Documenta Ophthalmologica 80: 51-61, 1992. 9 1992 Kluwer Academic Publishers. Printed in the Netherlands.

Pattern flash visual evoked potentials in patients with homonymous hemianopia W I L H A M R. BIERSDORF, 1 RAYMOND A. BELL 2 & ROY W. BECK 1 *University of South Florida, and James A. Haley Veterans Hospital, Tampa, Florida, USA; 2Medical College of Georgia, Augusta, Georgia, USA Accepted 20 December 1991

Key words: Dipole source, hemifield stimulation, homonymous hemianopia, pattern onset, visual evoked potential Abstract. Visual evoked potentials from seven horizontally spaced electrodes were recorded

from normal subjects and subjects with homonymous hemianopia in response to hemifield pattern flash stimulation. Stimulation produced a large early peak that was positive on the scalp contralateral to the hemifield and negative on the ipsilateral scalp. From computer fitting of the amplitudes versus electrode position, the position of the equivalent source was found to be in the contralateral hemisphere. The horizontal orientation of the dipole source was approximately tangential (parallel) to the occipital scalp surface with negative polarity toward the medial fissure. In normal subjects, visual evoked potential amplitudes at the first peak were positive on the left and negative on the right for right hemifield stimulation. Left hemifield stimulation showed the opposite results. Three patients with homonymous hemianopia showed normal visual evoked potential results from their functional hemifields and nearly flat results from their hemianopic hemifields. The normal visual evoked potentials originated in their intact cortical hemispheres. Abbreviation: C T - - c o m p u t e d tomographic.

Introduction The visual evoked potential (VEP) was originally recorded in hemianopic patients from scalp electrodes in response to unpatterned flashing lights [1]. The responses were found to show wide interindividual variability, making them unreliable for clinical studies. The introduction of pattern-reversal stimulation reduced the interindividual variability in several studies of hemianopia [2-6]. A different method of stimulation, that of pattern onset where the pattern stimulus alternates with a uniform field of the same average luminances, has been employed in cortical localization studies in normal subjects [7]. When the duration of the pattern is brief, it has been called pattern flash stimulation. Several studies with this type of stimulation have been carried out in normal subjects [8-12]. The polarities and amplitude distributions across the back of the head in

52 pattern-onset stimulation differ considerably from those produced by the commonly used pattern-reversal stimulation [13]. Pattern-onset VEPs are maximum positive contralateral to the hemifield stimulus, while pattern reversal produces a maximum positive ipsilateral VEP, 'paradoxic' to the pathways involved [14]. Interest in the pattern-onset VEP is in its possible use as a method of evaluation of hemifield visual defects. To investigate this, equivalent dipole analysis has been employed to determine if the equivalent dipole sources of the hemifield pattern-onset stimuli are correctly (contralaterally) located. The present study compares the results of pattern-onset flash stimulation in normal subjects and three patients with homonymous hemianopia.

Materials and methods

The patients viewed monocularly a video monitor 10~ 13~ wide at a distance of l m on which a high-contrast (90%) checkerboard pattern appeared for 32 ms once per second. Check size was 12'. Average screen luminance (296 c d / m 2) was maintained constant between the pattern on and off phases. An illuminated surround of 25 ~ x 25 ~ at 160 cm/m 2 was provided. Luminance and contrast were calibrated by means of a Macbeth Illuminometer. A red fixation light (light-emitting diode) was positioned at the center of the right or left edge of the checkerboard pattern. Electrodes were positioned on the posterior scalp at the midline 18~ above the inion (O z in the international 10-20 system) and three positions horizontally to each side. The reference electrode was on the nose and the ground on the right mastoid. Averaging at pattern-onset stimulation was based on 80 sweeps at 1.1 Hz. Both right and left eyes were tested. The first major deflection on the VEP waveform with a peak latency of about 90 ms was labeled C1 [7]. The amplitudes (negative or positive) of this deflection were measured on all channels at a constant latency (the same for both right and left hemifields). Amplitudes were measured from the peak of the small preceding deflection of opposite polarity (constant latency). The amplitudes were graphed for each hemifield of each eye of each subject. The amplitudes were also entered into a computer program (ASYSTANT) that determined the best-fitting (least-squares) Legendre polynomial, describing an equivalent dipole source for each graph [15]. This equation is a horizontal cross-sectional analysis with five variables, including orientation, horizontal position, depth, amplitude, and baseline offset. The best-fitting curve produced the location and horizontal orientation of the equivalent dipole source for each graph. The neuro-ophthalmologic examination of the hemianopic patients included visual fields on the Goldmann perimeter and computed tomographic (CT) scans or magnetic resonance images of the skull. Three normal subjects with visual acuities of 20/25 or better and three

53 patients with homonymous hemianopia with visual acuities of 20/30 or better were tested with hemifield pattern-flash stimulation. Normal subjects and patients were all right-handed. Informed consent was obtained from all subjects after the nature of the procedure had been explained fully.

