- Email: [email protected]
Monocular pattern-shift visual evoked potentials in hemispheric strokes
Electroencephalography and cfinical Neurophysiology, 1984, 58:205-210 Elsevier Scientific Publishers Ireland, Ltd.
205
M O N O C U L A R PATYERN-SHIFT VISUAL EVOKED P O T E N T I A L S IN H E M I S P H E R I C STROKES t
NARAYAN P. VERMA 2, KENNETH A. KOOI and JOHN GILROY Holden Laboratory of Clinical Neurophysiology, Wayne State University School of Medicine, Harper-Grace Hospitals, Detroit, All 48201 (U.S.A.) (Accepted for publication: February 15, 1984)
Monocular pattern-shift visual evoked potentials (PSVEPs) have been studied in m a n y neurological disorders including multiple sclerosis and other demyelinating diseases (Halliday et al. 1973; Chiappa 1980), spinocerebellar degenerations (Carroll et al. 1980), pernicious anemia (Troncoso et al. 1979), sarcoidosis (Streletz et al. 1981), Parkinson's disease (Bodis-WoUner and Yahr 1978), transverse myelitis (Ropper et al. 1982), and m a n y others (Chiappa and Ropper 1982), as a measure of functioning of the anterior visual pathways. Although alterations of the PSVEP have been reported in known ischemic optic neuritis (Wilson 1978; Halliday and Mushin 1980), and in stroke associated with neck trauma (Robertson and Feldman 1980), their occurrence in association with hemispheric strokes has not been explored systematically. The study reported here is designed to determine if a significant association exists, and, if so, to assess the nature and extent of changes.
Material and Methods
Three groups of subjects were studied. Relevant group characteristics are shown in Table I. The first group, henceforth to be referred to as the stroke group, was comprised of 33 subjects with neurologic evidence of unilateral non-hemorrhagic strokes. Twenty-two had left hemispheric 1 Presented in part at the American EEG Society meeting in New Orleans, October 1983. 2 Address requests for reprints to: N.P. Verma, M.D., Dept. of Neurology-127, V.A.M.C., Allen Park, MI 48101, U.S.A.
strokes, and 11, right. Twenty-two had 4-vessel cerebral arteriographic studies. Of these, 17 had significant stenosis or complete occlusion of the appropriate internal carotid artery; 6 had additional significant stenosis of the contralateral internal carotid artery. Twenty-three had PSVEP studies during hospitalization for a recent stroke, while the remaining 10 were studied a few months to several years after an earlier stroke. The second group, to be referred to as control group I, comprised of 21 age- and sex-matched patients with non-specific complaints such as headache, dizziness and blurring of vision, a normal neurologic examination, and no recent or remote stroke. The incidences of diabetes mellitus, hypertension and heart disease in the stroke group and control group I were not significantly different. The third group, to be called control group II, consisted of 21 ageand sex-matched elderly healthy community volunteers. Subjects with history of cataracts, other media opacities, glaucoma or symptomatic retinal lesions were not considered or included in any of the 3 study groups. In addition, all subjects in each group had a normal ocular and fundoscopic exarnination other than mild hypertensive changes. As the study involved the assessment of anterior visual pathways and utilized monocular full-field stimulation, patients with homonymous visual field defects were not excluded. Subjects who used glasses wore them during the visual acuity determination and the PSVEP procedure. The visual acuity was determined using the Snellen's chart from a distance of 20 feet. Goldplated cup electrodes were attached to the scalp in midoccipital (Oz), left and right occipital (01 and
0013-4649/84/$03.00 © 1984 Elsevier Scientific Publishers Ireland, Ltd.
N.P. VERMA ET AL.
206 TABLE I Characteristics of patients and normal study groups. Group
No.
Age range (years)
Mean age (years)
M/F
Hypertension
Diabetes mellitus
Heart disease
Stroke group Patient controls (control group I) Normal controls (control group II)
33 21 21
50-79 50-77 50-75
62.1 61.9 61.0
23/10 14/7 14/7
14 7 0
6 3 0
6 6 0
0 2) a n d m i d c e n t r a l (Cz) areas, as well as to b o t h e a r l o b e s using the c o l l o d i o n technique. Skin-elect r o d e interface i m p e d a n c e s were k e p t less t h a n 5000 ~ . A n a l t e r n a t i n g b l a c k - a n d - w h i t e p a t t e r n h a v i n g a check-size of 36' was g e n e r a t e d on a television screen at a f r e q u e n c y of 1.88 c / s e c . S t i m u l u s l u m i n a n c e for white squares was 225.5 c d / m 2 and, for b l a c k squares, 12.7 c d / m 2. Sixty-four individual responses derived from m o n o c u l a r s t i m u l a t i o n o f either eye were averaged, each for test, a n d for retest, e m p l o y i n g a N i c o l e t 1170 r e s p o n s e averager, viewing d i s t a n c e b e i n g 1 m a n d n o m i n a l l i n e a r b a n d p a s s filter width, 1 - 3 5 c / s e c . T h e subjects were o b s e r v e d for consistency o f gaze t h r o u g h o u t the p e r i o d of d a t a collection. A n E E G tracing was r e c o r d e d t h r o u g h o u t the p r o c e d u r e to ensure alertness a n d signal reliability. F u n c t i o n i n g of the a n t e r i o r visual p a t h w a y s was assessed b y m e a s u r i n g the P100 latencies, P100 a m p l i t u d e s , i n t e r o c u l a r P100 l a t e n c y differences a n d i n t e r o c u l a r P100 a m p l i t u d e ratios (small P 1 0 0 / l a r g e P100) at the m i d o c c i p i t a l - j o i n e d ears derivation, using d a t a d e r i v e d f r o m g r a n d averages o f 128 responses o n each subject. T h e statistical analyses were m a d e using Stud e n t ' s t test, the chi square test a n d correlative analytical methods.
