. Neurophysiol. 22, 204-209, 1967. 7. MULHOLLAND,W. and EVANS, C. R. Ocularmotor function and the alpha activation cycle. Nature, Lond. 211, 1278, 1966. 8. DEWAN, E. M. Occipital alpha rhythm, eye position and lens accommodation. Nature, Lond. 214, 975-977, 1967. 9. GAARDER,K., KRAUSKOPF,J., GRAF, V., KROPFL, W. and ARMINGTON,J. C. Averaged brain activity following saccadic eye movement. Science, N.Y. 146, 1481-1483, 1964. 10. GAARDER,K., KORESKO, R. and KROPEL, W. The phasic relation of a component of alpha rhythm to fixation saccadic eye movements. Electroenceph. clin. Neurophysiol. 21,544-551, 1966. 11. CALLAWAY,E. and YAEGER, C. L. Relationship between reaction time and electroencephalographic alpha phase. Science, N.Y. 132, 1765-1766, 1960. 12. LEISMAN,G. (unpublished observations). 13. LEISMAN,G. Conditioning variables in attentional handicaps. Neuropsychologia. 11, 199-295, 1973. 14. ROSVOLD, H. E., MIRSKY, A. F., SARASON,I., BRANSOME,E. D. and BECK, L. H. A continuous performance test of brain damage. J. cons. Psychol. 20, 343-350, 1956. 15. ARDEN, G. B. and KELSEY, J. H. Changes produced by light in the standing potential of the human eye. J. Physiol., Lond. 161, 189, 1962. 16. KRIS, C. Diurnal variation in periorbitally measured eye potential level. Electroenceph. clin. Neurophysiol. 9, 382, 1957. 17. KRIS, C. Corneo-fundal potential variations during light and dark adaptation. Nature, Lond. 182, 1027-1028, 1958. 18. LIPPOLD,O. C. J. Bilateral separation in alpha rhythm recording. Nature, Lond. 226, 459, 1970. 19. LIPPOLD, O. C. J. Alpha rhythm and extraocular muscles. Lancet ii, 1138, 1970. 20. FORD,A. WHITE, C. T. and LIcrrr~NSTEIN, M. Analysis of eye movements during free search. J. opt. Soc. Am. 49, 287-292, 1959. 21. LXPPOLD,O. C. J. Origin of the alpha rhythm. Nature, Lond. 226, 616-618, 1970. 22. KULIKOWSKI,J. and LEISMAN,G. The effect of nitrous oxide on the relation between the evoked potential and contrast threshold. Vision Res. 13, 2079-2086, 1973. 23. ELLINGSON,R. J. Brain waves and problems of psychology. Psychol. Bull. 53, 1-34, 1956. 24. HARTER, M. R. Excitability cycles and cortical scanning: a review of two hypotheses of central intcrmittency in perception. Psychol. Bull. 68, 47-58, 1967. 25. PITTS, W. and MCCULLOCH, W. S. How we know universals: the perception of auditory and visual forms. Bull. Nat. BiD. Phys. 9, 127, 1947. 26. WALTER,W. G. The Living Brain. Duckworth, London, 1953.

R~sum6---Cette recherche concerne les relations entre les potentiels 61ectro-oculographiques (EOG) et le rhythme alpha chez sujets h6mipl6giques avec des d6ficits attentionnels. On a pens6 que le rhythme alpha est reli6 temporellement b. I'EOG. On a 6tudi6 28 sujets normaux et 36 sujets avec h6mipl6gie spastique pr6sentant des d6ficits attentionnels. Le rythme alpha et I'EOG 6taient mesur6s et subissaient des variations exp6rimentales par modification de l'illumination et par des techniques de stabilisation de l'image r6tinienne. Les r6sultats sont en accord avec les hypoth6ses et indiquent que des patterns d6viants des mouvements oculaires de balayage et de fixation saccadique peuvent 6tre des composantes importantes des handicaps attentionnels.

218

GERALD LEISMAN Zusammenfassung--Die Untersuchung besch/iftigt sich mit der Beziehung zwischen elektrookulographischen Potentialen (EOG) und dem Alpha-Rhythmus bei hemiplegischen Patienten mit St6rungen in der Aufmerksamkeit. Es wird angenommen, dab dcr Alpha-Rhythmus tempor~ir in Beziehung zum EOG steht. 28 normale und 36 Probanden mit spastischer Hemiplegie und Aufmerksamkeitsst6rungen wurden untersucht. Alpha-Rhythmus und EOG wurden abgeleitet und dutch Wechsel der Beleuchtung und unbewegliche Netzhantbilder experimentell ver~indert. Die Ergebnisse stimmen mit den Hypothesen fzberein und zeigen, dab abweichende Skandierungs--und Fixationsmuster in den sakkadierenden Augenbewegungen wahrscheinlich wichtige Komlaonenten bei Aufmerksamkeitsst6rungen sind.