Electroencephalography and Clinical Neurophysiology, 1977, 4 2 : 6 9 1 - - 6 9 6

691

© Elsevier/North-Holland Scientific Publishers Ltd.

REGIONAL C E R E B R A L BLOOD FLOW IN CHILDREN. A R H E O E N C E P H A L O G R A P H I C STUDY OF THE MODIFICATIONS INDUCED BY READING J. JACQUY, P. NOEL, A. SEGERS, R. HUVELLE, A. PIRAUX and G. NOEL.

Department of Neurology, C.G.T.R., Montigny-Le-Tilleul and (P.N. and A.S.) Department of Pediatrics, H6pital Saint-Pierre, University of Brussels (Belgium) (Accepted for publication: October 19, 1976)

Cerebral blood flow has not been studied in children as extensively as in adults. Kety (1960) examined 13 children aged 5 to 10. He found CBF of about 100 ml/100 g/min as opposed to values of 50 to 55 ml/100 g/min in normal adults. In awake adults the CBF is not homogeneously distributed in the hemishere, being larger in the frontal than in the post central and temporal regions (Wilkinson et al. 1969). The distribution of the CBF in the awake child is not known. In adults, it is well known that mental activity induces specific modifications of the regional CBF (rCBF) (Ingvar and Risberg 1967; Ingvar and Schwartz 1974). These modifications can differ in the dominant and nondominant hemispheres according to the pattern of mental activity (Risberg et al. 1975). By rheoencephalography, an index (F) can be obtained which is highly consistent with the grey matter CBF (Fg) evaluated by intracarotid Xej3a clearance studies (Jacquy et al. 1974). This F index does not take into account the amplitude of the rheogram b u t takes into consideration the ratio between terminal and maximal slopes. It is independent of global tissue impedance. A good correlation exists not only with grey matter blood flow b u t also with its variations in hypo- or hypercapnia. During mental activity in the normal subject, the metabolic regulation of cerebral blood flow depends on CO2 production (Wahl et al. 1970; Ingvar and Schwartz 1974). Our method is thus well

adapted to the study of mental activity in the normal subject. The regional F variations were studied in subjects undergoing somatosensory stimulation or performing m o t o r tasks (Jacquy et al. 1976; Piraux et al. 1976). The aim of the present study was to determine the F index in children aged 6--11 and the modifications thereof induced by reading. The collected data were compared to those obtained in adults in similar conditions.

Material and methods

Subjects Twenty-seven subjects volunteered for this study, 10 adults (2 females and 6 males, 26-46 years old) and 17 children (7 females and 10 males, 6--11 years old). The children aged 6 had acquired syllabic reading for at least 4 months. The dominant side, as assessed by the laterality test of Harris (1958), was the right for hand, foot and vision in all the adults and in 9 children, while it was the left in 8 children. Dyslexic subjects were discarded from this study.

Rheographic recording The rheoencephalographic methods have been described in detail (Jacquy et al. 1974). The rheoencephalograph was a 4-electrode device with current emission circuit separate from the recording circuit. The rheoencepha-

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logram and its first derivatives were o b t a i n e d with an Elema p o l y g r a p h and averaged b y a c o m p u t e r o f average transients (CAT 400) triggered by the precordial e l e c t r o c a r d i o g r a m . Eight to 15 runs (0.5 sec for each run) were r e c o r d e d on the p o l y g r a p h . T h r o u g h metallic 15 sq cm surface electrodes, the occipital, parietal, precentral, p r e f r o n t a l and t e m p o r a l activities were r e c o r d e d in a 350 sec period. The F index measured was closely related to the grey m a t t e r b l o o d flow as d e t e r m i n e d b y the i n t r a c a r o t i d Xe t e c h n i q u e ( J a c q u y et al. 1 9 7 4 ) . The first run was p e r f o r m e d with the subject sitting quietly in an armchair, the eyes open. S u b s e q u e n t runs were r e c o r d e d 90 sec after the initiation o f m e n t a l activity i n d u c e d b y reading or p e r f o r m i n g a spatial test. The aim o f these tests was fully explained to the adults, i.e., to evaluate their c o n c e n t r a t i o n ability. In the preceding days, the children had the o p p o r t u n i t y to a t t e n d a r h e o e n c e p h a lographic r e c o r d i n g p e r f o r m e d o n a n o t h e r child in o r d e r to avoid a n x i e t y d u r i n g t h e test. T h e y were presented with t h e test as a c o m p e t i t i o n b e t w e e n children o f the same age. The spatial test was n o t used for the children for fear o f a lack o f a t t e n t i o n or f r u s t r a t i o n reactions.

s t a n d a r d texts, a d v e n t u r e stories for the adults and children over 8 or s h o r t sentences for children u n d e r 8. In t h e latter case, it was assessed that after the test t h e y were able to read t h e m aloud. The subjects were instructed to read to themselves w i t h o u t a n y a t t e m p t at m e m o r i z i n g . Nevertheless, all the children aged 6 to 8 m o v e d their lips during the test.