different f r o m that of c o n t r o l g r o u p I o r II ( T a b l e III). A d d i t i o n a l l y , the m e a n P100 l a t e n c y on ocular s t i m u l a t i o n ipsilateral to the side o f cerebral i n f a r c t i o n was significantly longer t h a n that on right or left eye s t i m u l a t i o n in c o n t r o l g r o u p I or II (Fig. 1). T h e m e a n P100 latency on o c u l a r s t i m u l a t i o n c o n t r a l a t e r a l to the side of the infarction was similarly, b u t less significantly, longer t h a n that o n right o r left o c u l a r s t i m u l a t i o n in c o n t r o l g r o u p I o r II (Fig. 1). O n the basis o f n o r m a l limits ( m e a n _+ 3 S.D.) d e t e r m i n e d from n o r m a l volunteers (control g r o u p II), 15 of 33 stroke subjects h a d a b n o r m a l PSVEPs c o m p a r e d to n o n e of 21 subjects in c o n t r o l g r o u p I ( P = 0.002, chi square test), when all 3 variables, viz., l a t e n c y differences, a m p l i t u d e alterations, a n d l a t e n c y p r o l o n g a t i o n , were c o n s i d e r e d together (Figs. 2 a n d 3). I n t r a g r o u p analyses, p a r t l y d e p i c t e d in T a b l e IV, d i d n o t reveal a n y significant differences in s t r o k e subjects with a n d w i t h o u t a m a u r o s i s fugax, in those with visual acuity 2 0 / 3 0 or b e t t e r a n d those with visual acuity 2 0 / 4 0 o r worse, a n d those with recent a n d r e m o t e event. T h e m e a n P100 l a t e n c y on o c u l a r s t i m u l a t i o n ipsilateral to the i n f a r c t i o n was significantly longer t h a n that on
TABLE II R ~
Mean interocular P100 latency differences and standard deviations of 3 study groups.
I n t e r g r o u p c o m p a r i s o n s are d e p i c t e d in T a b l e s II a n d III, a n d Fig. 1. T h e m e a n i n t e r o c u l a r P100 l a t e n c y difference in the s t r o k e g r o u p was signific a n t l y greater t h a n that of c o n t r o l g r o u p I or | I ( T a b l e II). T h e m e a n i n t e r o c u l a r P100 a m p l i t u d e r a t i o in the stroke group, also, was significantly
Group
Mean difference + S.D.
Significance of difference vs. stroke group
Stroke group Control group I Control group II
5.0 + 4.6 2.2 + 1.6 2.0 + 1.2
P = 0.009 P = 0.005
207
M O N O C U L A R PSVEPs IN HEMISPHERIC STROKES TABLE IlI Mean interocular P100 amplitude ratios and standard deviations of 3 study groups. Group
Stroke group Control group I Control group II
Mean ratio 5: S.D.
Significance of difference vs. stroke group
0.72 + 0.21 0.87 5:0.13 0.85 + 0.15
P = 0.009 P = 0.016
Control group I (right eye} 106, tl + 5 . 6 msec
• I • ! Cont~*ol g r o u p II (right eye) 105.2 + q. 9 msec ~
"~
.....
stimulation contralateral . , to s i d e o f i n f a r c t 112.2 + 1 t . 3 msec -
p=O. 009
p=O. 016 - -
L
i [
20/25
I', I
0
P100 l a t e n c y on o c u l a r p=0.0~'9 stimulation ipsilateral to side o f i n f a r c t s ./'/" l ) 11t1.6 + 1 2 , 2 m s e c ( ~ p=0.0q
Soo
V _A 20/25
i
Control group I ( l e f t eye) 106.7 +_ 6.it msec 0.006
p=0.03
Y E _ E R ~
•
50
I[[
I
I
msec
Fig. 2. Sixty-four-year-old female with right cerebral infarction. The mean P100 latency on right ocular stimulation is significantly longer than that on left ocular stimulation. The tracing is recorded with a midoccipital derivation referred to interconnected ears with relative positivity at the occipital electrode producing a downward deflection.
EYE R ~
VA 20/25
L ~
20/30
p 01o03 ' ! C o n t r o l g r o u p II ( l e f t eye} 105.8 +_ ~. 6 rnsec
Fig. 1. Mean P100 latencies on ocular stimulation ipsilateral and contralateral to the side of cerebral infarction, and comparison thereof with the same on right or left eye stimulation in control groups I and II. The broken lines indicate the levels of significance when compared with the ipsilateral stimulation, and the solid indicate the same with contralateral stimulation.
