Pattern reversal evoked potential amplitudes: Life span changes

Electroencephalography and Clinical Neurophysiology, 1981, 52:429--434

429

Elsevier/North-Holland Scientific Publishers, Ltd.

PATTERN R E V E R S A L EVOKED POTENTIAL AMPLITUDES: LIFE SPAN CHANGES

E.W. SNYDER 2, R.E. DUSTMAN and D.E. SHEARER Veterans Administration Medical Center and University o f Utah College o f Medicine, Salt Lake City, Ut. 84148 (U.S.A.)

(Accepted for publication: July 16, 1981)

Pattern reversal evoked potentials (PREPs) have been useful in the diagnosis of some neurological diseases, primarily multiple sclerosis, and a range of ophthalmological disorders (e.g., Halliday et al. 1973a; Regan 1977; Bodis-Wollner and Yahr 1978; Creel 1979; Carroll et al. 1980). Increased latency of the major positive (P100) c o m p o n e n t is an established and reliable sign of visual system dysfunction. Aging is also associated with PREP wave slowing particularly after age 60 (Asselman et al. 1975; Celesia and Daly 1977; Stockard et al. 1979; Shaw and Cant 1980; Shearer and Dustman 1980; Sokol et al. 1981). Early waves (P50, N65 and P100) are significantly delayed in older subjects but there is some evidence that later waves (N150 and P200) show the reverse effect (Kja~r 1980; Shearer and Dustman 1980). PREP amplitudes have traditionally received less attention than latencies because of their apparent variability and their responsiveness to peripheral visual defect (e.g., Halliday et al. 1972, 1973a,b). However, recent reports have suggested the diagnostic utility of conjoint amplitude/ latency analyses (e.g., Persson and Sachs 1978; Carroll et al. 1980). In general

1 Supported by the Research Service of the Veterans Administration and the National Institute on Aging Grant AG00568. 2 Address correspondence and reprint requests to: Edward W. Snyder, VA Medical Center, Neuropsychology Research (151A), Salt Lake City, Ut. 84148, U.S.A.

decreased PREP amplitudes have been associated clinically with peripheral visual defect and/or a conduction block somewhere between retina and cortex. Studies in our laboratory have shown dramatic age-related changes in the amplitudes of potentials evoked by the onset of diffused flashes (e.g., Dustman et al. 1979). Given these changes and the recent evidence that PREP amplitudes are clinically useful, this paper serves to evaluate normal life-span changes in PREP amplitudes. Latency evaluations (Shearer and Dustman 1980} will be summarized. Analyses of the influence of gender are included since the relationship between sex and evoked potential amplitude has been shown to interact with age (Rodin et al. 1965; Rhodes et al. 1969; Schenkenberg and Dustman 1970; Shagass 1972).

Methods The following is a brief review of the experimental m e t h o d which is described in detail elsewhere (Shearer and Dustman 1980). Subjects

PREPs were recorded from 104 males aged 4--90 years and 33 females aged 6--59 years. All were in good health as determined by interview, personal history questionnaire and, for subjects over 60 years, neurological evaluation. Subjects with visual, cardiovascular or neurological dysfunction were excluded.

0013-4649/81/0000--0000/$02.50 © 1981 Elsevier/North-Holland Scientific Publishers, Ltd.

430

E.W. SNYDER ET AL.

Procedure and apparatus Subjects were seated in a padded chair in a darkened, sound~leadened and electrically shielded room. Disc electrodes were attached to the scalp ('10-20' system) at Oz and Fz for bipolar recording. Stimuli of 51 lux were presented binocularly at a rate of one pattern reversal every 600 msec by a Digitimer stimulator. Sides of alternating black and white squares projected a retinal arc of approximately 70 min. EEG and stimulus pulses accompanying the initiation of pattern reversals were amplified and stored on magnetic tape. The EEG for 250 msec following each stimulus pulse was digitized at a 500/sec rate. Two hundred such sets of digitized values were summed and averaged for each PREP, the typical morphology of which has been previously illustrated (Shearer and Dustman 1980).

Results For males and females combined PREP amplitudes decreased significantly with age (Table I). However, based upon post hoc assessment of mean differences, only the

youngest group differed significantly from older subjects. That is, past mean age 7 years, no significant age-related changes occurred. The largest F ratio occurred for the N65P100 component. Since males and females were not equally represented, single factor analyses of variance (ANOVAs) were used to evaluate age-related changes within each sex (Table II). For females, all 3 waves were significantly attenuated with increasing age. Furthermore, the two youngest female groups differed significantly from one another and from the older groups. Males, on the other hand, showed no significant change in one c o m p o n e n t (P100N150); the only significant changes in the two earlier waves were between the youngest and older subjects. In general, prior to adult years females had larger PREP amplitudes than males. To further evaluate sex differences as a function of age, we separated subjects into two groups, 6--20 years (N = 14) and 21--59 years (N = 19). Females in the younger group had significantly larger amplitudes than agematched males (P50-N65, P < 0.08; N65P100, P < 0.001; P100-N150, P < 0.01). Male-female amplitude differences were not

