Development of rhythmic E.E.G. activities in infancy (waking state)

Rev. E.E.G. Neurophysiol., 1977, 7, 3, 327-334.

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DEVELOPMENT OF RHYTHMIC E.E.G. ACTIVITIES IN INFANCY (WAKING STATE) G. P A M P I G L I O N E ,

MD, FRCP

Department of Neurophysiology, Great Ormond Street, London WC1N 3JH. The Hospital for Sick Children,

R~SUM~ Ddveloppement des activitds E.E.G. rythmiques au cours de l'enfance. 666 enregistrements E.E.G. de veille ont dtd recueillis chez 146 nourrissons et jeunes enfants ~gds de 3 mois gt 5 ans, placds dans des erdehes ou des nurseries. Le choix de l' emplacement des dleetrodes et des montages a permis de ddtecter prdeocement les activitds rythmiques, de prdciser leur topographic et de suivre leur dvolution au tours de la maturation. Cette dtude montre que pour tout enfant, la maturation des activit~s rythmiques d~tectdes h I'E.E.G. clans les r@ions rolandiques, temporales et oceipitale mddiane, se fait par bond et non de fafon continue et progressive. Les d~lais avee lesquels ces drapes E.E.G. sont atteintes varient quelque peu suivant la r@ion c~rdbrale eonsiddrde.

INTRODUCTION. Since BERGER'S o b s e r v a t i o n s in 1932 t h a t the electrical activity o f the b r a i n in a m o n t h old baby is different f r o m t h a t of a six m o n t h old baby, a large v o l u m e of l i t e r a t u r e h a s a c c u m u l a t e d on the d e v e l o p m e n t a l aspects of t h e h u m a n E.E.G. R a t h e r t h a n reviewing t h e literature a n d discussing d i s c o r d a n t opinions of v a r i o u s authors, t h e p r e s e n t papers is limited to personal studies carried o u t o n n o r m a l i n f a n t s a n d children born a n d living in t h e L o n d o n area. T h i s work was carried o u t in order to establish s o m e aspects of m a t u r a t i o n of cerebral f u n c t i o n in v a r i o u s age groups, the range o f individual variability in type a n d t o p o g r a p h y of the E.E.G. activity recorded during the w a k i n g state, a n d the effect o f t r a n s i t o r y passive eye closure a n d s u b s e q u e n t eye opening. I n a n a t t e m p t to assess w h e t h e r cerebral m a t u r a t i o n is a u n i f o r m c o n t i n u u m or, instead, occurs in a series of s o m e w h a t irregular steps, the E . E . G . ' s were r e p e a t e d in m o s t of t h e children at v a r i o u s intervals r a n g i n g f r o m a few days to several m o n t h s . MATERIAL AND METHODS. Through the kindness of the Medical Officers of Health (now C o m m u n i t y Medicine) and the help of the Matrons of various day and residential nurseries a mixed population of y o u n g babies and children born in the London area were studied as well as my own children and those of friends. The consent of the parents, or guardians had been obtained in all cases. Adequate notes were available about the circumstances at

Texte pr6sent6 h la Soci~t~ d'E.E.G, et de Neurophysiologie clinique de langue franfaise le 30-11-1976, remis le 30-11-1976, d6finitivement accept6 le 20-5-1977. Tir~s gt part : G. PAMHGLIONE (~t l'adresse ci-dessus).

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birth, earIy milestones, familial and social aspects. The meals during the day provided in the nurseries were similar and of adequate nutritional value. None of the children had detectable cerebral disorders and most of the infants in the day nurseries were there because their mothers were at work during the day and could not take their babies with them. Each infant had been in the Nursery for at least a couple of months by the time the first E.E.G. was taken, and was fully accustomed to the locaI routine of feeding, rest and play. No attempt, however, was made to standardise the many environmental factors at home that might have influenced each child's early development. MONTAGES FOR 8 CHANN'~L EEG ApPARAIIIS

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Montages utilis~s d l'H6pital des Enfants Malades de Londres (dlectroencdphalographe 8 canaux). La plupart des montages rdalisent des suites d'Olectrodes (hormis le montage VI qui correspond une rdJ~rence moyenne de type Golclman-OJfner).