I
1OO 150 200
I ?-5pV I
O
I
50
I
I
I
100 150 200
I
rnsec
Fig. 3. Sixty-one-year-old female with left cerebral infarction. The P100 amplitude on left ocular stimulation is smaller than that on right ocular stimulation resulting in significantly small interocular P100 ratio (small P100/large P100).
TABLE IV Intragroup analyses.
Stroke patients with a. fugax (n = 9) VS.
those without (n = 24) Stroke patients with visual acuity 20/30 or better (n = 18) VS.
those with 20/40 or worse (n = 15) Recent stroke subjects (n = 23)
Interocular P100 latency difference (msec)
P value
Interocular P100 amplitude ratio
P value
4.75:4.6
0.83
0.795:0.24
0.3
VS.
VS.
5.2 _+4.5
0.69 5:0.20
4.5 _+3.6
0.51
0.68 + 0.22
VS.
VS.
5.6 _+5.8
0.74 ___0.22
4.6 + 4.7
0.79
0.74 + 0.20
VS.
VS.
VS.
remote stroke subjects (n = 10)
5.3 + 4.5
0.70 + 0.24
0.45
0.76
208
ocular stimulation contralateral to the side of the infarction ( P = 0.04). The mean P100 latency on ocular stimulation contralateral to the side of the cerebral infarction in patients with arteriographic evidence of contralateral internal carotid artery stenosis (n = 6) was not significantly different from that in those without contralateral internal carotid artery stenosis ( n = 11). The correlation coefficients between interocular P100 latency differences and interocular P100 amplitude ratios in each of the 3 groups were: stroke group, r = 0.35, control group I, r = 0.11, and control group II, r = 0.13; none of these are significant.
Discussion
The results of the intergroup comparisons of interocular P100 latency differences and amplitude ratios, those of intragroup comparison of P100 latencies and sides of infarction, combined with absence of cataracts, other media opacities, glaucoma, or significant retinal disease in any of the groups provide convincing evidence of dysfunction of anterior visual pathways in the stroke group. This confirms and extends the observations of Robertson and Feldman (1980) in a single patient with occlusive stroke related to neck trauma. The proportion of stroke subjects with abnormal PSVEPs, 45%, was lower than the combined average, 68%, of the 2 major series dealing with alterations of the PSVEPs in multiple sclerosis (Halliday et al. 1973; Shahrokhi et al. 1978). The pattern of abnormalities, however, was the same as in MS the most common alteration being increased interocular P100 latency difference, followed by amplitude alterations, and absolute prolongation of the P100 latency. The pattern of PSVEP alterations with clinically evident ischemic optic neuritis, however, is different, amplitude alterations being the most c o m m o n abnormality, latency abnormalities being minor and less frequent (Wilson 1978). The intragroup analyses of the stroke subjects indicated that (i) the PSVEP alterations were not directly related to visual complaints, i.e., amaurosis fugax, or to reduced visual acuity; the PSVEP technique thus eliciting the evidence of visually
N.P. V E R M A ET AL.
asymptomatic anterior pathway dysfunction, (ii) the presence of arteriographic evidence of significant vascular stenosis on the side contralateral to the infarction did not increase the likelihood of prolonged P100 latency on that side, and (iii) interocular P100 latency differences and interocular P100 amplitude ratios may be differentially sensitive parameters of anterior visual pathway dysfunction as no significant correlation existed between the two variables in any of the study groups. Three subjects in the stroke group had abnormal PSVEPs by virtue of prolonged P100 latencies with stimulation of either eye without a significant interocular latency difference. These patients cannot be classified in respect to anterior or posterior location of the involvement of visual pathways. Further, in those 2 patients with latency delays with both eyes, but, in addition a significant difference between eyes, a posterior element may have contributed to the extent of the lesser delay. The study design makes it likely that the observed PSVEP alterations were associated with the occurrence of the stroke, per se, since no comparable changes were found in a patient reference group without significantly different incidences of hypertension, diabetes mellitus and heart disease. This event may signal the presence of associated acute ischemia in the territory of the ophthalmic artery (Ackerman 1979). If sufficiently severe, permanent damage to the structures supplied by the ophthalmic artery may occur. In the patient with a remote stroke, since no significant differences occurred between patients with recent and with remote stroke, the abnormal PSVEPs might reflect damage incurred at the time of stroke, or a continuing vascular deficit. The interesting finding that the interocular P100 latency differences were not correlated with the interocular amplitude ratios within the stroke group, suggests that more than a single mechanism may be operative.
Summary Monocular pattern-shift visual evoked potentials were obtained in (i) 33 patients with unilateral non-hemorrhagic hemispheric infarction
MONOCULAR PSVEPs IN HEMISPHERIC STROKES (age 5 0 - 7 9 years; 23 males, 10 females), (ii) 21 age- and sex-matched patient controls (control group or C G I ) with no remote or recent stroke, n o r m a l neurological examination and similar incidence of diabetes mellitus, hypertension and heart disease, and (iii) 21 age- and sex-matched healthy elderly c o m m u n i t y volunteers (CGII). Subjects with history of glaucoma, cataracts, other media opacities or s y m p t o m a t i c retinal lesions were not considered or included in any of the 3 study groups. In addition, all subjects in each of the 3 groups had a normal ocular and fundoscopic examination. The mean interocular P100 latency difference in the stroke group was significantly greater than that. in C G I or II ( P < 0.01). The mean interocular P100 amplitude ratio (small P 1 0 0 / l a r g e P100) in the stroke subjects was significantly different from that of C G I or II ( P <0.02). The mean P100 latency on ocular stimulation ipsilateral to the side of infarction was significantly longer than that of either left or fight ocular stimulation in C G I or II ( P < 0 . 0 1 ) . The m e a n P100 latency on ocular stimulation contralateral to the side of infarction was similarly but less significantly longer than that on left or right ocular stimulation in C G I or II ( P < 0.05). Evidence of anterior visual p a t h w a y dysfunction was thus elicited in the stroke population using the technique.
