The visual evoked response to pattern reversal in ‘normal’ 6–11-year-old children

Electroencephalography and Clinical N europhysiology , 1981, 51:49--62

49

© Elsevier/North-Holland Scientific Publishers, Ltd.

THE VISUAL EVOKED RESPONSE TO PATTERN REVERSAL IN 'NORMAL' 6--11-YEAROLD CHILDREN P.B.C. FENWICK, D. BROWN and J. HENNESEY Institute o f Psychiatry, London SE5 8AF, and St. Thomas's Hospital, London SE1 7EH (England)

(Accepted for publication: August 27, 1980)

Visual evoked responses (VEPs) to pattern reversal have now become a standard method of investigating the visual system in a d u l t s (Halliday et al. 1972, 1974; Asselman et al. 1975; Sokol and Bloom 1973; Sokol and Shatterian 1976). However, despite the method's wide acceptance as being valuable in investigating visual functioning, no paper has yet been published establishing norms in 6--11-year~ld children. Considerable work has already been undertaken showing the development of the flash evoked response in children. Dustman et al. (1977), in a review article summing up their former work, point out that 'when recorded from the occiput (O~, O2) the VEP shows a rapid increase in amplitude of most components during early childhood reaching a maximum in 6--8-year~ld children. At this age, the mean amplitude of the VEP was more than twice as large as the VEP amplitude of older age groups. Following this increase there was a decline in amplitude associated with increasing age until ages 13--14 when an abrupt increase in amplitude appeared in components occurring in the first 200 msec. This surge in amplitude during the early teenage years was consistently present.' Callaway and Halliday (1973) studied the VEP in children between the ages of 6--16 again using a flash stimulus, they found that the amplitude of the response peaked at the age of 9. From a multivariate analysis they concluded that the visual evoked potential amplitude to a flash stimulus was not correlated with age.

They did, however, find that some of the latency measurements that they took did correlate with age. This paper describes the maturation with age of the amplitude and latency of the visual evoked response to pattern reversal stimulation in 'normal' children. No attempt has been made to correlate the changes observed with the psychological development of the children measured. This study is purely clinical and is designed to provide norms for use in a clinical department. It was initially decided to investigate the changes with age to full square pattern reversal using the electrode placement and technique of Asselman et al. (1975). However, Fenwick and Turner (1977) and Fenwick and Parry~Jones (1979) have already shown that in adults the amplitude of the pattern reversal visual evoked response varies with the displacement of the pattern stimulus. They also showed that the relationship between the amplitude of the VER and pattern displacement was linear for ~,~~,~¼and full pattern displacement using a 7 mm check (40'). In view of this finding it was decided also to investigate the development of this relationship throughout childhood and to establish whether or not there was a linear relationship at different ages. Method Eighty-four children between the ages of 5 and 11 were obtained from 3 different neigh-

50 b o u r h o o d schools near the city centre. Permission was sought f r om the headmistress and parents and only those children whose parents agreed participated. It was felt t h a t this bias to the sample would n o t significantly alter the results. Teachers rated t he childrens' intellectual functioning, emotional m a t u r i t y and standard o f behaviour on a 4-point scale: average, above, below and low average. Parents completed a questionnaire o f their child's medical history. Abnormalities of the retina were excluded b y examining t he fundus. Visual acuity was measured by Snellen charting and colour perception by Ishihara charting. Recordings were made using silver/silver chloride electrodes applied with collodion at t h e vertex and 5 cm above t h e inion after the m e t h o d o f Asselman et al. (1975). The stimulus was a black and white checkerboard pattern reflected f r o m a moveable mirror o n t o a translucent screen. Electromechanical movem e n t o f t h e mirror pr oduc e d a rapid sideways m o v e m e n t o f the pattern which t o o k a constant 7--7.5 msec whatever t he displacement amplitude. Quarter, half and full square pattern displacements were used; t he full square displacement gave t he impression of pattern reversal. Pattern m o v e m e n t occurred every 1/sec, alternately to left and right. The child was seated 57 cm in f r o n t of t he stimulus screen in a darkened r o o m . The check size was 7 mm (subtending an angle o f 40' at th e retina) and t he screen size 15.4 cm (subtending an angle o f 15 ° 24'). The luminance o f the black squares was 120 candles/ m 2 and that o f the white squares 1500 candles/m 2 . The child was connect ed to a Devices EEG amplifier, with a high f r e q u e n c y cut o f 3 dB d o w n at 250 Hz and a time constant of I sec. T h e o u t p u t f r o m this was fed into a Data Laboratories DL400 averager and microprocessor. The averager was triggered b y a pulse coinciding with pattern m o v e m e n t t o t h e left. 128 pattern movements were averaged per trial. F o u r separate conditions were examined: these were full, half and q u a r t e r dis-

P.B.C. FENWICK ET AL. placements for the right eye, full displacement only for t he left eye. U n f o r t u n a t e l y , the 3 displacement had to be o m i t t e d due to the disproportionate extra time involved. The order o f t he conditions was varied r a n d o m l y . Great care was taken during t he recording to ensure t hat t he child was looking at the fixation point at the centre of the screen, any trials were this did not occur were rejected. The results were plotted on an X-Y plotter and also recorded on cassettes by an ASR Texas Silent 700 Inst rum ent terminal/casette recorder. The latency o f the evoked response was defined after t he m et hod of Halliday et al. (1972) as t he time from pattern m o v e m e n t onset to t he first major positive peak P95. Two amplitude measures were taken, t he first a peak to peak measurement f r o m N65 to P95 similar t o t hat o f Asselman et al. (1975), the second from peak to peak of the P95-N125 component. A routine EEG was recorded using an SLE 8 ~ h a n n e l portable EEG machine and photic stimulation was given using a Devices Photic Stimulator 2182.