Spatial test The subjects were presented with t w o pairs o f a p p a r e n t l y identical pictures with eight slight differences w h i c h t h e y had to find o u t and signify after c o m p l e t i o n o f the recording. In the 350 sec period o f the test, eight subjects d e t e c t e d six or seven differences in the first set.

Results

Hemispheric F values at rest (Table I) The m e a n h e m i s p h e r i c F was larger in the children t h a n in the adults. It decreased significantly b e t w e e n age 6 and 11. There was no d i f f e r e n c e b e t w e e n right and left h a n d e d subjects o f the same age, or b e t w e e n the t w o hemispheres.

Reading test

Regional F values at rest (Fig. 1)

The subjects were presented with simple

The F values were n o t significantly differ-

TABLE I Item±spheric F values at rest Groups

N

Mean age + S.D.

Hemispheric F values. see-1 M ± S.D.

A. Adults B. Children aged 6 to 8 C. Children aged 9 to 11 D. Right-handed children E. Left-handed children

10 9 8 9 8

36 7 10 8 8

90 ~ 9 --1 ± 3 (N.S.) 139 ± 23 --1 ± 2 (N.S.) 121 + 16 --2 ± 5 (N.S.) 133 + 27 I ± 2 (N.S.) 128 ± 15 --2 ~+3 (N.S.) Differences A versus C: P < 0.001 B versus C: P < 0.05 D versus E: N.S. The test of significance of variance ratio (between groups - - within groups) F: significant at 1%.

• 10 ~ 1 + 1 , 2 ± 2

Difference left hemisphereright hemisphere, sec -1 M ± S.D.

R E G IN C H I L D R E N

693

AGE 6-8

F(sec -I ) : 139_+ 23

+ 22°/°

+ 14 °/o

9-11 : 121+16

+13°/o 22-50 : 90-+9 25% I ~ \ / + 25% Fig. 1. D i s t r i b u t i o n of regional F values as % of h e m i spheric F value. A d i f f e r e n c e of +25% is r e p r e s e n t e d by a black q u a d r a n t . A d i f f e r e n c e of --25% is repres e n t e d by a h a t c h e d q u a d r a n t . T h e level o f significance o f t h e difference f r o m h e m i s p h e r i c value o f regional F values is s y m b o l i z e d by: *, for P < 0 . 0 5 ; **, for P < 0.01; ***, for P < 0.001.

ent in homologous hemispheric areas. In the adults the F values were larger in the frontal, smaller in the parietal and temporal areas. In the children another pattern emerged in which the largest F value was found in the temporal area. Between age 9 and 11 the predominance of the frontal areas was not statistically evident.

Reading test in children and adults Reading induced a clear-cut increase in mean hemispheric F in both groups (Table II). In the adults this increase was more evident in the dominant hemisphere, the main asym-

+23"/. RIGHT-HANDED ADULTS

(~

+ 2S°/°

Fig. 2. Mean h e m i s p h e r i c and regional F increases as p e r c e n t a g e of resting values in adults.

metry being obtained in the temporal (P < 0.01) and precentral (P < 0.05) areas (Fig. 2). In the children, the F values increased symmetrically in both the dominant and nondominant hemispheres. Moreover, no significant difference appeared between the homologous temporal and precentral areas. In the children under 9 the temporal CBF of the dominant hemisphere increased only in a small proportion as compared with the adult findings (Figs. 3 and 4).

Spatial test in adults (Fig. 2) During this test, hemispheric F increased in both hemispheres (P < 0.001) but more so on the right ( P < 0.01). The main asymmetry was discovered in the parietal ( P < 0,05) and prefrontol (P < 0.05} areas.

T A B L E II Increase of F (per c e n t ) i n d u c e d b y reading Groups

Left h e m i s p h e r e (%)

R i g h t h e m i s p h e r e (%)

Difference L > R (%)

Adults Right-handed children Left-handed children

22± 7 (P< 0.001) 17 +- 5 (P < 0 . 0 0 1 ) 13 ± 5 (P < 0 . 0 0 1 )

14± 5(P< 0.001) 14 + 3 (P < 0 . 0 0 1 ) 18 + 7 (P < 0 . 0 0 1 )

8+ 5(P< 0.001) 3 ± 5 (N.S.) --5 -+ 10 (N.S.)