All the E.E.G. were taken in the nurseries with a uniform technique using a portable 8 Channel E.E.G. apparatus (Offner Type T). In spite of the occasional earthing problems in some nurseries, all records were taken with a high frequency response ± 10 p. 100 linear up to 70 c/s, a time constant of 0.3 seconds and a sensitivity of 10 microvolts per millimeter pen deflection. The paper speed was usually 30 millimeters per second, though on occasions reduced to 15 millimeters per second. The silver-silver chloride disc electrodes were stuck to the scalp with Collodion according to measurements from bony landmarks (PAMPIGLIONE, 1956), but in view of the smallness of the ear in young children the mid-temporal electrodes were placed immediately above the pre-auricular point. The electrode on the mid line in the occipital region was placed about 1-1 1/2 cm above the occipital protuberance. The montages were those indicated in figure 1, although in the illustrations of E.E.G. samples fewer montages are shown in order to emphasise particular points.

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Each record lasted between 20 minutes and one hour and during this time some of the babies became drowsy or fell asleep. However, as part of the procedure at least half of the record was taken during the waking state and passive eye closure was carried out for periods of 2-10 seconds and repeated several times. In addition the effect of sudden noises (hand clap) or calling the child by n a m e was also included. A total of 666 records were taken on 146 infants and children between the age of 3 m o n t h s and 5 years, with an average of over 4 records per child. In the present survey no photic stimulation was carried out and no drugs of any kind were given, either on the day of the test or in the previous 2 weeks. Babies, however continued their routine immunisatio n programme. All the E.E.G.'s were studied by the author with uniform criteria. Particular attention was devoted to the main rhythmic components and their distribution over the two hemispheres during the waking state, when the child was looking around, handling toys or playing with them. In y o u n g babies sucking a teat, this was at times gently removed from the m o u t h (frustrating stimulus) and then re-inserted (gratification). The repeated gentle application of the fingers on the eyelids to obtain passive eye closure for a few seconds was an integral part of the examination, but some of the babies protested ; as an alternative manoeuvre vision was occluded with the palm of the hand, or a soft cloth or with tissue paper. The technique is familiar to all parents and nannies (the <>) and parallel to that illustrated in a study of the E.E.G. in young dogs (PAMPIGLIONE, 1963). RESULTS. Three m a i n areas were f o u n d where, d u r i n g the w a k i n g state, r h y t h m i c activity appeared with s o m e w h a t different characteristics and evolution : n a m e l y the rolandic areas, the mid temporal areas, a n d the m i d occipital area, as follows : 1. In the rolandic area of each hemisphere a n d at the vertex s o m e r h y t h m i c activity kept o n appearing in m o s t infants at s o m e w h a t irregular intervals, in the f o r m of tufts o f 8-10 per sec waves of the order of 20-40 microvolts, w i t h variable lateralisation, often occurring independently over the right or t h e left side. This activity t h o u g h recognizable at 3 m o n t h s became well established by the age of 6 m o n t h s a n d would persist in the s a m e child for m a n y years with relatively m i n o r individual variations. This activity w o u l d often diminish or disappear altogether w h e n t h e baby used his h a n d s or played with toys, b u t it w o u l d increase w h e n t h e baby was at rest with his a r m s a n d h a n d s re/axed. I n the first 3 to 6 m o n t h s this activity was less obvious, often m i x e d with m o r e p r o m i n e n t slower r h y t h m i c activity at a b o u t 5-6 per sec in the s a m e areas, w i t h similar characteristics. B o t h these activities w o u l d n o t be affected by eye opening or eye closure b u t would d i s a p p e a r during drowsiness a n d sleep. T h e i r d i s t r i b u t i o n , frequency a n d b e h a v i o u r were similar to t h o s e of the m u r h y t h m in older children a n d adults. 2. In the mid temporal areas r u n s of r h y t h m i c 4 per sec waves were recognisable during t h e w a k i n g state, reaching 50-100 microvolts in m o s t babies between the ages o f 3 a n d 18 m o n t h s with variable lateralised p r e d o m i n a n c e . T h i s activity w o u l d usually a p p e a r in relatively short runs lasting 1 or m o r e seconds a n d did n o t s e e m to be related to m o v e m e n t s of the h a n d s or opening or closing of the eyelids. S o m e t i m e s this activity would be increased when t o u c h i n g the baby, particularly in the perioral region, b u t this p h e n o m e n o n was n o t c o n s t a n t and it seemed t h a t t h e presence or absence of this activity was related to s o m e w h a t less obvious, p e r h a p s m e n t a l or emotional factors. Sometimes, this activity w o u l d increase w h e n the teat t h a t t h e baby w a s sucking was removed f r o m his m o u t h b u t again, as this action was repeated, the p h e n o m e n o n was n o t necessarily seen again. There was no s u b s t a n t i a l change in frequency, amplitude, or distribution of this activity during the period between 3-18 m o n t h s after w h i c h it would disappear altogether. 3. In the occipital region o n the mid line a r o u n d the age of 3 m o n t h s r h y t h m i c activity at a b o u t 3 per second began to a p p e a r following passive closure of the eyes, t h e baby r e m a i n i n g awake. F r o m the age of 4-5 m o n t h s to a b o u t 7-8 m o n t h s the m a i n r h y t h m i c activity elicited by passive eye closure in the m i d occipital region was at a b o u t 4-5 c/s. Its frequency w o u l d change at a b o u t 8-9 m o n t h s to a well f o r m e d r h y t h m at 6 c/s p r o m p t l y a p p e a r i n g w h e n vision was occluded a n d this r h y t h m equally p r o m p t l y blocked on eye o p e n i n g w o u l d persist until a b o u t 2 years of age. This