Results The older children cooperated well in t he experimental situation but t he 5-year~l ds were excluded f r o m the study after t he first 3 found c o o p e r a t i o n difficult. Several children were excluded due to visual anomalies. Five children who were found to he colour-blind were included in t h e series since Regan (1977) showed t h a t this does not affect the amplit ude o f t he evoked response. Subsequent examination of the wave forms and amplitudes f r o m these children confirmed his finding. T he total n u m b e r of children finally included in t he sample was 73. Table I shows t h e age and sex distributions o f the sample. Our dependence on schools and parents made it impossible to obtain equal numbers in each age group, but t he n u m b e r o f boys and girls over t he whole sample is almost equal.

51

PATTERN VEP IN 'NORMAL' CHILDREN TABLE I Age (years)

Number of children Sex : Male Female

6

7

8

9

10

11

Total

11 4 7

7 5 2

9 3 6

20 11 9

13 5 8

13 7 6

73 35 38

TABLE II

Intelligence Behaviour Emotional maturity

TABLE

Above average

Average

Below average

Low average

26 25 13

37 38 43

8 8 15

2 2 2

III

Visual acuity

6/6 or better 6/7.5 6/9--6/18 Total

No. of children Right eye

Left eye

55 11 5 71

54 10 7 71

Table II shows t h e d i s t r i b u t i o n o f t h e t e a c h e r s ' ratings o f t h e children's intelligence, e m o t i o n a l m a t u r i t y a n d b e h a v i o u r . Schools t e n d e d t o send m o r e ' a b o v e average' t h a n ' b e l o w average' children b u t t h e d i s t r i b u t i o n s are n o t severely s k e w e d and t h e r e are suffic i e n t children in e a c h c a t e g o r y . Table III shows t h e d i s t r i b u t i o n o f visual a c u i t y w i t h i n t h e sample w i t h glasses being w o r n w h e r e necessary. T w o children were n o t t e s t e d b u t had n o r m a l vision. No child had a squint o r a n a m b l y o p i c e y e . All t h e children's E E G s w e r e r a t e d as normal f o r t h e i r age b y a c o n s u l t a n t clinical n e u r o p h y s i o l o g i s t and n o child was p h o t o s e n s i tive w i t h p h o t i c s t i m u l a t i o n . A l t h o u g h a w i d e variety o f e v o k e d r e s p o n s e wave f o r m s were e n c o u n t e r e d , t h e s e did n o t s h o w a n y signifi-

c a n t d i f f e r e n c e s f r o m t h e range in n o r m a l adults and so will n o t b e illustrated. Figs. 1--6 show t h e relationships b e t w e e n p a t t e r n d i s p l a c e m e n t a n d N 6 5 - P 9 5 and P95N 1 2 5 a m p l i t u d e s f o r each age g r o u p . F o r each age t h e best fit regression line is s h o w n d o t t e d . Table IV gives t h e y i n t e r c e p t s , slopes and c o r r e l a t i o n c o e f f i c i e n t s f o r t h e regression lines. T h e regression lines are a g o o d fit t o t h e d a t a e x c e p t t h e c o r r e l a t i o n c o e f f i c i e n t s are n o t significant f o r t h e N65-P95 wave f o r t h e 8-year-olds and t h e P 9 5 - N 1 2 5 wave f o r t h e 6- and 7-year-olds. T h e y i n t e r c e p t s o f t h e regression lines f o r t h e N 6 5 - P 9 5 wave at t h e d i f f e r e n t ages s h o w a wide scatter, with a range f r o m 1.7 t o 6.4 pV: t h e largest values are f o r t h e 8- and 10-yearolds. F o r t h e P 9 5 - N 1 2 5 wave t h e range is o n l y f r o m 2.1 t o 3.2 gV, t h e largest values are for t h e 7- and 8-year-olds. A S t u d e n t t test just s h o w e d a significant d i f f e r e n c e in y i n t e r c e p t b e t w e e n t h e t w o waves N65-P95 m e a n 3.6 # V , S.D. 4.2; P 9 5 - N 1 2 5 , m e a n 2.6 p V , S.D. 3.8 # V (t = 2.0, P = 0.05}, h o w e v e r , t h e d i f f e r e n c e s are n o t significant b e t w e e n age groups. T h e variances o f t h e a m p l i t u d e s o f t h e N 6 5 - P 9 5 and P 9 5 - N 1 2 5 waves at t h e d i f f e r e n t p a t t e r n d i s p l a c e m e n t s are s h o w n in T a b l e V

P.B.C. FENWICK ET AL.