209 pr6sentant une histoire de glaucome, de cataracte ou autre opacit6 des milieux oculaires ou de 16sions r6tiniennes symptomatiques n ' o n t 6t6 ni consid6r6s ni i n d u s duns un des 3 groupes. De plus t o u s l e s sujets des 3 groupes avaient un examen oculaire et de fond d'oeil normal. D a n s le groupe h infarctus, la m o y e n n e de la diff6rence de latence interoculaire de P100 6tait significativement plus grande que dans le groupe C G I ou II ( P < 0,01) et la m o y e n n e du rapport de l'amplitude interoculaire de P100 (petit P 1 0 0 / ample P100) 6tait significativement diff6rente de celle de C G I ou II ( P < 0,02). La m o y e n n e de latence de P100 h une stimulation oculaire ipsilat6rale h l'infarctus 6tait significativement plus longue que celle correspondant h une stimulation oculaire droite ou gauche duns les C G I ou II ( P < 0,01). La m o y e n n e de la latence de P100 une stimulation oculaire contralat&ale h l'infarctus 6tait 6galement plus longue mais de fa9on moins significative que celle correspondant h la stimulation droite ou gauche des groupes t6moins G I et II ( P < 0,05). La preuve d ' u n disfonctionnement de la voie visuelle ant6rieure dans la population avec infarctus a 6t6 aussi mise en 6vidence avec cette technique. We thank Mr. Robert E. Marshall, B.A., B.S.E.E. and Mr. Lu Lee for help with the statistical analysis, and Mrs. Sheila Crowley for typing the manuscript.
R6sum6 References
Potentiel bvoqub visuel monoculaire iz une inversion de pattern aprbs attaque hbmisphbrique Des potentiels 6voqu6s visuels monoculaires h des inversions de pattern ont 6t6 obtenus (i) chez 33 patients avec infarctus h6misph6rique unilat6ral n o n h~morragique (~g(~s de 50 h 79 ans: 23 hommes, 10 femmes), (ii) chez 21 patients t6moins d'~ge et de sexe correspondants (groupe t6moin ou C G I ) sans attaque r6cente ou ancienne avec examen neurologique normal et la m~me fr~quence de diab6te sucr6, d'hypertension et de troubles cardiaques, et (iii) chez 21 volontaires ~g~s sains d'~ge et de sexe correspondants (CGII). Les sujets
Ackerman, R.H. A perspective on noninvasive diagnosis of carotid disease. Neurology (Minneap.), 1979, 29: 615-622. Bodis-Wollner, I. and Yahr, M.D. Measurement of visual evoked potentials in Parkinson's disease. Brain, 1978, 101: 661-671.
Carroll, W.M., Kriss, A., Baritser, M., Barrett, G. and Halliday, A.M. The incidence and nature of the visual pathway involvement in Friedreich's ataxia: a clinical and visual evoked potential study of 22 patients. Brain, 1980, 103: 413-434. Chiappa, K.H. Pattern-shift visual, brainstem auditory, and short-latency somatosensory evoked potentials in multiple sclerosis. Neurology (Minneap.), 1980, 30: 110-123. Chiappa, K.H. and Ropper, A.H. Evoked potentials in clinical medicine. New Engl. J. Med., 1982, 306: 1140-1150.
210 Halliday, A.M. and Mushin, J. The visual evoked potential in neurophthalmology. Int. ophthalmol. Clin., 1980, 20: 155-183. HaUiday, A.M., McDonald, W.I. and Mushin, J. Visual evoked response in the diagnosis of multiple sclerosis. Brit. reed. J., 1973, 4: 661-664. Robertson, E. and Feldman, R.G. Pattern-shift visual evoked response in carotid occlusion. Clin. Electroenceph., 1980, 11: 67-71. Ropper, A.H., Miett, T. and Chiappa, K. Absence of evoked potential abnormalities in acute transverse myelopathy. Neurology (Minneap.), 1982, 32: 80-82. Shahrokhi, F., Chiappa, K.H. and Young, R.R. Pattern-shift
N.P. VERMA ET AL. visual evoked responses. Two hundred patients with optic neuritis and/or multiple sclerosis. Arch. Neurol. (Chic.), 1978, 35: 65-71. Streletz, L.J., Chambers, R.A., Bae, S.H. and Israel, H.L. Visual evoked potentials in sarcoidosis. Neurology (Minneap.), 1981, 31: 1545-1549. Troncoso, J., Mancall, E.L. and Schatz, N.J. Visual evoked responses in pernicious anemia. Arch. Neurol. (Chic.), 1979, 36: 168-169. Wilson, W.B. Visual evoked response differentiation of ischemic optic neuritis from the optic neuritis of multiple sclerosis. Amer. J. Ophthal., 1978, 86: 530-535.
