Brain (1976), 99, 357-374
THE PATTERN-EVOKED POTENTIAL IN COMPRESSION OF THE ANTERIOR VISUAL PATHWAYS by A. M. HALLIDAY, ELISE HALLIDAY, A. KRISS, W. I. MCDONALD and JOAN MUSHIN
INTRODUCTION
DEMYELINATION in the optic nerve produced by optic neuritis or multiple sclerosis produces a persistent increase in the latency of the potential evoked in the occipital cortex by pattern stimulation of the retina (Behrman, Halliday and McDonald, 1972; Halliday, 1972a, c, 1976; Halliday, McDonald and Mushin, 1972, I973a-d, \914a-d, 1976; Arden, 1973; Milner, Regan and Heron, 1974; Asselman, Chadwick and Marsden, 1975). Some evidence of delay can also be demonstrated byflashstimulation (Richey, Kooi and Tourtellotte, 1971; Namerow and Enns, 1972; Feinsod, Abramsky and Auerbach, 1973; Feinsod and Hoyt, 1975) but the most striking and consistent results have been obtained with a reversing checkerboard of black and white squares as the retinal stimulus. The method of pattern reversal shows that over 90 per cent of the patients with optic neuritis, and between 60 and 90 per cent of patients with clinically definite MS, have delays, even in the absence of the usual clinical signs of optic nerve disease (Halliday, McDonald and Mushin, 1973a, d; Asselman et ai, 1975). The evoked potential method thus provides the most sensitive means at present available for detecting subclinical lesions of the optic nerve. As such, it is being used increasingly as an aid to the early diagnosis of multiple sclerosis. Since the method has begun to come into routine clinical use, there has been a tendency to imagine that delays are specific to multiple sclerosis and optic neuritis. We have, however, repeatedly emphasized that this is not the case (Halliday et ai, 1973a1, 1976), and in this paper we present our findings in 19 patients with operatively proven compression of the optic nerve, chiasm or tract. The evoked response was abnormal in 18 of them. A preliminary account of this investigation has appeared elsewhere (Halliday, Halliday, Kriss, McDonald and Mushin, 1976a, b).
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(From the Medical Research Council, Institute of Neurology, National Hospital, Queen Square, London WC1)
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A. M. HALLIDAY AND OTHERS CLINICAL MATERIAL
Since our aim was to establish whether or not compression of the nerve fibres in the optic nerve, chiasm or radiation affected the pattern-evoked potential, we have restricted the clinical material to operatively proven cases of compression. We have examined 19 such cases (Table 1). Four patients had tumours confined to the orbit; 5 patients had an intracranial meningioma, 2 arising from the sphenoid wing and 3 from the region of the anterior clinoid process (suprasellar); 2 patients TABLE 1. PRESENTING SYMPTOMS IN THE 19 PATIENTS WITH COMPRESSIVE LESIONS INCLUDED IN THIS STUDY
Mode of presentation
Se.
47
M
Proptosis and visual distortion nine months
58
M
43
F
Proptosis. Previous excision meningioma one year earlier. Proptosis recurred with blurred vision Blurring of vision one year. Proptosis six months
52
F
Blurring vision plus proptosis ten months
48
F
40
F
Episode of aphasia one year ago. Visual loss three months Diplopia five years. Blurring of vision three years
45
F
59 46
F F
Craniopharyngioma 10 J. D.
29
M
11 N. S.
44
F
Pituitary tumour 12 P. H.
30
M
13 I. G. 14 E. P. 15 L. G.
58 46 57
F F M
16 H. P.
60
M
17 M. A. 18 C. D. 19 A. J.
50 56 39
F F M
Sphenoidal wing meningioma 5 J. G. 6 B. S. Suprasellar meningioma 7 J. B. 8 B. M. 9 J. N.