52 TABLE IV Wave

6-yr~tds

N65-P95 P95-N125

7-yr~lds 8-yr-olds 9-yr-olds 10-yr-olds 11-yr-olds

Linear regression y intercept (uv)

Slope

r

P

3.06 2.12 2.21 3.29 6.42 3.18 3.87 2.94 4.68 2.58 1.73 2.17

8.31 4.51 9.57 3.82 7.63 8.73 10.29 6.45 9.48 5.60 13.3 7.51

0.59 0.35 0.52 0.31 0.35 0.47 0.57 0.37 0.54 0.43 0.71 0.54

0.05 NS 0.05 NS NS 0.05 0.05 0.01 0.05 0.05 0.01 0.01

f o r t h e w h o l e g r o u p o f children a n d in T a b l e V I t h e variances are s h o w n s e p a r a t e l y f o r e a c h age. O v e r t h e w h o l e s a m p l e o f c h i l d r e n t h e r e are significant d i f f e r e n c e s in variance b e t w e e n t h e early a n d late waves f o r t h e ½ a n d ¼ disp l a c e m e n t s . T h e o n l y individual age g r o u p s w h i c h s h o w e d significant d i f f e r e n c e s b e t w e e n t h e t w o w a v e s at t h e s a m e p a t t e r n s displacem e n t w e r e t h e 6- a n d 8-year-olds f o r t h e ¼ d i s p l a c e m e n t . This suggested t h a t t h e signifi-

15[

6 years

15

Amplitude10 in )JV

N65-Pg5 ~ _ . .

G

c a n t d i f f e r e n c e s in t h e variance f o r t h e w h o l e s a m p l e w e r e d u e t o d i f f e r e n c e s b e t w e e n age groups. T h e similarity o f t h e variance o f t h e a m p l i t u d e s at e a c h age also i n d i c a t e d t h a t t h e regression lines f o r t h e N 6 5 - P 9 5 a n d P95N 1 2 5 w a v e s f o r e a c h age g r o u p w e r e an equally good estimate of the data. Therefore, t h e d i f f e r e n c e in y i n t e r c e p t s was n o t d u e t o a g r e a t e r s c a t t e r o f a m p l i t u d e values f o r t h e N 6 5 - P 9 5 wave.

- ~-~ P95-N1Z5

1/4 1/2 Pattern displacement

Fig. 1. Mean amplitude for the eleven 6-year-old children in/~V and the standard error o f the mean for the N65-P95 and P95-N125 wave plotted against ¼, ~, 1 and full pattern displacement. The dotted lines are the calculated straight lines fitted to the data for each amplitude.

10 Amplitude

7 years N65-P95 1 .-

1/4 1/2 1 Pattern dispiacemenl Fig. 2. Mean amplitude for the seven 7-year-old children in/~V and the st4mdard error of the mean for the Ne5-P95 and P95~N!25 wave plotted against ¼, ½, and full pattern displacement~ The dotted lines are calcu lated straight lines fitted t o the data for each amplitude.

PATTERN VEP IN ' N O R M A L ' CHILDREN

15

8 yeors

53

15

10 ~N65.pg

5

P95-N125 I0

I0 Amplitude in )JV

Amplitude in juV 5

"'"

~4

112

I

Pottern displacement

Pattern displacement

Fig. 3. Mean amplitude for the nine 8-year-old children in/JV and the standard error of the mean for the N65-P95 and P95-N125 wave plotted against ~, 5, 1 and full pattern displacement. The dotted lines are the calculated straight lines fitted to the data for each amplitude.

Fig. 5. Mean amplitude for the thirteen 10-year-old children in ~V and the standard error of the mean for the N65-P95 and P95-N125 wave plotted against ~, ~-, and full pattern displacement. The dotted lines are the calculated straight lines fitted to the data for each amplitude.

We also l o o k e d at t h e p a t t e r n o f t h e varia n c e s o f t h e a m p l i t u d e s f o r e a c h w a v e at different displacements over the whole group of children ( T a b l e V ) . F o r t h e N 6 5 - P 9 5 w a v e t h e variances are significantly d i f f e r e n t f o r e a c h p a t t e r n d i s p l a c e m e n t . (Full --½, F = 1.5, P < 0 . 0 5 , ~ - - ~ , F = 3.2, P = < 0 . 0 0 0 1 ) f o r t h e P 9 5 - N 1 2 5 a m p l i t u d e s t h e variances f o r t h e

a n d ~1 are significantly smaller ( F = 2.5, P = 0 . 0 0 0 1 ) c o m p a r e d w i t h t h e full d i s p l a c e m e n t b u t t h e ~ a n d ½ are n o t significantly d i f f e r e n t . This suggests t h a t t h e t w o w a v e s are b e h a v i n g d i f f e r e n t l y . W i t h i n age g r o u p s t h e d i f f e r e n c e in variance b e t w e e n d i s p l a c e m e n t s f o r t h e t w o w a v e s is less o b v i o u s . T a b l e V I s h o w s t h e varia n c e s s e p a r a t e l y f o r e a c h age g r o u p a n d T a b l e