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activity was also seen in the parietal and posterior temporal areas though somewhat slower and larger in the posterior temporal than in the parieto-occipital region between 9 and 15 months. Occlusion of vision through passive eye closure was remarkably effective in eliciting this type of E.E.G. change in all babies and young children tested, provided the confidence of the infant had been secured and the baby was contented and relaxed during the <>game. It was essential that the eye lids be completely closed and that the baby or child did not peep. The occlusion of vision seemed to be much more important than the contact of the hands or cloth on the eye lids. The amplitude of the activity at about 3-5 c/s between 3 and 5 months was of the order of 100 microvolts, while

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after the age of 5 months it increased in amplitude to 100-200 microvolts. At an age of between 7 and 9 months with considerable individual variability the frequency rapidly increased to 6 c/s in all European and Indian children, though this change occurred somewhat earlier in African Negro children. This occipital activity on eye closure remained remarkably stable in frequency and amplitude between 9 and 24 months with relatively minor changes in amplitude (diminishing in the last few months). In all cases this activity would be blocked on eye opening if the infant remained awake. However, if he dozed off this activity (like the alpha rhythm of older children) would disappear, to reappear on waking up. During drowsiness this rhythmic activity could reappear for a few seconds on eye opening and disappear as soon as the baby was fully alert whitb his eyes open. At the age of 24-27 months a fairly well formed alpha rhythm, at about 8-9 c/s would appear during passive eye closure in the European and indian children (figure 2, a, b, c, d 3 and 4) of the

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order of 30-80 microvolts, while in the African Negro children the alpha rhythm at 8-9 c/s could be seen as early as 15-18 months with similar frequency, amplitude, distribution and dynamic features. The amplitude of this activity was sometimes slightly larger over the right than over the left temporo-occipital region but the asymmetry was not constant. Individual differences in the rates of E.E.G. development seemed to be related to some ethnic or genetic factors (PAMPIGLIONE,1965) but by the age of 2 1/2 years the frequency and amplitude of the alpha rhythm reached a similar range, whether in African Negro children or in European and Indian children. At whatever age, it was often difficult to elicit the rhythmic activity on the first attempt at passive eye closure and the manoeuvre had to be repeated on several occasions, once the infant began to enjoy the game.

DISCUSSION. From serial E.E.G. studies in each child it became apparent that the variability in type and distribution of rhythmic activities between 9 months and 2 years of life was much less marked than suggested by previous studies. Moreover there was an independent maturational evolution of the E.E.G. features in the various regions of the cerebral hemispheres during the waking state. For example, the rhythmic activity in the rolandic areas had an early maturation in the first 6 months while the activity elicited by passive eye closure in the occipital area had a much more complex and later evolution over a period of about 2 years (fig. 5). In the literature statistical studies of fairly large numbers of children tended to average out individual variations. This could lead to a false impression that the change in so-called dominant frequencies was continuous and followed a smooth curve. In the present study it soon became apparent that such maturational evolution was not a uniform process when each child was considered separately. When allowances were made for particular ethnical differences definite ~ electrical milestones ~ emerged in these normal children with relatively short periods (a few days or perhaps a few weeks) during which the change in frequency would occur, Then, for much longer periods of several months (particularly between 9 and 24 months), the frequency of the rhythmic activity in the occipital area would not change until the next maturational step (fig. 6). While the alpha rhythm at 8-9 c/s persisted at this frequency and amplitude (30-80 microvolts) at least until the age of about 5 years, the present follow-up was not extended to an older age group and no longitudinal data are available on further maturational steps such as the development of the adult alpha rhythms. The main emphasis of this paper is on the discovery that different maturational steps in the electrical activity of the brain occur in different areas of the cerebral hemispheres in any normal infant. This is obvious in the development of the mu rhythm in the rolandic areas and particularly of the alpha rhythm in the occipital region. In the literature some topographic differentiation had already been described in some early work by M me SAMSON-DOLrUSand by DUMMERMUTHbut longitudinal studies of the same babies and children as they grew older seem to he few. Different authors employed different electrode placements (often without a mid line occipital electrode) and different montages in the maturational studies of the electrical activity of the brain. Moreover the importance of passive eye closure in eliciting rhythmic activity in the occipital region has largely been neglected. The confusion in the literature about the age at which a proper alpha rhythm at 8-9 c/s begins to appear may well be related to the various techniques employed in the study of maturational phenomena. In view of some ethnic differences (PAMPIGLIONE,1965) it is probable that statistical studies on a mixed population have blurred the existence of fairly precise electrocerebral milestones in each child. There is no doubt in the present study that by the age of 24-27 months in a North European