205
M O N O C U L A R PATYERN-SHIFT VISUAL EVOKED P O T E N T I A L S IN H E M I S P H E R I C STROKES t
NARAYAN P. VERMA 2, KENNETH A. KOOI and JOHN GILROY Holden Laboratory of Clinical Neurophysiology, Wayne State University School of Medicine, Harper-Grace Hospitals, Detroit, All 48201 (U.S.A.) (Accepted for publication: February 15, 1984)
Monocular pattern-shift visual evoked potentials (PSVEPs) have been studied in m a n y neurological disorders including multiple sclerosis and other demyelinating diseases (Halliday et al. 1973; Chiappa 1980), spinocerebellar degenerations (Carroll et al. 1980), pernicious anemia (Troncoso et al. 1979), sarcoidosis (Streletz et al. 1981), Parkinson's disease (Bodis-WoUner and Yahr 1978), transverse myelitis (Ropper et al. 1982), and m a n y others (Chiappa and Ropper 1982), as a measure of functioning of the anterior visual pathways. Although alterations of the PSVEP have been reported in known ischemic optic neuritis (Wilson 1978; Halliday and Mushin 1980), and in stroke associated with neck trauma (Robertson and Feldman 1980), their occurrence in association with hemispheric strokes has not been explored systematically. The study reported here is designed to determine if a significant association exists, and, if so, to assess the nature and extent of changes.
Material and Methods
Three groups of subjects were studied. Relevant group characteristics are shown in Table I. The first group, henceforth to be referred to as the stroke group, was comprised of 33 subjects with neurologic evidence of unilateral non-hemorrhagic strokes. Twenty-two had left hemispheric 1 Presented in part at the American EEG Society meeting in New Orleans, October 1983. 2 Address requests for reprints to: N.P. Verma, M.D., Dept. of Neurology-127, V.A.M.C., Allen Park, MI 48101, U.S.A.
strokes, and 11, right. Twenty-two had 4-vessel cerebral arteriographic studies. Of these, 17 had significant stenosis or complete occlusion of the appropriate internal carotid artery; 6 had additional significant stenosis of the contralateral internal carotid artery. Twenty-three had PSVEP studies during hospitalization for a recent stroke, while the remaining 10 were studied a few months to several years after an earlier stroke. The second group, to be referred to as control group I, comprised of 21 age- and sex-matched patients with non-specific complaints such as headache, dizziness and blurring of vision, a normal neurologic examination, and no recent or remote stroke. The incidences of diabetes mellitus, hypertension and heart disease in the stroke group and control group I were not significantly different. The third group, to be called control group II, consisted of 21 ageand sex-matched elderly healthy community volunteers. Subjects with history of cataracts, other media opacities, glaucoma or symptomatic retinal lesions were not considered or included in any of the 3 study groups. In addition, all subjects in each group had a normal ocular and fundoscopic exarnination other than mild hypertensive changes. As the study involved the assessment of anterior visual pathways and utilized monocular full-field stimulation, patients with homonymous visual field defects were not excluded. Subjects who used glasses wore them during the visual acuity determination and the PSVEP procedure. The visual acuity was determined using the Snellen's chart from a distance of 20 feet. Goldplated cup electrodes were attached to the scalp in midoccipital (Oz), left and right occipital (01 and
0013-4649/84/$03.00 © 1984 Elsevier Scientific Publishers Ireland, Ltd.
N.P. VERMA ET AL.
206 TABLE I Characteristics of patients and normal study groups. Group
No.
Age range (years)
Mean age (years)
M/F
Hypertension
Diabetes mellitus
Heart disease
Stroke group Patient controls (control group I) Normal controls (control group II)
33 21 21
50-79 50-77 50-75
62.1 61.9 61.0
23/10 14/7 14/7
14 7 0
6 3 0
6 6 0
0 2) a n d m i d c e n t r a l (Cz) areas, as well as to b o t h e a r l o b e s using the c o l l o d i o n technique. Skin-elect r o d e interface i m p e d a n c e s were k e p t less t h a n 5000 ~ . A n a l t e r n a t i n g b l a c k - a n d - w h i t e p a t t e r n h a v i n g a check-size of 36' was g e n e r a t e d on a television screen at a f r e q u e n c y of 1.88 c / s e c . S t i m u l u s l u m i n a n c e for white squares was 225.5 c d / m 2 and, for b l a c k squares, 12.7 c d / m 2. Sixty-four individual responses derived from m o n o c u l a r s t i m u l a t i o n o f either eye were averaged, each for test, a n d for retest, e m p l o y i n g a N i c o l e t 1170 r e s p o n s e averager, viewing d i s t a n c e b e i n g 1 m a n d n o m i n a l l i n e a r b a n d p a s s filter width, 1 - 3 5 c / s e c . T h e subjects were o b s e r v e d for consistency o f gaze t h r o u g h o u t the p e r i o d of d a t a collection. A n E E G tracing was r e c o r d e d t h r o u g h o u t the p r o c e d u r e to ensure alertness a n d signal reliability. F u n c t i o n i n g of the a n t e r i o r visual p a t h w a y s was assessed b y m e a s u r i n g the P100 latencies, P100 a m p l i t u d e s , i n t e r o c u l a r P100 l a t e n c y differences a n d i n t e r o c u l a r P100 a m p l i t u d e ratios (small P 1 0 0 / l a r g e P100) at the m i d o c c i p i t a l - j o i n e d ears derivation, using d a t a d e r i v e d f r o m g r a n d averages o f 128 responses o n each subject. T h e statistical analyses were m a d e using Stud e n t ' s t test, the chi square test a n d correlative analytical methods.