15

I0 Amplitude

9 yeors

/~75. 7

11years

p95

15

~.~P95-N125

10 Amplitude in -yV 5

inff

5

114 112

I

Pattern displacement Fig. 4. Mean amplitude for the twenty 9-year~ld children i n / J V and the standard error of the mean for • 1 1 the N65-P95 and P95-N125 wave plotted against ~, and full pattern displacement. The dotted lines are the calculated straight lines fitted to the data for each amplitude.

o

N65-P95 P95- N125 ..:;

1/4 1 Pattern displacement

Fig. 6. Mean amplitude for the thirteen 11-year-old children in/~V and the standard error of the mean for I 1 the N65-P95 and P95-N125 wave plotted against ~, ~, and full pattern displacement. The dotted lines are the calculated straight lines fitted to the data for each amplitude.

54

P.B.C. F E N W I C K ET AL

TABLE V Variance

Left eye full d i s p l a c e m e n t Right eye full d i s p l a c e m e n t Right eye 1/~ d i s p l a c e m e n t Right eye % d i s p l a c e m e n t

N65-P95

P95-N125

F

P

34.2 26.5 18.3 57.3

31.0 31.4 12.4 12.6

1.1 1.2 1.5 4.0

NS NS 0.05 0.000

TABLE VI Variance (age)

Full

N65-P95 P95-N125 N65-P95 P95-N125 N65-P95 P95-N125

½ ¼

6

7

8

9

10

11

14.1 12.7 13.9 12.9 10.3 2.6

47.2 30.9 21.5 16.2 13.9 18.1

70.4 69.9 24.6 56.2 37.6 10.4

35.6 39.8 21.3 20.1 12.3 21.9

36.5 22.9 1.9.0 14.0 13.2 5.4

32.5 27.1 15.3 8.6 7.1 7.8

T A B L E VII Age N65-P95

P95-N125

6

7

8

9

10

11

6

7

8

9

10

11

Full ½

NS

NS

NS

NS

NS

NS

NS

NS

NS

NS

NS

***

Full ¼

NS

NS

NS

**

**

***

***

NS

***

NS

***

***

½ 'h

NS

NS

NS

***

NS

NS

**

NS

***

NS

NS

NS

Significance: * P < 0.05; ** P < 0.025; * * * P < 0:01.

T A B L E VIII Wave

Eye

Amplitude (pV)

S.D.

t test L V R correlation L V R

Significance

N65-P95

Left Right Left Right Left Right

13.34 13.55 8.4 8.9 102.85 m s e c 102.79 m s e e

5.8 6.1 5.6 5.6 5.3 5.2

t r t r t r

NS P < 0.01 NS P < 0.01 NS P < 0.1

P95-N125 Latency

--- 0.51 -- 0.82 = 1.13 - 0.83 = 0.12 = 0.64

PATTERN VEP IN 'NORMAL' CHILDREN

15

Meanamplitudeplottedagainstage /

I0 Amplitude in )JV 5

"5-P95

/

/

~

55 20

Full square

15 . ~

~'2 squar~

10 Amplitude in ~V

I"4 square

7

8

9

10

MeanampLitudepLottedagoins! ~je P95-N125 ~ ~---~ ~

5

Flesh [~l[ewoy] j _ Full square 1/2 square ~/4 square

8 ~1 lb 1'1 Age in years Fig. 8. Mean amplitude for the fight eye at each age

11

Age in years

Fig. 7. Mean amplitude for the right eye at each age of the N65-P95 wave plotted against age for the full, z and 41-pattern displacement.

of the P95-N125 wave plotted against age for the full, and ~ pattern displacement.

VII shows the significant differences in variance between displacements. Fig. 7 shows the change of the N65-P95 amplitude with age for the right eye only, plotted separately for each displacement. For the full pattern displacement there appears to be a gradual increase in amplitude with age, although this was not found to be significant using a Student t test. This trend is absent for the -~ square displacement, while the -14square displacement shows a completely different pattern, rising markedly between 7 and 8 years (t = 2.35, P = 0.04) and f~|ling again between 8 and 9 years (t = 2 . 4 , P = 0.02).

Fig. 8 shows the change with age of the P95-N125 amplitude for different displacements together with the curve for flash stimulation of a group of similar aged children reproduced from Callaway and Halliday (1973). The curves for flash and for full pattern displacement are very similar. Student t tests revealed no significant differences in amplitudes for any of the pattern displacements between age groups. Fig. 9 shows the changes in latency with age for the right eye. For the full pattern displacement there is a gradual decrease in latency from age 6 to 8 which then levels off

II},t w.'q m] Iozi

Full I~

displacement

Latency in

msecs I01, IOO'

IQ2 Hit

7

I

i

Age in years

,e

i,

Fig. 9. Mean duration of the latency of the P95 wave for full, half and quarter pattern displacements is plotted against age.

56

P.B.C. F E N W I C K E T A L .