Right-sided headache three years. Deterioration in vision one year Blurring of vision one year Blurring of vision ten months Fluctuating L. visual loss nine months. Blurring R. vision one month Headaches and visual loss one year Episode of headache and blurring vision thirteen months ago and blurring vision five weeks Visual deterioration nine months Blurring vision two months Asymptomatic. Accidental discovery of enlarged pituitary fossa Impotence two years. Sudden severe headache and visual loss eleven weeks Visual loss two and a half months Blurring of vision two years Headache eight years. Hypopituitarism seven years. Increasing headache and diplopia six years. Visual loss five months
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Age
Case No. and site Orbital 1 R. B. Cavernous hsemangioma 2 A. S. Neurilemmoma 3 I. H. Meningioma 4 L. H. Cavernous haemangioma
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had a craniopharyngioma and 8 had pituitary tumours. Four of the latter were histologically proven adenomas (patients 12-15), but in 4 the histology, although consistent with adenoma, was indecisive (patients 16-19). METHOD
Parameters Studied The peak latency of the major positive wave at the mid-occipital electrode, and its peak-to-peak amplitude measured from the immediately preceding negative wave, was determined in every record in which this component could be identified. The form of the potential and its distribution in the occipital region was also noted. Measurements of the latency and amplitude were more difficult in this series of patients with compressive lesions than in the patients with optic neuritis and multiple sclerosis. In the latter group of patients the normal waveform of the response was usually preserved, even when the potential was markedly delayed, and a well-defined positivity was generally recorded at the mid-line occipital electrode. In the present series of patients, however, two types of alteration in the potential made meaningful measurements difficult in some cases and impossible in others. First, the waveform of the response recorded from the mid-occipital electrode was sometimes so much altered that the positive peak was ill-defined or absent, and no precise latency measurements could be made (compare, for instance, the waveform of the response from the affected and unaffected eyes in figs. 1 and 3). Secondly, the distribution of the response was altered and became asymmetric in some cases; in this event significant features were missed if attention was confined to measurements of the response from the mid-occipital electrode (see, for instance, figs. 4 and 5). None the less, the values for latencies and amplitudes given in Tables 2 and 3 are all based on records from the mid-line electrode. We have deliberately chosen to do this for several reasons. First, this is the electrode at which the response is normally largest and best defined, and the values can be compared directly with our previous observations on patients with retrobulbar neuritis and multiple sclerosis (Halliday, McDonald and Mushin, 1972, 1973a). Secondly, many departments of clinical neurophysiology which are introducing the evoked
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The technique was similar to that used in the earlier studies on multiple sclerosis (Halliday, McDonald and Mushin, 1972, \973d). The patient sat facing a circular translucent screen, subtending 32° at the eye, on to which was back-projected the slide of a black-and-white checkerboard. The individual squares subtended 50 minutes and the brightness levels were 227 cd/m2 for the white squares and 8-2 cd/m2 for the black squares. The white squares were about twice as bright as those used in the earlier studies. The recordings were made stimulating each eye separately, with the other eye covered with an eye pad, the subject being asked to fixate a small spot of light in the centre of the screen while the response was being averaged. Pattern reversal was produced, once every 600 ms, by a rapid lateral displacement of the checkerboard through one square (the transition taking approximately 10 ms). The occipital potentials were averaged, using a PDP-12 computer, which was triggered by the pattern reversal. The average response to 100 complementary reversals (200 pattern changes) was recorded at least twice for each eye. The response was measured from a recording made with a mid-occipital/mid-frontal electrode montage, the mid-occipital electrode being placed 5 cm above the inion. In addition, recordings were also made from electrodes 5 cm and 10 cm to the left and right of the mid-line occipital channel, also referred to the common mid-frontal reference. A sixth electrode was placed in the mid-line 5 cm below the inion. In certain cases, where the field of the potential was studied in more detail, the responses were averaged from a larger montage of up to 16 occipital electrodes. In a number of patients flash responses were also recorded. Visual acuity was measured at the time of the recording with a Snelien card, and, where appropriate, field defects were charted on a Goldman perimeter.