Results

Figure 1 illustrates results from the right eye of a normal subject. Electrodes were positioned at the midline and at 18~ (O1, 02) , 36~ 54~ (Ts, T6) and 90~ (T3, T4) horizontally to each side. The left column of VEPs is from the left hemifield (fixation on the right edge of the pattern). Electrodes 1-4 (left side of the head) have an early large negative deflection, while electrodes 6-9 on the right side of the head have a positive deflection at the same peak latency (96 ms). Amplitudes at this latency are measured from the average latency of the preceding small deflection (62ms) and presented in the bottom graph as crosses. Stimulation of the left hemifield produces positive VEPs on the right scalp contralateral to the hemifield and negative VEPs on the ipsilateral scalp. The dashed line is the best-fitting theoretical curve (computer fitted) describing the surface potential (microvolts) versus horizontal position (degrees right or left of midline). This theoretical curve describes an equivalent dipole source for these VEPs located right of the occipital midline and oriented approximately tangential to the scalp surface positive to the right (Table 1). The VEPs in the right column of Fig. 1 are from the same electrodes for stimulation of the right hemifield of the right eye. The polarities of the potentials are reversed, now being positive on the left side of the head and negative on the right. Measurement of the amplitudes at the same latencies (62-96 ms) produces the data fitting the solid line in the graph at the bottom. The computer-fitted line indicates an equivalent dipole source located left of the occipital midline and approximately tangential to the scalp surface. The positive end of this dipole points to the left, away from the medial fissure. For both hemifields, the equivalent source is in the brain contralateral to the hemifield, producing positive contralateral VEPs and negative ipsilateral VEPs. Similar results were obtained from stimulation of the left eye. The other normal subjects showed similar results. Computerfitted curve constants are listed in Table 1 for both eyes of this normal subject and three patients. Case 1

A 41-year-old man without any known predisposing medical conditions began complaining of increasing headaches, especially in the left retro-orbit region, associated with nausea and 'confusion'. A C T scan revealed a large left temporal-lobe hematoma, which was evacuated through a left temporal craniotomy. Convalescence was unremarkable, and a follow-up CT scan

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Fig. 1. Pattern-onset VEPs for left hemifield (top left) and right hemifield (top right) in the right eye of a normal subject. Electrodes 1-4 were on left scalp; 5, midline; and 6-9, right scalp. Positive is upward. The abscissa shows milliseconds. Bottom, amplitude (I~V) versus degrees from the midline at the first major peak at 62-96 ms.

s h o w e d c o m p l e t e e v a c u a t i o n o f t h e h e m a t o m a . V i s u a l field e x a m i n a t i o n s h o w e d a d e n s e r i g h t h o m o n y m o u s h e m i a n o p i a with m a c u l a r splitting (Fig. 2). V i s u a l a c u i t y was 2 0 / 2 0 in b o t h eyes.

55 Table 1. D i p o l e s o u r c e c o n s t a n t s * Left hemifield Eye Normal

subject

Patient 1 Patient 2 Patient 3

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* A d i p o l e w i t h a p o s i t i v e l o c u s is to t h e r i g h t o f t h e m i d l i n e ; w i t h a n e g a t i v e l o c u s , left o f t h e m i d l i n e . P o s i t i v e o r i e n t a t i o n s h a v e p o s i t i v e V E P s to t h e r i g h t a n d n e g a t i v e V E P s to t h e left. Orientation

o f 0 ~ is r a d i a l s u r f a c e p o s i t i v e , a n d 90 ~ is s u r f a c e t a n g e n t i a l , p o s i t i v e to t h e r i g h t .

OD = right eye, OS = left eye. Amplitudes,

t o o s m a l l f o r r e l i a b l e fit b y a d i p o l e , a r e i n d i c a t e d w i t h a d a s h .