T A B L E IX Full p a t t e r n d i s p l a c e m e n t N65-P95 Full

'/2 p a t t e r n

P95-N125

Latency

N65~95 P95-N125 La~ncy

1.000000 0 . 6 0 8 8 5 2 ** 0.065897

1.000000 --0.037729

½

N65-P95 P95-N125 La~ncy

0 . 7 3 8 9 4 4 ** 0 . 4 0 0 6 2 4 ** 0.000978

0.440669 0 . 5 6 5 5 1 9 ** --0.044328

0.141636 --0.085461 0 . 4 1 6 8 7 8 **

¼

N65-P95 P95-N125 Latency

0.275523 * 0 . 5 0 8 7 9 8 ** --0.034312

0.268631 * 0 . 8 6 0 3 8 0 ** --0.116778

--0.158677 0.084090 0.280690

N65-P95

1.000000 1.000000 0 . 5 0 2 7 3 1 ** 0.186063 0.106852 0 . 4 3 8 4 0 8 ** --0.062487

Significance * = 0 . 0 5 ; ** = 0.01.

from 8 to 11. For the ~ square displacement there is a marked decrease between 7 and 8 followed by a gradual rise. For the ~1 square displacement a rise between 7 and 8 is followed by a gradual fall. None of these agerelated changes were significant using a t test, but the trends across age were quite d i f f e r e n t for the different displacements. Table VIII shows the results of a comparison of the right and left eye for the P95 latency and the amplitudes of both waves for full displacement over the whole sample. In each case the correlation between the eyes is high and the difference non-significant. The variances of the amplitudes for t h e whole sample are shown in Table V. Again there is no significant difference in variance between the eyes although for N65-P95 F = 1,3 and just fails significance. Table IX shows the correlations calculated for all the children between the N65-P95 amplitude, the P95-N125 amplitude, and the P95 latency for each pattern displacement. Not surprisingly, the amplitudes of the N65-P95 and P95-N125 wave at the same pattern displacement were significantly correlated. For full r = 0.61, P < 0.01; for 21r = 0.5, P < 0 . 0 1 and for ~r = 0.34, P < 0.01. The correlations decreased with decreasing displacement. Correlations between N65-P95 amplitude

at different displacements are also shown. The amplitude for the full displacement is highly correlated with that for ½ displacement, r = 0.73, P <~ 0.01, but less so for the ~ displacement, r = 0.28, P < 0.05; ~and ~ displacements were n o t significantly correlated r = 0.11, P-NS. The picture for the P95-N125 wave was quite different as the amplitudes for all 3 displacements were highly correlated (full-half, r = 0.57, P ~ 0.01; full-~, r = 0.86, P < 0.01; ~,r=O.55, P<~ 0.01). The latency for the full square displacement was correlated with t h a t for the 1 square displacement r = 0 . 4 5 , P < 0.01 and for the 1square r = 0.28, P < 0.05. ¼ and ½ square latencies were not significantly correlated. The only significant correlation between latency and amplitude was a negative correlation for the N65-P95 wave to ~ square displacement, r = --0.35, P < 0.01. This showed that as N65-P95 amplitude diminished the P95 latency increased. Multivariate analysis of variance was carried out on the University of L o n d o n Computer using a standard programme distributed by the National Educational Resources Inc., Ann Arbour, Mich. The means and the linear and quadratic trends for latency and amplitude across different displacements were calculated for each age together with the trends across

P A T T E R N V E P IN ' N O R M A L ' C H I L D R E N

1A pattern displacement

displacement P95-N125

Latency

1.000000 -0.109053

1.000000

0.149033 0 . 5 5 3 7 6 8 ** -0.144562

57

--0.224090 -0.108870 0.245127

N65-P95

P95-N125

1.000000 0 . 3 3 9 2 0 7 ** - 0 . 3 5 5 7 0 8 **

ages for each displacement. The main effects and interactions of the variables o f displacement, age, sex and eye were obtained. The results of this analysis are shown in Table X. Both the mean displacement and linear displacement terms are highly significant (P = 0.0001) for b o t h the N65-P95 and P95-N125

1.000000 --0.075273

Latency

1.000000

amplitudes. This confirms that n o t only are the amplitudes significantly affected b y the size o f the pattern displacement, b u t that the relationship of pattern displacement to amplit u d e over the whole sample of children is linear. The analysis also showed that once the variance due to the linear term was sub-

TABLE X A n a l y s i s o f variance

Age Sex Age × sex Subjects within groups Displacement D i s p l a c e m e n t × age D i s p l a c e m e n t x sex D i s p l a c e m e n t x age x sex Displacement x subject L i n e a r age L i n e a r age × sex Linear displacement L i n e a r d i s p l a c e m e n t x linear age L i n e a r d i s p l a c e m e n t x q u a d r a t i c age L i n e a r d i s p l a c e m e n t x linear age x sex Sex (for left e y e o n l y ) Age x sex × e y e * = Statistically significant.

N65-P95

P95-N125

Latency

P NS NS NS NS 0.0001 * NS NS NS NS NS NS 0.0001 * 0.0048 * NS NS NS 0.0120 *

P NS NS NS NS 0.0001 * NS NS NS NS NS NS 0.0001 * NS NS NS NS NS

P NS NS NS NS 0.0001 NS NS NS NS NS NS 0.0239 NS 0.0105 NS 0.0102 NS

*

* * *

58

P.B.C. FENWICK ET AL.