different f r o m that of c o n t r o l g r o u p I o r II ( T a b l e III). A d d i t i o n a l l y , the m e a n P100 l a t e n c y on ocular s t i m u l a t i o n ipsilateral to the side o f cerebral i n f a r c t i o n was significantly longer t h a n that on right or left eye s t i m u l a t i o n in c o n t r o l g r o u p I or II (Fig. 1). T h e m e a n P100 latency on o c u l a r s t i m u l a t i o n c o n t r a l a t e r a l to the side of the infarction was similarly, b u t less significantly, longer t h a n that o n right o r left o c u l a r s t i m u l a t i o n in c o n t r o l g r o u p I o r II (Fig. 1). O n the basis o f n o r m a l limits ( m e a n _+ 3 S.D.) d e t e r m i n e d from n o r m a l volunteers (control g r o u p II), 15 of 33 stroke subjects h a d a b n o r m a l PSVEPs c o m p a r e d to n o n e of 21 subjects in c o n t r o l g r o u p I ( P = 0.002, chi square test), when all 3 variables, viz., l a t e n c y differences, a m p l i t u d e alterations, a n d l a t e n c y p r o l o n g a t i o n , were c o n s i d e r e d together (Figs. 2 a n d 3). I n t r a g r o u p analyses, p a r t l y d e p i c t e d in T a b l e IV, d i d n o t reveal a n y significant differences in s t r o k e subjects with a n d w i t h o u t a m a u r o s i s fugax, in those with visual acuity 2 0 / 3 0 or b e t t e r a n d those with visual acuity 2 0 / 4 0 o r worse, a n d those with recent a n d r e m o t e event. T h e m e a n P100 l a t e n c y on o c u l a r s t i m u l a t i o n ipsilateral to the i n f a r c t i o n was significantly longer t h a n that on
TABLE II R ~
Mean interocular P100 latency differences and standard deviations of 3 study groups.
I n t e r g r o u p c o m p a r i s o n s are d e p i c t e d in T a b l e s II a n d III, a n d Fig. 1. T h e m e a n i n t e r o c u l a r P100 l a t e n c y difference in the s t r o k e g r o u p was signific a n t l y greater t h a n that of c o n t r o l g r o u p I or | I ( T a b l e II). T h e m e a n i n t e r o c u l a r P100 a m p l i t u d e r a t i o in the stroke group, also, was significantly
Group
Mean difference + S.D.
Significance of difference vs. stroke group
Stroke group Control group I Control group II
5.0 + 4.6 2.2 + 1.6 2.0 + 1.2
P = 0.009 P = 0.005
207
M O N O C U L A R PSVEPs IN HEMISPHERIC STROKES TABLE IlI Mean interocular P100 amplitude ratios and standard deviations of 3 study groups. Group
Stroke group Control group I Control group II
Mean ratio 5: S.D.
Significance of difference vs. stroke group
0.72 + 0.21 0.87 5:0.13 0.85 + 0.15
P = 0.009 P = 0.016
Control group I (right eye} 106, tl + 5 . 6 msec
• I • ! Cont~*ol g r o u p II (right eye) 105.2 + q. 9 msec ~
"~
.....
stimulation contralateral . , to s i d e o f i n f a r c t 112.2 + 1 t . 3 msec -
p=O. 009
p=O. 016 - -
L
i [
20/25
I', I
0
P100 l a t e n c y on o c u l a r p=0.0~'9 stimulation ipsilateral to side o f i n f a r c t s ./'/" l ) 11t1.6 + 1 2 , 2 m s e c ( ~ p=0.0q
Soo
V _A 20/25
i
Control group I ( l e f t eye) 106.7 +_ 6.it msec 0.006
p=0.03
Y E _ E R ~
•
50
I[[
I
I
msec
Fig. 2. Sixty-four-year-old female with right cerebral infarction. The mean P100 latency on right ocular stimulation is significantly longer than that on left ocular stimulation. The tracing is recorded with a midoccipital derivation referred to interconnected ears with relative positivity at the occipital electrode producing a downward deflection.
EYE R ~
VA 20/25
L ~
20/30
p 01o03 ' ! C o n t r o l g r o u p II ( l e f t eye} 105.8 +_ ~. 6 rnsec
Fig. 1. Mean P100 latencies on ocular stimulation ipsilateral and contralateral to the side of cerebral infarction, and comparison thereof with the same on right or left eye stimulation in control groups I and II. The broken lines indicate the levels of significance when compared with the ipsilateral stimulation, and the solid indicate the same with contralateral stimulation.
I
1OO 150 200
I ?-5pV I
O
I
50
I
I
I
100 150 200
I
rnsec
Fig. 3. Sixty-one-year-old female with left cerebral infarction. The P100 amplitude on left ocular stimulation is smaller than that on right ocular stimulation resulting in significantly small interocular P100 ratio (small P100/large P100).