VEP recordings 5 months after the intracranial hemorrhage were obtained from the posterior scalp at the midline and at 27 ~ 54 ~ and 81~ horizontally to each side. Figure 2 illustrates the VEP amplitude graphs from right and left hemifields of the right eye to pattern flash stimulation. The first major deflection was measured at its peak (56 to 84 ms), and the results are plotted in the figure. Stimulation of the preserved left hemifield produced VEPs positive over the right cortex and negative over the left cortex. Stimulation of the right hemianopic field produced low-amplitude VEPs. Results were similar in the right and left eyes. The equivalent dipole source data are given in Table 1 for both eyes. Case 2 A 19-year-old man suffered a severe head injury in December 1979, with loss of consciousness lasting 1 week. After awakening, he has noted to have an inconsistent left homonymous inferior quadrantanopia on confrontation testing. Visual acuity was 20/20 in both eyes. A CT scan at that time and on a subsequent occasion during the next year was normal. Visual fields on a Goldmann perimeter 10 months after injury showed a complete left homonymous hemianopia. Nine years later, another CT was performed and was normal. Visual fields on the Goldmann perimeter again showed a complete left homonymous hemianopia with macular splitting. An ophthalmologic examination showed a mild left relative afferent pupillary defect. No optic atrophy was noted. Visual evoked potential recordings 10 years after the head injury were obtained from the posterior scalp at the midline and 27~ 54~ and 90~ horizontally to each side. Figure 3 illustrates the VEP amplitude graphs from right and left hemifields of the right eye to pattern-flash stimulation. The first major deflection amplitude was measured at 62 to 91 ms, and the

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Fig. 2. Case 1 (right homonymous hemianopia). VEPs for left hemifield (top left) and right hemifield (top right) in the right eye. Electrodes 1-3 were on left scalp; 4, midline; and 5-7, right scalp. Bottom, amplitude (~V) versus degrees from the midline at the first major peak at 56-88 ms.

results are plotted in the figure. Stimulation of the preserved right hemifield produced VEPs positive over the left cortex and negative over the right cortex. Stimulation of the left hemianopic field produced nearly flat VEPs. Results were similar in both eyes. The equivalent dipole source data are given in Table 1. In this case, VEP recording performed 10 years after the injury produced confirmatory evidence of a retrochiasmatic lesion consistent with the patient's hemianopia.

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Fig. 3. Case 2 (left homonymous hemianopia). VEPs in the right eye. Electrodes and graphs are as in Fig. 2. The first major peak is at 62-91 ms.

Case 3 A 52-year-old m a n suffered a large subarachnoid hemorrhage, presumably due to a ruptured aneurysm, which was surgically repaired. CT scans showed e d e m a involving the right occipital lobe and medial portion of the right t e m p o r a l lobe. With correction, visual activity was 20/20 in each eye. T h e r e was a complete left h o m o n y m o u s hemianopia. The patient had

58 convergence insufficiency, with exophoria greater at near than at distance. Visual e v o k e d potentials 3 years after the intracranial h e m o r r h a g e were obtained f r o m the posterior scalp at the midline and at 27 ~ 54 ~ and 90 ~ horizontally to each side. Figure 4 illustrates the V E P amplitude graphs f r o m right and left hemifields of the right eye to pattern flash stimulation.

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are as in Fig. 2. The first major peak is at 47-96 ms.

59 The first major deflection amplitude was measured at its peak (47-96 ms), and the results are plotted in the figure. Stimulation of the preserved right hemifield produced VEPs positive over the contralateral left cortex and negative over the right cortex. Stimulation of the impaired left hemifield produced nearly flat VEPs. Results were similar in both eyes. Equivalent dipole source data are in Table 1. For all subjects, the VEP source locations were in the hemisphere contralateral to the hemifield stimulated. The locus of the dipoles in this study ranged from 2.5 ~ to 25 ~ from the scalp midline (Table 1). The horizontal orientation of the dipole source was approximately tangential (parallel) to the occipital scalp surface, with negative polarity toward the medial fissure. Table 1 shows the variability from 42 ~ to 110~ of angle with the radius to the scalp surface. Similar results were found when the C1 amplitudes were measured from the start of the baseline. Control runs on the hemianopic patients with central fixation of the field showed VEP amplitudes and latencies similar to those obtained from their functional hemifields.