-

regression

14 12

,." N65.P95

Slope 10 ~

tle msec b

i

~oo 6

2 6 7 8 9 10 11 Age ~n years. Fig. 10. The amplitude of the slope of the regression line for the P95-N125 and N65-P95 wave fitted across displacements for each age group of children is plotted against age. This graph shows clearly the relationship between age and slope.

tracted, the residual variance was non,significant thus a simple regression line gave a good fit to the data. For the N65-P95 amplitude, the linear trend across displacements interacts with a linear trend across age (P = 0.005), thus the slope of the regression lines, of amplitude against displacement, changes systematically with age. This can be seen in Fig. 10 where the slope of the regression line has been plotted against age. There is also a complex interaction for N65-P95 amplitude between age, sex and eye (P = 0.01). For the latencies both displacement (P =

- girls boys

pgs_N125

4 """ '--7 /

Latency - r ,~,ht eye

\

~'--~

........:

7 8 9 !0 ;! Age in years

Fig. 12. The latency o f the P95 wave is plotted for the right eye of the boys ( s o l i d ) a n d the girls ( d o t t e d ) at each age. There is no clear relationship for the right eye b e t w e e n latency and sex.

0.0001) and linear displacement (P= 0.02) are significant. There is also a complex interaction of linear displacement with quadratic age (P = 0 . 0 1 ) and an interesting effect of sex on latency for the left eye only. Further study showed that the effect of sex on latency was due to slightly longer latencies for the boys, mean 104 msec, S.D. 5.64 msec, than for the girls, mean 101.6 msec, S~D. 4.47, but that the difference was not significant using a Student t test (t = 0.01, NS). This failure of the t test to reach significance is due to the wide variance and the inclusion of the older children (see Figs. 11 and 1 2 ) a s the latency change is most pronounced for the younger children.

Discussion 11[ " ,

Lotmcy- left eye

msec

I0~ i / ,

,,

--

girls

i i

1001

1 ~ 9 fo 1i Age in years

Fig. 11. The latency of the P95 wave is plotted for the left eye of the boys (solid) and the girls(dotted) at each age. The Younger male children s h o w a significantly longer latency which shortens with age to match that of the girlsby the age of 10.

The results of this study are interesting. They confirm for children the relationship between VER amplitudes and fractional pattern displacement already shown for adults b y Fenwick and Turner (1977) for the P95N125. They also show interesting age-related changes in the belmviour of both the amplitude and latency measures. The sample of children examined suffers from the disadvantage of not being randomly selected and thus not truly representative of the London population. However, the 3

PATTERN VEP IN 'NORMAL' CHILDREN schools that t o o k part in the study each had a different social class mix of children and taken together t h e y were representative of the schools in the district from which the hospital drew its patients. It is clear from the results that the N65-P95 and the P95-N125 amplitudes behave quite differently. The N65-P95 wave was always of higher amplitude than the corresponding P95N125 wave for the same displacement and age. Changes in the amplitude of these waves across age were also different. Whereas the N65-P95 amplitude to full displacement showed a gradual, b u t non-significant increase across the entire age range the P95-N125 showed a marked rise in amplitude f o r the 8- and 9-year~ld children, returning almost to the previous level at the age of 10. This rise was not significant using a t test because of the very wide variance, b u t there is no d o u b t that it would be significant had more subjects been measured. This change in amplitude with age is very similar to that published b y Callaway and Halliday (1973) for a group of children of similar age b u t using a flash stimulus. The difference in the behaviour of the N65P95 and P95-N125 waves suggests that they may reflect different underlying neural mechanisms with different rates of maturation. Interesting differences b e t w e e n the t w o waves also emerge from studying the variance of their amplitudes. For the P95-N125 wave the variance shows a similar trend across the ~ and full square displacements to that found for the same wave in a group of adults (Fenwick and Turner 1977) using the same size pattern, b u t a lower luminance. Variances for these children were ¼, 12.6; -~, 12.4; full, 31.4 as against ¼, 2.4, ~, ' 2.3 and full,'18.3 for the adults. In this and the previous study the variance is much larger for the full displacement than for ' and ½, an F test b e t w e e n full and half is significant. This suggests that despite the much larger variance of the amplitude in the children, there are constant relationships between the variance o f the different displacements which are preserved into adult-