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A. M. HALLIDAY AND OTHERS
potential technique in the routine assessment of visual function, record only the mid-occipital channel because of the limited channel capacity of their small on-line averagers, and we wish to give some idea of the frequency and type of abnormality that may be detected with relatively simple equipment at a recording session of reasonable length.
RESULTS
TABLE 2. PATTERN EVOKED RESPONSE FINDINGS Side of lesion
L
R
Amplitude L R
L
Orbital 1 R. B.
L
6/24
6/9
6-8
9-6
115
106
2 AS.
L
6/36
6/5
5-7
13-9
127
117
3 I. H.
R
6/5
6/36
10-6
6-3
98
101
4 L. H.
L
6/6
6/9
11 5
18-3
102
98
L
NPL
6/6
79
-
127
R
6/9
6/9
110
104
134
C
6/5
6/36
14-5
0
100
R R
6/9 6/6
6/60 HM
8-8 5-9
0 0
104 110
Cranlopharyngloma 10 J. D.
C
HM
6/12 +
11 N. S
C
6/5
6/12
Sphenoidal wing meningioma 5 J. G.
6 B. S. Suprasellar meningioma 7 J. B. 8 B. M. 9 J. N.
Acuity
5-0
Latency R
3-3
-
GAW
93
Comments Not definitely beyond normal bnuts Marginal increase in latency of L eye response compared with other eye (9 ms difference). Major component of smaller amplitude and slightly altered waveform Reduction in amplitude (P < 0-001) and delay in L. eye response Reduction in amplitude ( P < 0 0 5 ) in R. eye Reduction in amplitude of L. eye response ( P < 0-001) associated with marked decrease of preceding negative wave
Responses from both eyes abnormal. Absent response from L. eye Asymmetrical and delayed response from R. eye (normal acuity) Reduced ( P < 0 001), asymmetrical and delayed response from R eye Absent pattern response and definitely delayed flash response from R. eye Absent response from R. eye 2nd record—Absent response from R. eye; marked deterioration since 1st record six months before (1st record showed an abnormal response from R. eye with greatly broadened positivity)
97
Responses from both eyes abnormal. Absent response from L eye Small asymmetrical response from R. eye GAW Responses from both eyes abnormal. Small asymmetrical responses, with grossly abnormal waveform from R. eye
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Table 2 gives the amplitude and latency measurements of the major positive component of the pattern evoked potential from each eye, recorded at the mid-occipital electrode for the 19 patients listed in Table 1. The visual acuity in each eye is also noted. Definitely abnormal values appear in bold type in the table, borderline abnormalities being indicated by italics. Under 'comments' are noted any asymmetries in the distribution of the response and any notable abnormalities in its waveform.
VISUAL-EVOKED POTENTIALS IN COMPRESSION
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TABLE 2 (cont.) Side of Acuity lesion L Pituitary tumour 12 P. H.
C
L
Amplitude R
Latency L
6/6
GAW
GAW
GAW
13 I. G.
6/6
6/36
6-2
GAW
137
14 E. R.
6/9
6/36
GAW
GAW
GAW
15 L. G.
6/6
6/6
5-4
101
116
16 H P
6/6
6/5
55
6-9
123
17 M A.
6/5
6/5
22-4
241
107
18 C D.
6/24
6/18
0
4-6
—
19 A. J
6/18pt
6/9pt
37
4-3
113
Comments
GAW Responses from both eyes abnormal Very small abnormal response from L. eye. Larger response from R eye with marked asymmetry GAW Responses from both eyes abnormal. Delayed response from L eye. Small abnormal response from R. eye GAW Responses from both eyes abnormal. Asymmetrical responses from both eyej. The response from the right eye is of much smaller amplitude 109 Reduced response from L eye (P < 005) with abnormal waveform (broad posiuvity) and marked asymmetry. Normal response from R. eye 121 Responses from both eyes abnormal. Asymmetrical response from each eye 105 Responses from both eyes abnormal Asymmetrical response from each eye 124 Responses from both eyes abnormal. Absent response from L eye. Small delayed, asymmetrical response from R. eye 111 Responses from both eyes abnormal. Asymmetrical responses from each eye
GAW = grossly abnormal waveform. Definitely abnormal values are printed in bold type, borderline abnormalities in italics.