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LEFTTEMPORALCHANGE ",-60 (°/o)

+L,O

+1"7%

m

go

+14% LEFT'HANDED

SD

+20

+13%



R= .67z,9 ( p < 0.05)

+18°/, ICHILDRENI

(~+25 °/o

6

" 7

8' 9' I'0 AGEINYEARS

II'

'

'

ADULTS

Fig. 3. Mean hemispheric and regional F increase, as percentage or resting values, induced by reading in children.

Fig. 4. F increase in the left temporal area induced by reading in right handed children and adults.

Discussion

affective hyperventilation was not observed in the children, a slight variation in paco 2 could have brought about a significant change in CBF. It is probable that ventilation changes do influence the flow, particularly in children.

Significance of the rheoencephalographic data Rheoencephalography is a unique nontraumatic m e t h o d of evaluating the grey matter CBF {Fg) (Jacquy et al. 1974). The contribution of the external carotid artery has been shown not to exceed 7% of the measures obtained by this technique. Interregional variations can be determined at rest and during mental activity (Piraux et al. 1976). The limitation of the method remains its relatively large error (up to 15%) and the limited spatial resolution due to the distance between the surface electrodes, as compared to the techniques described by Lassen and Ingvar (1972}. Systemic factors For practical reasons, no arterial blood pressure or paco 2 monitoring was performed, which would have necessitated arterial punction. It was presumed that the cerebral autoregulation was intact in the adults so that variations in the arterial blood pressure during the test would not influence the CBF. In the children this factor cannot be discarded since, to our knowledge, the cerebral autoregulation has not been studied in this age range. The same holds true for the paco2. Though an

F values at rest The results obtained in the adults are in keeping with previously published data (Jacquy et al. 1976). The 'hyperfrontal' pattern described in the normal awake adult (Ingvar and Franzen 1974) is thought to result from spontaneous conscious ideation. The F value in the children is significantly higher than in adults. Kety (1960) published lower values but it should be pointed out that he determined the global CBF, which is significantly inferior to the grey matter CBF (Wilkinson et al. 1969). Of more significance is the absence of 'hyperfrontality' in the children aged 6--11. These findings can be compared with those of genetic psychology. At age 7--11, children have not yet acquired the ability of abstraction. They can use neither verbal material, still less hypotheses, to build up logical thinking (Piaget 1962}. Also, at the same age, the alpha r h y t h m is predominantly situated in the posterior and the theta r h y t h m in the anterior regions (Samson-Dolfus 1963). This pattern could represent the particular

REG IN CHILDREN

distribution of rCBF in children, since a correlation between the rCBF and the EEG basic r h y t h m was demonstrated by Ingvar et al. (1965). Mental activity in the adults The increase of F in the dominant hemisphere during reading has already been described in the premotor, rolandic, sylvian and occipital regions (Ingvar and Schwartz 1974). In this study, the largest modifications were noted in the precentral and temporal areas of the dominant hemisphere, as previously reported by Risberg et al. (1975). On the contrary, the spatial test triggers an increased activity in the right hemisphere and notably in the parietal and prefrontal areas, which is consistent with the predominance of that hemisphere in spatial activity (Nebes 1974). But it should not be forgotten that, in these tests, other mental activity could be involved, such as memory. Reading in children The children appeared to be highly motivated in this study and read a large number of pages during the test. No attempt was made to oppose the silent verbalization of the children under 8, though there was a possibility of activation of the temporal structures, as noted in the adults (Ingvar and Schwartz 1974). The slight variation of the temporal F observed in these children argues against this hypothesis. These children had already acquired laterality, as demonstrated by the Harris test, yet the hemispheric increase of F disclosed no significant difference between the two sides as it did in the adults. The left temporal lobe did not exhibit the greatly increased activity observed in the adults. These data would support the hypothesis of a lack of specialization or, at least, of a rather labile hemispheric and regional specialization in children. This may be in accordance with well known facts about children with acquired aphasia and facultative alexia who, one year later, presented no residual difficulty in verbal and written speech.

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Summary Cerebral impedance changes (F changes) indicating cerebral blood flow were studied ill 17 children aged 6--11 years and in 10 normal adults. At rest, large values were found in children, who never exhibited the 'hyperfrontality' pattern of the adults. Reading induced an F increase in both the dominant and nondominant hemispheres, in contrast with a larger increase in the dominant hemisphere in adults. A spatial test was designed in adults which triggered a larger increase in the nondominant hemisphere.