59 hood. A fuller picture of these relationships emerged from the Fenwick and Turner study (1977) where the ¼ square displacement was included. In that study the ¼ and full displacements formed a pair with equivalent variance as did the 1 and ½ square displacements in b o t h studies. They suggested that each pair of displacements m a y involve a different underlying generation mechanism and put forward a model to account for the differences. For the N65-P95 wave the picture is quite different. The difference in amplitude variance between full and ~ is smaller and h o t quite significant. Variance for the quarter square displacement is higher than for any other displacement and differs significantly from them. Comparing Tables V and VI and Fig. 7 it is evident that this is due to age differences in amplitude particularly for the 8- and 9-year-old children since the variance within age groups is relatively low. The amplitude of the N65-P95 wave at the 41- square displacement for all the children shows a poor correlation with the N65-P95 amplitude at the ~ square displacement and with the 1 square P95-N125 measure. These low correlations show that the ¼ square N65P95 measure is showing variations which are n o t found in the other measures. A possible explanation follows from our impression that the amplitude of the N65-P95 wave is sensitive to changes in .attention. This fluctuation in attention would have a disproportionate effect on the ¼ pattern displacement where the generated amplitudes are close to the noise level. Alternatively, it may be that the capacity of the visual system to generate this wave varies b e t w e e n ages. The N65-P95 amplitude to ¼ displacement is also the only amplitude measure which correlates significantly with P95 latency, r = --0.36. The correlation is negative so ttm P95 latencies increase as the N65-P95 amplitudes decrease. The latter finding could be explained b y the assumption that small stimulus displacements such as a ¼ square affect the latency and amplitude of the response in the

60 same way that t h e y are affected by luminance. Halliday et al. (1974)have shown that the latency of the P95 wave is very sensitive to the brightness of the pattern and lengthens with a low luminance. The reduction in latency saturates at a relatively low luminance but the amplitude increases with luminance over a larger range. Thus a negative correlation between latency and amplitude will occur at low luminances. The negative correlation could thus be explained if small pattern displacements had a similar effect on latency and amplitude, but saturated at around the ¼ square displacement so that no shortening o f latency occurs for larger displacements. The latency at the 1 square displacement would then be dependent on these saturation curves. The low correlation could be explained by the saturation curves being different for each child because o f physiological or psychological factors, If this explanation was: correct one might expect a longer mean latency for the ¼ square compared with the larger displace•ments. This was not found as there were no significant differences between latencies for the various pattern displacements. The same process cannot be invoked to explain the previously mentioned age-related changes in the N65-P95 amplitude to a ~ square, as the mean latency is longest, although n o t significantly so, and the amplitude highest at age 8, while a shorter latency would be predicted if saturation occurred earlier at this age. Further evidence for a maturation process for the N65,P95 wave comes from the analysis o f variance. There is a significant interaction of linear displacement with linear age. Again this could be due to developmental changes, either specific to the visual system or possibly in the attention mechanisms. There are no significant changes with age in the P95-N125 wave. As previously mentioned, the linear relationship between amplitude and pattern displacement for the P95-N125 wave shown for adults by Fenwick and Turner (1977) has been confirmed for children, this relationship also holds true in this study for the N65-P95 wave as well.

P.B.C. FENWICK ET AL. Our study also shows significant effects of displacement size on latency as there is a significant linear trend for latency for all the children across displacement (Table VII). However, the exact relationship is difficult to untangle because of complex changes in this trend across different ages (linear displacement × quadratic age, P < 0.01). From the grand means (full 102.4 msec, ~1 102.7 msec, 1 101.1 msec) the trend appears to be towards a shorter latency for the small displacement although none of these differences is significant using a Student t test. In the Fenwick and Turner {1977) study full square displacement had the longest latency. Perhaps this was not seen in the present study because a greater luminance was used. Latency as shown by the analysis of variance also shows another interesting feature not related to age although Figs. 11 and 12 show that the effect is maximum for the younger children. Latency for the left eye is significantly longer for the boys than for the girls. The latencies for both eyes in the girls and the right eye in the boys were comparable. Cobb et al. (1967) have described the suppression of the amplitude of the visual evoked response in the non~lominant eye to pattern reversal during binocular rivalry, thus showing a clear relationship between eye dominance and amplitude. Arden et al. (1974) and Meyles and Mulholland (1980) showed changes in latency for the amblyopic or non-dominant eye of children and adults. These two studies taken together emphasise the sensitivity of the visual evoked response using a pattern reversal stimulus to slight changes in the dominance of the eye from which the VER is being recorded. Differences in eye dominance between boys and girls could thus account for the differences in latency we found between the two sexes. Unfortunately, no handedness questionnaires were given to the children, although t h e y were asked if t h e y were left or right handed. From t h e replies the majority were right handed; there also appeared to be no difference in handedness between boys and girls,

PA TT ER N VEP IN ' N O R M A L ' CHILDREN

implying no difference in cerebral or eye dominance. This suggests t h a t the sample of children were mainly right eye d o m i n a n t , although rivalry could lead to changes in functional eye dominance at the time o f the test. There is some evidence t h a t girls in the 6--11 age range are significantly faster than boys on some cognitive tasks (Fairweather and H u t t 1972). Perhaps better attention in the girls leads to less suppression of the nond o m i n a n t eye. If this is the explanation for our latency differences it is puzzling t h a t no clearly associated amplitude differences have emerged. However, there is also a complex interaction between age, sex and eye in relation to N65-P95 amplitude which could be explained on the eye
Summary The visual evoked response to a 7 m m (40') check using a pattern reversal stimulus was measured in 73 normal children, aged 6--11. Full pattern displacement for the right and left eye and ¼ and ½ pattern displacement for the right eye were studied. The amplitudes of

61

the N65-P95 and P95-N125 wave, together with the P95 latency, were measured. Analysis of the data showed t h a t there was no clear relationship between the mean amplit u d e or latency of the evoked response and age. However, significant changes were found between linear displacement and linear age for the N65-P95 wave and there was a complex interaction for the same wave between age, sex and eye. There was a significant difference in latencies between right and left eye between the boys and the girls, with the boys having longer latencies. There are thus both age- and sex-related differences in the amplit u d e and latency of the N65-P95 wave in 6--11-year-old children.