Discussion

In this study, VEPs from three patients with homonymous hemianopia with good visual acuity tested with hemifield pattern-flash stimulation showed clear differences in results from the two sides of the scalp. Stimulation of the intact hemifield produced positive VEPs at the first major peak on the contralateral side of the scalp, with negative VEPs on the ipsilateral scalp. The relative amplitudes of the negative and positive peaks varied between subjects, with most of the hemianopic patients in this study having larger positive contralateral amplitudes. This reflects the orientation of the dipole source indicating a tilt of the positive end toward the scalp surface. The patients with homonymous hemianopia produced nearly flat VEPs from their hemianopic hemifields. CT or magnetic resonance imaging findings confirmed cerebral damage contralateral to the hemianopic hemifields. All of the patients showed similar VEPs, including another hemianopic patient with a presumed optic tract lesion whom we described previously [16]. A recent study on normal and hemianopic subjects tested with hemifield pattern-onset stimulation found results similar to these, with a small early contralateral positive peak at a latency similar to that of a larger ipsilateral negative peak [17]. All three hemianopic patients in this study showed macular splitting. Whether similar results would also be obtained in patients with macular sparing requires further investigation. Electromagnetic theory postulates an equivalent dipole to be equivalent to two electrically charged sheets at the center. The use of the equivalent dipole here does not assume a single local source for the VEPs or even a single pair of extended surface sources. It represents the weighted average

60 of all sources contributing to the VEP at these electrodes at this particular latency. A simplified two-dimensional horizontal analysis was used here, as our interest was in the location of the dipole sources in the right or left hemisphere. The present analysis gives only horizontal and depth information on the location and orientation of the dipole sources. To determine vertical (longitudinal) components of the dipoles would require more electrode positions and a different dipole equation, e.g., that described by Scherg and yon Cramon [18]. Constants are published for the correction of homogeneous sphere data to that in a three-layer sphere model [19]. The only constant differences between the two models are in the apparent depth of the equivalent dipole [19], not considered in this study. The dipole analysis of the present pattern flash stimulation data showed that the equivalent source dipoles for the left- and right-hemifield VEPs were nearly opposed in the back plane of the head. The horizontal orientations of the left- and right-source dipoles were near 180 ~ apart, pointing in opposite directions perpendicular to the medial fissure. The locations of the source dipoles were also in the primary hemispheres, contralateral to the visual hemifield stimulated. Thus, the VEP results of hemifield pattern-onset stimulation in these hemianopic patients are consistent with the physiologic characteristics of the primary visual pathways. Pattern-onset VEP stimulation may be of assistance in the evaluation of hemianopia.

Acknowledgment This study was supported in part by National Institutes of Health grant EY08097.

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61 9. Shagass C, Amadeo M, Roemer PA. Spatial distribution of potentials evoked by half-field pattern reversal and pattern onset stimuli. Electroencephalogr Clin Neurophysiol 1976; 41: 609-22. 10. Leserve N, Joseph JP. Modifications of the pattern evoked potential (PEP) in relation to the stimulated part of the visual field (clues for the possible origin of each component). Electroencephalogr Cfin Neurophysiol 1979; 47: 183-203. 11. Darcey TM, Ary JP, Fender DH. Spatio-temporal visually evoked scalp potentials in response to partial-field patterned stimulation. Electroencephalogr Clin Neurophysiol 1980: 50: 348-55. 12. Maier J, Dagnelie G, Spekreijse H, van Dijk BW. Principal components analysis for source localization of VEPs in man. Vision Res 1987; 27: 165-77. 13. Biersdorf WR. Different scalp localization of pattern onset and reversal visual evoked potentials. Doc Ophthalmol 1987; 66: 313-20. 14. Barrett G, Blumhardt LD, Halliday AM, Halliday E, Kriss A. A paradox in the lateralization of the visual evoked response. Nature 1976; 261: 253-5. 15. Frank E. Electric potential produced by two point current sources in a homogeneous conducting sphere. J Appl Physics 1952; 23: 1125-8. 16. Bell RA, Biersdorf WR, Beck RW. Homonymous hemianopia and pattern onset hemifield visual evoked potentials. Arch Ophthalmol 1989; 107: 1429-30. 17. Onofrj M, Bodis-Wollner I, Basciana M, Gambi D. Stimulus specificity of visual evoked potential lateralization in humans compared with visual evoked potential lateralization in monkeys and rats. In: Barber C, Blum T, eds. Evoked potentials III. Boston: Butterworths, 1987: 213-20. 18. Scherg M, von Cramon D. Evoked dipole source potentials of the human auditory cortex. Electroencephalogr Clin Neurophysiol 1986; 65: 344-60. 19. Ary JP, Klein SA, Fender DH. Location of sources of evoked scalp potentials. Corrections for skull and scalp thickness. Biomed Eng 1981; 28: 447-54.

Address for correspondence: William R. Biersdorf, PhD, Ophthalmology 130B, JAH Veterans Hospital, 13000 Bruce B. Downs Blvd., Tampa, FL 33612, USA

Pattern flash visual evoked potentials in patients with homonymous hemianopia.

Visual evoked potentials from seven horizontally spaced electrodes were recorded from normal subjects and subjects with homonymous hemianopia in respo...
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