. Abnormal PEPs were found in 18 of the 19 cases with proven compression (95 per cent). The single case with a normal response (patient 1) had an intracranial cavernous haemangioma of the left orbit, and visual acuity was reduced in the left eye to 6/24. Although not beyond normal limits, the response from the affected eye showed a marginal increase in latency (9 ms) compared with the other eye, and the major component was of smaller amplitude and slightly altered waveform. A variety of more definite abnormalities was found in the remaining cases. The other 3 patients with intra-orbital lesions all showed a significantly smaller amplitude of response from the affected eye (Table 2). In one case (patient 2), where there was an orbital neurofibroma, the positivity was also abnormally delayed. The reduction in amplitude in patients 3 and 4 was associated with a major positive peak of entirely normal latency and waveform. In patient 4 the reduction in amplitude of the major positive component was largely due to a loss of the preceding negative peak from which it was measured. In the 4 patients with intra-orbital tumours, the abnormality was limited to the response from the affected eye. The remaining 15 patients had intracranial space-occupying lesions, 2 arising from the sphenoidal wing and the remainder from the region of the sella turcica, and in this group the responses from more than one eye could be affected. Of the 5 intracranial meningiomas, the majority
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CF
R
362
A. M. HALLIDAY AND OTHERS
had only a uniocular abnormality of the PEP, and only one had definitely abnormal responses from each eye (patient 5). Serial recording suggested, however, that patient 9 also showed a slight alteration in the response on the less affected side, as compared with a previous record six months before {see fig. 2). In contrast to the meningiomas, 9 of the 10 patients in whom compression of the visual pathway arose from an extension of either an intrasellar or parasellar tumour had marked abnormalities in the response from both eyes (the exception being patient 15). Complete abolition of the PEP was none the less much commoner among the cases with intracranial meningioma, occurring in 4 out of 5 patients.
B.S. Age: 40 30.6.72
r
Left Eye
Right Eye
5MV
L
I
1
1
FIG. 1. Pattern responses from each eye of a patient with a right sphenoidal wing meningioma showing the distortion of the normal waveform and the delayed latency of the response from the affected eye. Visual acuity was 6/9 in each eye at the time of the recording. Time scale 10, 50 and 100 ms.
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Relationship of PEP and Visual Acuity All patients except one presented with visual symptoms; in patient 15 an enlarged pituitary fossa was discovered accidentally as a result of a routine skull x-ray. In spite of the normal acuity in this case, the amplitude of the PEP from one eye was significantly reduced. In the other patients also, the incidence of abnormalities did not correlate well with the acuity level on testing. Patient 5, for instance, showed a pathologically delayed response from the right eye at a time when the acuity level was 6/6. Patient 6 had an acuity level of 6/9 in each eye, but, whereas stimulation of the left eye produced a response of normal waveform and latency, the response from the right eye was pathologically reduced and delayed. The waveform was also greatly altered (fig. 1).
VISUAL-EVOKED POTENTIALS IN COMPRESSION
363
The 6 patients with absent responses from one eye had quite a wide range of visual acuities in this eye, varying from no perception of light (patient 5) to the perception of hand movements (patients 9 and 10), 6/60 (patient 8), 6/36 (patient 7) and 6/24 (patient 18). As with multiple sclerosis and optic neuritis, abnormalities in the PEP were also found in the absence of abnormality in the corresponding visual fields (patients 5 and. 14), optic discs (patients 4, 5, 10, 12, 14, 17 and 19) and acuity (patients 4, 5, 6, 12, 13 and 15). There was one case in which all three clinical parameters were normal (patient 5). Absent Responses
Pre-operative J.N. Age: 45
17.11.72
Post-operative 4.6.73
23.5.73
I "
• ••••
Left Eye
Right Eye 5uV
..I.