R~sum~ Ddbit sanguin cdrdbral rdgional chez l'enfant. Etude rhdoencdphalographique de modifications lides d la lecture. Le d~bit c~r~bral ~tudi5 par une m~thode de rh~ographie (indice de d~bit F) a ~t~ estim6 chez 17 enfants ~g~s de 6 /t 11 ans et 10 adultes. Au repos, l'indice de d~bit ~tait plue ~lev6 chez l'enfant off l'on n'a pas retrouv~ le 'pattern hyperfrontal' de l'adulte. La lecture a augrnent~ l'indice de d~bit des deux h~misph~res alors que cette augmentation ~tait plus importante au niveau de l'h~misph~re dominant chez l'adulte. Un test spatial r~alis~ chez l'adulte a provoqu~ une augmentation plus marqu6e au niveau de l'h~misph~re non dominant.

References Harris, A.J. Harris tests of lateral dominance manual of directions for administration and interpretation, Psychological Corporation, New York, 1958. Ingvar, D.t4., Baldy-Moulinie,-, M., Sulg, I. and Horman, S. Regional cerebral blood flow related to the EEG. Acta Neurol. Scand. 1965, 14: 179. Ingvar, D.H. and Risberg, J. Increase of regional cerebral blood flow during mental effort in normal and in patients with focal brain disorders. Exp. Brain Res., 1967, 3: 195--211. Ingvar, D.H. and Franzen, G. Abnormalities of c e r e -

696 bral blood flow distribution in patients with chronic schizophrenia. Aeta psychiat. Scand., 1974, 50: 425--462. Ingvar, D.tt. and Schwartz, M.S. Blood flow patterns induced in the dominant hemispheres by speech and reading. Brain, 1974, 97: 273--288. dacquy, J., De Koninck, W.J., Piraux, A., Calay, R., Bacq, J., Levy, D. and Noel, G. Cerebral blood flow and quantitative rheoencephalography. Electroenceph, clin. Neurophysiol., 1974, 37: 507-511. Jacquy, J., Wilmotte, J., Piraux, A. and Noel, G. Cerebral blood flow patterns studied by rheoencephalography in schizophrenia. Neuropsychobiology 1976, in press. Kety, S. The cerebral circulation. In: Handbook of physiology, Vol. III. American physiological Society, Washington, 1960: 1751--1759. Lassen, N.A. and Ingvar, D.H. Radioisotopic assessment of regional cerebral blood flow. In: Progress in Nuclear Medicine, Vol. I. Karger, Basel, 1972: 376--409. Nebes, R.D. Hemispheric specialization in commissurotomized man. Psychol. Bull., 1974, 81: 1--14. Piaget, J. Le langage et les op6rations intellectuelles.

J. JACQUY ET AL. In: Probl6mes de psycholinguistique, P.U.F., Paris, 1962: 5--61. Piraux, A., Jacquy, J., Lhoas, J.P., Wilmotte, J. and Noel, G. Regional cerebral blood flow variations in mental alertness. Neuropsychobiology, 6: 335-343. Risberg, K., Halsey, J.H., Wills, E.L. and Wilson, E.M. Hemispheric specialization in normal man studied by bilateral measurements of the regional cerebral blood flow. A study with the 133-Xe inhalation technique. Brain, 1975, 98: 511--524. Samson-Dolfus, Etat actuel de 1'61ectroenc6phalographic clinique IV. L'Electroenc6phalogramme de l'enfant. Rev. Neurol., 1963, 108: 138--141. Wahl, M., Deetjen, P., Thurau, K., Ingvar, D.H. and Lassen, N.A. Micropuncture evaluation of the importance of perivascular PH for the arteriolar diameter on the brain surface. Pfliigers Arch. ges. Physiol., 1970, 311: 152--163. Wilkinson, I.M.S., Bull, J.W.D., Du Boulay, G.H., Marshall, J., Ross Russel, R.W. and Symon, L. Regional blood flow in the normal cerebral hemisphere. J. Neurol. Neurosurg. Psychiat., 1969, 32: 367--378.

Regional cerebral blood flow in children. A rheoencephalographic study of the modifications induced by reading.

Electroencephalography and Clinical Neurophysiology, 1977, 4 2 : 6 9 1 - - 6 9 6 691 © Elsevier/North-Holland Scientific Publishers Ltd. REGIONAL C...
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