TABLE IV Intragroup analyses.
Stroke patients with a. fugax (n = 9) VS.
those without (n = 24) Stroke patients with visual acuity 20/30 or better (n = 18) VS.
those with 20/40 or worse (n = 15) Recent stroke subjects (n = 23)
Interocular P100 latency difference (msec)
P value
Interocular P100 amplitude ratio
P value
4.75:4.6
0.83
0.795:0.24
0.3
VS.
VS.
5.2 _+4.5
0.69 5:0.20
4.5 _+3.6
0.51
0.68 + 0.22
VS.
VS.
5.6 _+5.8
0.74 ___0.22
4.6 + 4.7
0.79
0.74 + 0.20
VS.
VS.
VS.
remote stroke subjects (n = 10)
5.3 + 4.5
0.70 + 0.24
0.45
0.76
208
ocular stimulation contralateral to the side of the infarction ( P = 0.04). The mean P100 latency on ocular stimulation contralateral to the side of the cerebral infarction in patients with arteriographic evidence of contralateral internal carotid artery stenosis (n = 6) was not significantly different from that in those without contralateral internal carotid artery stenosis ( n = 11). The correlation coefficients between interocular P100 latency differences and interocular P100 amplitude ratios in each of the 3 groups were: stroke group, r = 0.35, control group I, r = 0.11, and control group II, r = 0.13; none of these are significant.
Discussion
The results of the intergroup comparisons of interocular P100 latency differences and amplitude ratios, those of intragroup comparison of P100 latencies and sides of infarction, combined with absence of cataracts, other media opacities, glaucoma, or significant retinal disease in any of the groups provide convincing evidence of dysfunction of anterior visual pathways in the stroke group. This confirms and extends the observations of Robertson and Feldman (1980) in a single patient with occlusive stroke related to neck trauma. The proportion of stroke subjects with abnormal PSVEPs, 45%, was lower than the combined average, 68%, of the 2 major series dealing with alterations of the PSVEPs in multiple sclerosis (Halliday et al. 1973; Shahrokhi et al. 1978). The pattern of abnormalities, however, was the same as in MS the most common alteration being increased interocular P100 latency difference, followed by amplitude alterations, and absolute prolongation of the P100 latency. The pattern of PSVEP alterations with clinically evident ischemic optic neuritis, however, is different, amplitude alterations being the most c o m m o n abnormality, latency abnormalities being minor and less frequent (Wilson 1978). The intragroup analyses of the stroke subjects indicated that (i) the PSVEP alterations were not directly related to visual complaints, i.e., amaurosis fugax, or to reduced visual acuity; the PSVEP technique thus eliciting the evidence of visually
N.P. V E R M A ET AL.
asymptomatic anterior pathway dysfunction, (ii) the presence of arteriographic evidence of significant vascular stenosis on the side contralateral to the infarction did not increase the likelihood of prolonged P100 latency on that side, and (iii) interocular P100 latency differences and interocular P100 amplitude ratios may be differentially sensitive parameters of anterior visual pathway dysfunction as no significant correlation existed between the two variables in any of the study groups. Three subjects in the stroke group had abnormal PSVEPs by virtue of prolonged P100 latencies with stimulation of either eye without a significant interocular latency difference. These patients cannot be classified in respect to anterior or posterior location of the involvement of visual pathways. Further, in those 2 patients with latency delays with both eyes, but, in addition a significant difference between eyes, a posterior element may have contributed to the extent of the lesser delay. The study design makes it likely that the observed PSVEP alterations were associated with the occurrence of the stroke, per se, since no comparable changes were found in a patient reference group without significantly different incidences of hypertension, diabetes mellitus and heart disease. This event may signal the presence of associated acute ischemia in the territory of the ophthalmic artery (Ackerman 1979). If sufficiently severe, permanent damage to the structures supplied by the ophthalmic artery may occur. In the patient with a remote stroke, since no significant differences occurred between patients with recent and with remote stroke, the abnormal PSVEPs might reflect damage incurred at the time of stroke, or a continuing vascular deficit. The interesting finding that the interocular P100 latency differences were not correlated with the interocular amplitude ratios within the stroke group, suggests that more than a single mechanism may be operative.
Summary Monocular pattern-shift visual evoked potentials were obtained in (i) 33 patients with unilateral non-hemorrhagic hemispheric infarction
MONOCULAR PSVEPs IN HEMISPHERIC STROKES (age 5 0 - 7 9 years; 23 males, 10 females), (ii) 21 age- and sex-matched patient controls (control group or C G I ) with no remote or recent stroke, n o r m a l neurological examination and similar incidence of diabetes mellitus, hypertension and heart disease, and (iii) 21 age- and sex-matched healthy elderly c o m m u n i t y volunteers (CGII). Subjects with history of glaucoma, cataracts, other media opacities or s y m p t o m a t i c retinal lesions were not considered or included in any of the 3 study groups. In addition, all subjects in each of the 3 groups had a normal ocular and fundoscopic examination. The mean interocular P100 latency difference in the stroke group was significantly greater than that. in C G I or II ( P < 0.01). The mean interocular P100 amplitude ratio (small P 1 0 0 / l a r g e P100) in the stroke subjects was significantly different from that of C G I or II ( P <0.02). The mean P100 latency on ocular stimulation ipsilateral to the side of infarction was significantly longer than that of either left or fight ocular stimulation in C G I or II ( P < 0 . 0 1 ) . The m e a n P100 latency on ocular stimulation contralateral to the side of infarction was similarly but less significantly longer than that on left or right ocular stimulation in C G I or II ( P < 0.05). Evidence of anterior visual p a t h w a y dysfunction was thus elicited in the stroke population using the technique.