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RHYTHMIC E.E.G. ACTIVITIES IN INFANCY MATURATIONOFTHE ELECTRICALACTIVITYOFTHE BRAIN OF NORMALCHILDREN

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Fro. 5. - - Diagrammatic changes in frequency in the rhythmic E.E.G. activity recorded from the rolandic regions (dotted line)and from the parieto-occipital region (continuous line). Regional maturation occurs at different times in these different areas of the brain. (Reprinted from : G. P . , <>, John Wiley and Sons, New York, p. 239.) Diagramme des variations de frdquence de l' aetivitd tythmique des rdgions rolandiques (pointilld) et paridto-occipitales (ligne eontinue). Les temps de maturation rdgionale sont difJ~rents clans ees rOgions e~rdbrales. (Reproduit de G. P. <>, John Wiley and Sons, New York, p. 239.)

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population (and in some Indians) the alpha rhythm at 8-9 c/s becomes well established while in black African children and probably in some Mediterranean children this type of maturational step occurs earlier (often even before 18 months). The equivalent of the adult mu rhythm at about 8-10 c/s becomes established in contrast with the alpha rhythm by the age of 6 months or earlier, while other rhythmic components during the waking state like the runs of 4 c/s waves in the mid temporal regions occur only for a limited period in infancy and usually have already disappeared by the age at which the 8-9 c/s alpha rhythm becomes well established in the mid occipital area. There appear to be critical phases in the maturation of the electrical activity of the brain which are to some extent predictable in terms of age of each child provided other factors such as ethnic and nutritional aspects are known. The idea often mentioned in the literature that the alpha rhythm is not seen in children until the age of 3-5 years is in contrast with the present finding and may well be due to differences in techniques employed. Of course, omission of transitory passive eye closure might have given a different slant to the interpretation of the E.E.G. findings. The second point that emerges from the present survey is that electro-cerebral maturation in a given area does not appear to be a continuing uniform process but occurs in irregular steps. This finding is parallel to observations in young dogs (PAMPIGLIONE, 1963), in young pigs (PAMPIGLIONE, 1 971) and in young lambs (PAMPI~HONE, to be published). It seems therefore that such electrocerebral milestones are a more general biological phenomenon, at least in mammals, even if the age at which each maturational step is reached differs substantially in different species. At present we do not know the biological significance of maturational differences in the regional activity of the brain whether in animals or man although it seems that afferences from peripheral sense organs play only a very limited role in the regional development of the human E.E.G. Factors related to malnutrition (through some other poorly understood mechanisms) may have instead some importance in delaying some aspects of cerebral maturation in babies. It is very much hoped that the present report will ecourage some uniformity of methods in the study of maturation of cerebral function and a better understanding of its underlying mechanisms.

BIBLIOGRAPHY BERGER (H.). Ueber das Elektrenkephalogramm des Menschen, V. Arch. Psychiat. Nervenkr., 1932, 98, 231-254. PAMPIGLIONE (G.). Some anatomical considerations upon electrode placement in E.E.G. Proc. Electrophysiol. Technol. Ass., 1956, 7, 1-11. PAMeIGLIONE(G.). Development of cerebral function in the Dog. Butterworth, London, 1963. PAMPIGLIONE (G.). Brain development and the E.E.G. of normal children of various ethnical groups. Brit. Med. J., 1965, 2, 573-575. PAMPIGLIONE (G.). Some aspect of the development of cerebral function in mammals. Proc. Roy. Soc. Med., 1971, 64, 429-435. PAMPIGLIONE (G.). E.E.G. studies in animals with experimental malnutrition. In : ~< Brain function and malnutrition ~. Edited by PRESCOTT,.L W., READ, M. S. and COURSIN, D. B., John Wile)' and Sons, 1975, New York.