FIG. 2. Pattern responses recorded on three different occasions in a patient with a right anterior clinoid meningioma. Note the alteration in waveform of the major positive component from the right eye in the first record. Visual acuity at this time was 6/9 in the right eye and there was some temporal pallor of the right optic disc. Six months later, when the second record was taken, acuity in the right eye was reduced to the perception of hand movements and the pattern response is virtually abolished; the response from the left eye shows some reduction in amplitude and loss of the initial negative component when compared with the previous recording. The post-operative recording shows a full recovery of the response from the left eye, but no return of the response from the right eye, in spite of an improvement of the visual acuity in this eye to 6/60. Time marks 10, 50 and 100 ms.
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The PEP was absent from the eye with the more reduced acuity in 6 cases, including 4 of the 5 intracranial meningiomas and 2 cases of chiasmal compression, one by a craniopharyngioma (patient 10) and one by a pituitary tumour (patient 18). In all these patients the field loss involved central vision. In patient 9, two pre-operative records were obtained at an interval of six months. In thefirstthe response on the affected side was still present but of altered waveform and reduced amplitude. Six months later it was abolished on this side (fig. 2). The values given in Table 2 are those for the second record.
364
A. M. HALLIDAY AND OTHERS
Abnormal Waveform In addition to amplitude and latency changes, the waveform of the response recorded from the mid-occipital channel was altered in many cases. As has already been mentioned, in 4 cases the distortion was so great that no meaningful measurements of latency or amplitude could be made (patients 11, 12, 13 and 14). An example of one such record is shown in fig. 3, where the major positive component appears to be completely replaced by a broad negative wave in the response from the right eye. An example of a less florid change in waveform, which made the identification of the major positive component problematical, is shown in fig. 1. Cross-correlation between the responses from the two eyes reinforced the suggestion arrived at on visual inspection, that the clear bifid positivity seen in the response from the left eye is delayed and that there is a relative loss of the earlier positivity (corresponding to the major component) in the affected right eye. In patient 9 an alteration in the shape of the major positive component, which became broadened and rounded with an ill-defined peak, was
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Reduced Amplitude of Response In addition to the 6 patients who had an absent response from one eye, a further 9 had a relatively decreased amplitude when compared with the other eye. In 4 of these the waveform was so altered that the major positivity was unrecognizable on one side, and comparable measurements could not be made; the reduction was seen as an over-all diminution in the peak-to-peak amplitude of the response on one side as compared with the other. Only where the positivity was present and measurable could its relationship to the limits of normal be defined. There is considerable variation in the amplitude of the major positive component of the response in different healthy individuals and unless the absolute amplitude is less than 20 /xV it cannot be regarded as unequivocally abnormal. However, the size of the responses from the two eyes in any given subject is usually very similar. Under the standardized conditions of the test used here the amplitude ratio of the major positive component from the two eyes in 30 healthy individuals had a mean of 1 03 and a standard deviation of 0-15. Comparison of the responses from the two eyes in a given patient may thus allow identification of a unilateral reduction in amplitude which exceeds that of the normal population at either the 5 per cent or the 1 per cent level. Such a difference was observed in patients 2, 3, 4, 6 and 15. In patients 3 and 4 a reduction in amplitude was the only abnormality in the PEP. No probability level can, of course, be assigned to the marked amplitude difference observed in the 4 other cases in whom no major positivity could be identified (patients 11,12,13 and 14). It is notable that the pattern response was either absent or reduced on one side in all except one of the cases with orbital tumours, meningiomas or craniopharyngiomas. Even the one exception (patient 1) had a smaller amplitude in the affected eye, although this did not quite exceed the limits of normal variability at the 5 per cent level of probability.