TABLE I Means, standard deviations (in parentheses), and A N O V A results for amplitudes (in pV) of 3 waves from subjects of both sexes in 8 age groups. Age group

1 2 3 4 5 6 7 8

N

16 20 16 17 16 15 15 22

F ratio (7/129 df) P value Significant mean differences

Mean age

7 14 26 34 45 55 65 76

Waves P50-N65

N65-P100

P100-N150

8.1 (5.6) 4.4 (2.9) 3.5(2.6) 4.3(3.2) 4.2(5.1) 2.4(1.7) 2.0(1.3) 1.7(1.3)

25.9 (11.4) 15.7 (8.8) 12.2 (4.5) 11.8 (7.2) 12.3 (5.7) 13.2 (6.8) 9.2 (4.5) 10.3 (5.5)

25.1 (15.7) 19.9 (12.8) 13.3 (5.6) 13.9 (5.5) 16.9 (6.2) 17.7 (9.3) 15.5 (6.3) 17.7 (9.1)

6.52

8.75

<0.001

<0.001

1 > 2--8

1 > 2--8

2.52 <0.02 1 > 3,4,7

PREP AMPLITUDES

431

TABLE II Means, standard deviations (in parentheses), and ANOVA results for amplitudes (in #V) of 3 PREP waves of males (A) and females (B). Age group

N

Mean age

P50-N65

N65-P100

P100-N150

(A) Males 1 2 3 4 5 6 7 8

9 13 10 9 14 12 15 22

6 14 26 34 45 55 65 76

6.8 3.2 3.2 4.5 3.9 2.2 2.0 1.7 3.2

(5.5) (2.2) (2.7) (4.0) (5.4) (1.6) (1.3) (1.3)

19.1 (9.1) 10.8 (3.1) 11.3 (5.3) 12.2 (8.0) 11.6 (5.7) 12.9 (6.8) 9.2 (4.5) 10.3 (5.5) 2.66

19.1 (12.7) 13.9 (3.6) 12.5 (5.4) 14.6 (6.4) 17.0 (6.6) 17.4 (10.1) 15.5 (6.3) 17.7 (9.1) 0.89

< 0.01 1 > 6--8

< 0.05 1 > 2--8

> 0.1 --

9.8 (5.7) 6.5 (3.0) 3.8 (2.5) 4.0 (2.3) 4.5 (2.6) 3.60

34.7 (7.6) 24.9 (8.7) 13.7 (2.7) 11.3 (6.6) 15.5 (6.0) 14.20

32.9 (16.5) 31.1 (16.3) 14.9 (6.1) 13.1 (4.7) 17.9 (5.0) 4.64

< 0.001

< 0.01

F ratio (7]96 df) P value Significant mean differences (B) Females 1 7 2 7 3 6 4 8 5 5 F ratio (4/28 df) P value Significant mean differences

8 14 26 33 50

< 0.05 1 > 3--5

a p p a r e n t f o r t h e o l d e r subjects. A c o m p a r i s o n of amplitudes for younger and older females {6--20 vs. 2 1 - - 5 9 ) d e m o n s t r a t e d t h a t P R E P s o f t h e y o u n g e r g r o u p w e r e significantly larger than those of the older group (P50-N65, P 0.01; N 6 5 - P 1 0 0 , P ( 0 . 0 0 1 ; P 1 0 0 - N 1 5 0 , P ( 0 . 0 0 1 ) . This age g r o u p i n g did n o t reveal a significant e f f e c t f o r males. A m p l i t u d e c h a n g e s w e r e t y p i c a l l y inversely related to latency changes (Shearer and Dustman 1980). However, the most profound a m p l i t u d e r e d u c t i o n s o c c u r r e d in t h e early y e a r s while l a t e n c y increases w e r e m o s t d r a m a t i c in l a t e r life. Discussion While age-related changes in P R E P amplit u d e s are as d r a m a t i c as c h a n g e s in latencies,

1 > 2--5 2 > 3--5

1 > 3--5 2 > 3--5

the two measures demonstrate some independence. Amplitudes of most components decrease significantly f r o m c h i l d h o o d t o a d o l e s c e n c e (Tables I, II) b u t changes therea f t e r are t y p i c a l l y m i n i m a l . L a t e n c i e s o n t h e o t h e r h a n d increase gradually d u r i n g t h e early y e a r s w i t h o u t b e c o m i n g significantly p r o l o n g e d until t h e fifth or sixth d e c a d e o f life (Shearer and Dustman 1980). Some independ e n c e o f a m p l i t u d e s a n d latencies is, theref o r e , evident; o n e c a n n o t ignore e i t h e r p a r a m e t e r w i t h o u t losing s o m e i n f o r m a t i o n . P R E P a m p l i t u d e s h a v e b e e n u s e d clinically t o i n d e x visual a c u i t y . F o r e x a m p l e , d u r i n g stages o f o p t i c neuritis, b o t h latencies a n d a m p l i t u d e s are reliably altered. H o w e v e r , as t h e neuritis clears a n d a c u i t y r e t u r n s , amplit u d e s increase while latencies r e m a i n prol o n g e d , s o m e t i m e s f o r y e a r s (Halliday et al.