R~sum~ Rdponse visuelle dvoqude au renversement d'un damier chez des enfants normaux dgds de 6--11 ans La r~ponse visuelle ~voqu~e par la rotation d ' u n damier de 7 m m (40') a ~t~ mesur~e chez 73 enfants normaux ~g~s de 6--11 ans. Ont ~t~ ~tudi~es, la rotation complete du damier pour chacun des deux yeux, des rotations de 1 quart et de 1 demi pour l'oeil droit. L'amplitude des ondes N65-P95 et P95-N125 avec la latence de P95 o n t ~t~ mesur~es. L'analyse des donn~es montre qu'il n ' y avait pas de relations pr~cises entre l'amplitude m o y e n n e ou la latence de la r~ponse ~voqu~e avec l'~ge. Cependant, des relations lin~aires significatires o n t ~t~ trouv~es entre le d~placement et l'~ge pour l'onde N65-P95, et il y avait une relation complexe entre cette m~me onde et l'~ge, le sexe et l'oeil considerS. I1 y avait une diffdrence significative dans les latences entre oeil droit et oeil gauche, et entre garqons et flues, avec des latences plus longues pour les garqons. Ainsi, il y a des differences li~es l'~ge et au sexe dans l'amplitude et la latence de l'onde N65-P95 chez les enfants fig,s de 6--11 ans.

62 We would like to thank St. Thomas's Hospital and the Westminster Hospital Endowment Funds for their financial support of the project. We are also greatly indebted to the Headmistresses of the schools and the parents of the children involved in the study. Our thanks also go to Miss J. Shine for her technical assistance and to Miss N. West, Miss D. Lee-Woolf, Mrs. T. Chandler and Mrs. B. Cook for typing and preparation of the manuscript, and Miss S. Campbell for preparing the diagrams.

References Arden, G.B., Barnard, W.M. and Mushin, A.S. Visual evoked responses in amblyopia. Brit. J. Ophthalmol., 1974, 58: 183--192. Asselman, P., Chadwick, D.W. and Marsden, C.D. Visual evoked responses in the diagnosis and management of patients suspected of multiple sclerosis. Brain, 1975, 98: 261--282. Callaway, E. and Halliday, R.A. Evoked potential variability: effects of age, amplitude and methods of measurement. Electroenceph. clin. Neurophysiol., 1973, 34: 125--133. Cobb, W.A., Ettlinger, G. and Morton, H.B. Visual evoked potentials in binocular rivalry. Electroenceph. clin. Neurophysiol., 1967, Suppl. 26: 100-107. Dustman, R.E., Schenkenberg, T., Lewis, E.G. and Beck, E.C. The cerebral evoked potential: life-span changes and twin studies. In: J.E. Desmedt (Ed.), Visual Evoked Potentials in Man, New Developments. Clarendon Press, Oxford, 1977: 363--377. Falrweather, H. and Hutt, S.J. Sex differences in a perceptual-motor skill in children. In: C. Ounsted

P.B.C. FENWlCK ET AL. and D.C. Taylor (Eds.), Gender Differences: their Ontogeny and Significance. Churchill-Livingstone, Edinburgh, 1972: 159--175. Fenwick, P.B.C. and Parry-Jones, N.O. Coloured pattern displacement anti VEP amplitude. Electroenceph. clin. Neurophysiol., 1979, 46: 49--57. Fenwick, P.B.C. and Turner, C. Relationship between amplitude of pattern displacement and visual evoked potentials. Electroenceph. clin. Neurophysiol., 1977, 43: 74--78. Halliday, A.M., McDonald, W.I. and Mushin. J. Delayed visual evoked responses in optic neuritis. Lancet, 1972, i: 982--985. Halliday, A.M., McDonald, W.I. and Mushin, J. The dissociation of amplitude and latency changes in the pattern-evoked response following optic neuritis. Electroenceph. clin. Neurophysiol., 1974, 36: 218. Meyles, W.P.M. and Mulholland, W.V. The response to pattern reversal in amblyopia. In: C. Barker (Ed.), Evoked Potentials. MTP Press, Lancaster, 1980: 243. Regan, D. Evoked potential indications of the processing of pattern, colour and depth information. In: J.E. Desmedt (Ed.), Visual Evoked Potentials in Man New Developments. Clarendon Press. Oxford, 1977: 234--249. Sokol, S. and Bloom B. Visually evoked cortical responses of amblyopias to a spatially alternating stimulus. Invest. Ophthal., 1973, 12: 936--939. Sokol, S. and Shatterian, E.T. The pattern evoked cortical potential in amblyopia as an index of visual function. In: S. Moore, J. Mein and L. Stockbridge (Eds.), Orthoptics, Past, Present, Future. Symposia Specialists, Miami, Fla., 1976 : 59-67.