VISUAL-EVOKED POTENTIALS IN COMPRESSION
365
I.G. Age: 58 28.2.74 Left Eye
5MV
FIG. 3. Pattern responses from each eye of a patient with a pituitary adenoma. VAL 6/6, VAR 6/36. Note the grossly altered waveform of the response from the right eye with loss of the major positive component and a reduction in the over-all amplitude. The response from the left eye, which has a reasonably well-preserved waveform, is pathologically delayed.
the earliest change recorded in association with a right anterior clinoid meningioma (fig. 2, left-hand record), and was seen at a time when the visual acuity was only slightly reduced to 6/9 in the right eye. Six months later, when vision had deteriorated to the perception of hand movements, the response from this eye was virtually abolished (fig. 2, middle record). After surgical removal of the tumour, the vision in this eye improved slightly to 6/60, but the response remained absent (fig. 2, right-hand record). Abnormal Distribution of Responses In addition to alterations of the waveform recorded from the mid-line channel, the lateral distribution of the response evoked from one or other eye was often asymmetrical. Examples are illustrated in figs. 4 and 5 (pre-operative records). The PEP from patient 17, for instance, showed a marked asymmetry pre-operatively, the major positive component being clearly present at the electrodes 5 and 10 cm to the left of the mid-line, whereas there was a relative flattening of the response from the right side of the head (fig. 4, left hand records). This pattern was associated with an acuity of 6/5 in each eye, but there was an incongruent right homonymous hemianopia. The left-sided positivity here presumably corresponds to pattern stimulation of the preserved left half of the visual field. An ipsilateral positivity is characteristic of stimulation of those areas of the halffieldadjoining the horizontal meridian (Halliday, 19726; Halliday, Barrett, Halliday and Michael, 1976).
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Right Eye
A. M. HALLIDAY AND OTHERS
366
Post-operative
Pre-operative Left Eye
i.........i.
i
.......i
.
Right Eye
i.........i
Common reference
MA Age: 50
10 uV
FIG. 4. Pre-operative and post-operative pattern responses recorded from each eye of a patient with a pituitary tumour. The pre-operative records show a clear uncrossed asymmetry in the occipital distribution of the response, which has a left-sided predominance whichever eye is stimulated. The patient had an incongnient right homonymous hemianopia. Note the loss of asymmetry following the operation; however, the amplitude of the response from the left eye is significantly reduced, and the acuity in this eye was reduced from 6/5 to 6/9. In the pre-operative record there is a suggestion of a phase reversal of the positivity in the channel furthest out on the right side.
Hence, both visual field defect and evoked response suggest a lesion of the left optic tract. At subsequent operation the left optic nerve was reported to be pushed right forward by a tumour mass between it and the carotid. The chiasm was prefixed. Patient 10 had an absent response from the left eye, where vision was reduced to the perception of hand movements (fig. 5, left hand record). In the right eye, which had an acuity better than 6/12, there was a temporal cut sparing the mid-line. The mid-line and contralateral occipital response was small but of normal latency, while the channels ipsilateral to the stimulated eye showed a small but well-formed negative component occurring a few milliseconds later than the mid-line positivity and followed by a positive wave. This may represent either an asynchronous phase reversal of the mid-line response on this side or a rather more delayed positivity. Delayed positivities in the channels ipsilateral to the stimulated eye were seen clearly in 5 cases (patients 5, 10, 15, 16 and 19) and doubtfully in a further 2 (patients 6 and 18). In 2 of the patients this took the form of a crossed asymmetry,
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.