432 1973b; Wilson 1978). Amplitudes are also attenuated when acuity is artificially decreased by defocusing the stimulus (Neetens et al. 1974). The present results indicate t h a t PREP amplitudes can change independently of alterations in visual acuity. That is, while one can support the conclusion that children's acuity matches that of adults (Sokol 1978; Sokol and Dobson 1978), there is certainly reason to reject any suggestion that acuity w o r s e n s to y o u n g adulthood. Nevertheless, PREP amplitudes decreased in a highly significant fashion. The decrease in PREP amplitudes from childhood to adolescence appears to contradict a recent report (Fenwick et al. 1980) of a slight developmental i n c r e a s e in two PREP components. However, Fenwick and associates analyzed year-to-year changes in prepubescent children. Ours was a coarser grained analysis of changes t h r o u g h o u t life. Sex differences in PREP amplitudes are striking but only in preadult years. Females show significantly larger PREPs during childh o o d and adolescence after which the differences are not statistically significant. It is doubtful that sex differences in PREP amplitudes are related to visual acuity; we find no reports of sex differences in visual acuity. Differences in head circumference or brain mass might affect evoked potential amplitudes (e.g., Buchsbaum et al. 1974). However, such anatomical sex differences follow a parallel course during childhood (NCHS Growth Charts 1976) unlike the initial disparity and subsequent convergence of PREP amplitudes. When sex differences in PREP amplitudes are disappearing, i.e., adolescent years (Table II), gross anatomical differences between males and females are becoming more apparent. Sex differences in EEG development are clearly evident. Girls have increased alpha frequency, more 2--5 c/sec EEG and greater photic sensitivity than boys (Schenkenberg and Dustman 1970; Petersen and Eeg-Olofsson 1971). These differences suggest an earlier cerebral maturation in girls. Such a conclusion is supported by the present data.

E.W. SNYDER ET AL. PREP amplitudes indicate that the visual system of preadolescent girls is more responsive than that of similarly aged boys. In fact, Vaccari (1980) reported t h a t the developing female brain has a more efficient catecholamine system than does the male brain. Schafer and McKean (1975) offer convincing evidence that increased availability of monoamines enhances the activity of feature-sensitive neurons in striate and extra-striate cortex. In summary, the results of the present study suggest a large and highly significant PREP amplitude attenuation from childhood to adolescence. Young girls have larger PREPs than do boys but the differences disappear sometime after puberty. These changes have a certain degree of independence from latency changes. Since both latencies and amplitudes provide useful information regarding lifespan changes, evaluation of both measures should enhance the validity of the PREP as a clinical tool.

Summary Pattern reversal evoked potentials (PREPs) were recorded from people whose ages ranged from 4 to 90 years. Dramatic reductions in PREP amplitudes occurred between childhood and adolescence. These changes were most evident in females. Following adolescence there were no significant changes in amplitudes, even to old age. Latencies, on the other hand, have been shown to change most dramatically between adulthood and old age. PREP amplitudes and latencies, therefore, appear to provide different and unique information regarding development and aging. One cannot ignore PREP amplitudes w i t h o u t sacrificing information regarding early development.

PREP AMPLITUDES R6sum6

Amplitude du potentiel dvoqud d l'inversion du damier: modification au cours de la vie Les p o t e n t i e l s ~voqu~s ~ l ' i n v e r s i o n d u d a m i e r ( P E I D ) o n t 6t~ e n r e g i s t r 6 s c h e z des s u j e t s d o n t l'~ge v a r i a i t de 4 h 90 ans. U n e r ~ d u c t i o n c o n s i d e r a b l e de l ' a m p l i t u d e des PEID survient entre l'enfance et l'adolescence. C ' e s t c h e z les f e m m e s q u e ces m o d i f i c a t i o n s s o n t les p l u s ~ v i d e n t e s . A p r ~ s l ' a d o l e s c e n c e , il n ' y a pas de m o d i f i c a t i o n s i g n i f i c a t i v e d ' a m p l i t u d e , m S m e a u x ages avanc~s. Les l a t e n c e s , d ' a u t r e p a r t , c h a n g e n t de la m a n i 6 r e la p l u s m a r q u e e e n t r e l'~ge a d u l t e e t l'~ge avanc6. A i n s i , les a m p l i t u d e s des l a t e n c e s des P E I D semblent fournir une information diff~rente e t u n i q u e en ce q u i c o n c e r n e le d ~ v e l o p p e m e n t e t la s 6 n e s c e n c e . O n ne p e u t pas i g n o r e r les a m p l i t u d e s des P E I D sans s a c r i f i e r l ' i n f o r m a t i o n q u i c o n c e r n e le p r e m i e r d ~ v e l o p p e ment.

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