209 pr6sentant une histoire de glaucome, de cataracte ou autre opacit6 des milieux oculaires ou de 16sions r6tiniennes symptomatiques n ' o n t 6t6 ni consid6r6s ni i n d u s duns un des 3 groupes. De plus t o u s l e s sujets des 3 groupes avaient un examen oculaire et de fond d'oeil normal. D a n s le groupe h infarctus, la m o y e n n e de la diff6rence de latence interoculaire de P100 6tait significativement plus grande que dans le groupe C G I ou II ( P < 0,01) et la m o y e n n e du rapport de l'amplitude interoculaire de P100 (petit P 1 0 0 / ample P100) 6tait significativement diff6rente de celle de C G I ou II ( P < 0,02). La m o y e n n e de latence de P100 h une stimulation oculaire ipsilat6rale h l'infarctus 6tait significativement plus longue que celle correspondant h une stimulation oculaire droite ou gauche duns les C G I ou II ( P < 0,01). La m o y e n n e de la latence de P100 une stimulation oculaire contralat&ale h l'infarctus 6tait 6galement plus longue mais de fa9on moins significative que celle correspondant h la stimulation droite ou gauche des groupes t6moins G I et II ( P < 0,05). La preuve d ' u n disfonctionnement de la voie visuelle ant6rieure dans la population avec infarctus a 6t6 aussi mise en 6vidence avec cette technique. We thank Mr. Robert E. Marshall, B.A., B.S.E.E. and Mr. Lu Lee for help with the statistical analysis, and Mrs. Sheila Crowley for typing the manuscript.
R6sum6 References
Potentiel bvoqub visuel monoculaire iz une inversion de pattern aprbs attaque hbmisphbrique Des potentiels 6voqu6s visuels monoculaires h des inversions de pattern ont 6t6 obtenus (i) chez 33 patients avec infarctus h6misph6rique unilat6ral n o n h~morragique (~g(~s de 50 h 79 ans: 23 hommes, 10 femmes), (ii) chez 21 patients t6moins d'~ge et de sexe correspondants (groupe t6moin ou C G I ) sans attaque r6cente ou ancienne avec examen neurologique normal et la m~me fr~quence de diab6te sucr6, d'hypertension et de troubles cardiaques, et (iii) chez 21 volontaires ~g~s sains d'~ge et de sexe correspondants (CGII). Les sujets
Ackerman, R.H. A perspective on noninvasive diagnosis of carotid disease. Neurology (Minneap.), 1979, 29: 615-622. Bodis-Wollner, I. and Yahr, M.D. Measurement of visual evoked potentials in Parkinson's disease. Brain, 1978, 101: 661-671.
Carroll, W.M., Kriss, A., Baritser, M., Barrett, G. and Halliday, A.M. The incidence and nature of the visual pathway involvement in Friedreich's ataxia: a clinical and visual evoked potential study of 22 patients. Brain, 1980, 103: 413-434. Chiappa, K.H. Pattern-shift visual, brainstem auditory, and short-latency somatosensory evoked potentials in multiple sclerosis. Neurology (Minneap.), 1980, 30: 110-123. Chiappa, K.H. and Ropper, A.H. Evoked potentials in clinical medicine. New Engl. J. Med., 1982, 306: 1140-1150.
210 Halliday, A.M. and Mushin, J. The visual evoked potential in neurophthalmology. Int. ophthalmol. Clin., 1980, 20: 155-183. HaUiday, A.M., McDonald, W.I. and Mushin, J. Visual evoked response in the diagnosis of multiple sclerosis. Brit. reed. J., 1973, 4: 661-664. Robertson, E. and Feldman, R.G. Pattern-shift visual evoked response in carotid occlusion. Clin. Electroenceph., 1980, 11: 67-71. Ropper, A.H., Miett, T. and Chiappa, K. Absence of evoked potential abnormalities in acute transverse myelopathy. Neurology (Minneap.), 1982, 32: 80-82. Shahrokhi, F., Chiappa, K.H. and Young, R.R. Pattern-shift
N.P. VERMA ET AL. visual evoked responses. Two hundred patients with optic neuritis and/or multiple sclerosis. Arch. Neurol. (Chic.), 1978, 35: 65-71. Streletz, L.J., Chambers, R.A., Bae, S.H. and Israel, H.L. Visual evoked potentials in sarcoidosis. Neurology (Minneap.), 1981, 31: 1545-1549. Troncoso, J., Mancall, E.L. and Schatz, N.J. Visual evoked responses in pernicious anemia. Arch. Neurol. (Chic.), 1979, 36: 168-169. Wilson, W.B. Visual evoked response differentiation of ischemic optic neuritis from the optic neuritis of multiple sclerosis. Amer. J. Ophthal., 1978, 86: 530-535.