Left Eye
Right Eye
VISUAL-EVOKED POTENTIALS IN COMPRESSION Post-operative
Pre-operative Left Eye
367
Right Eye
Left Eye
Right Eye
J.D. Age: 29
|
5 M
V
FIG. 5. Pre-operative and post-operative pattern responses in a patient with a craniopharyngioma. There is no response pre-operatively from the left eye, in which the visual acuity was reduced to the perception of hand movements. In the right eye the response is small and asymmetric, the reduced major positivexomponent appearing at normal latency in the mid-line and left-sided channels, while the channels to the right of the mid-line show a slightly later negative component followed by a positivity. Acuity in the right eye was better than 6/12 and there was a temporal field defect sparing the mid-line. Post-operatively both responses are markedly improved, paralleling the return of normal acuity.
the delayed ipsilateral positivity being seen for stimulation of either eye, but on opposite sides. The patient who showed this more clearly (patient 19) had a bitemporal hemianopia; the other patient (patient 16) had a temporal hemianopia in the right eye, while in the left eye islands of vision were preserved in the upper nasal and lower temporal quadrants. Such crossed asymmetries were in contrast to the uncrossed asymmetries seen in patient 17 (fig. 4) and in one other case (patient 12). In these the pattern of asymmetry was similar for stimulation of each eye. In patient 17 the left optic tract was compressed, producing an incongruent right homonymous hemianopia. Patient 12 had incongruent partial right field defects, viz. a nasal hemianopia in the left eye and an upper temporal cut in the right eye. Two further cases had doubtful asymmetries (patients 11 and 18), the first associated with a left homonymous hemianopia, the second with a bitemporal hemianopia. Two patients gave asymmetric responses from one eye in the absence of any associated field defect (patients 5 and 14).
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Common reference
368
A. M. HALLIDAY AND OTHERS
Increased Latency of Response In 4 patients (patients 2, 5, 6 and 13) there was a clear-cut delay in the mid-line response, which had a recognizable major positive component. In 2 other cases (1 and 18) the latencies were at the upper end of normal for the patient's age. Moreover, one further patient who had latencies within the normal range showed a 9 ms difference between the latency of the response from the two eyes (patient 1). In patient 6 (sphenoidal wing meningioma) a delayed response of reduced amplitude was associated with some distortion of the waveform (fig. 1). Because of the difficulty of recognizing the major positive component in this record, latency measurements were also carried out using a cross-correlation technique. This .confirmed the cursor measurements given in Table 2. In at least one other instance there was difficulty in distinguishing between a change in the waveform and a true delay. The details given in Table 2 for patient 9, who had an anterior clinoid meningioma, are those for the immediate pre-operative record, and, as already mentioned, a previous record had been taken six months before (fig. 2). At the time of thefirstrecording the response from the right eye was still present and had a clearly recognizable major positivity of altered waveform, measuring 61 ^.V. Formal measurements of the peak suggested that this was slightly delayed (122 ms), but inspection will show that the distinction between a true delay and a broadening of the waveform is almost a semantic one, the onset of the major positivity being hardly any later than on stimulation of the unaffected eye. The acuity of the right eye at the time was 6/9 and there was already temporal pallor of the optic disc. The longest latency recorded in this series of patients was 137 ms (patient 13) and none of the patients was delayed more than 20 ms beyond the upper limit of the normal latency range for their age. This is in contrast to the earlier results
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Asymmetries occurred in the response from one eye where the response from the other eye was either absent (patients 5, 10 and 18) or normal (patients 15 and 6). It is clearly only when both eyes showed asymmetries that these could be characterized as either crossed (patients 16 and 19) or uncrossed (patients 12 and 17). Even when this was so, however, the waveform could be so abnormal and so different for the two eyes that this differentiation was impossible (patient 14). Overall, 9 patients showed a clear asymmetry (patients 5, 6, 10, 12, 14, 15, 16, 17 and 19) and there were some less definite asymmetrical features in another 2 (11 and 18). Five of the 9 cases with marked asymmetry had evidence at operation of involvement of the chiasm (10, 12, 15, 16 and 19) and in 2 others both optic nerves were involved (6'and 14). In patient 5, who had a sphenoidal wing meningioma, the operation note did not mention the state of the chiasm or the optic nerve from the eye with surviving vision. It is of interest that the potential from this eye (which was clinically otherwise normal) was markedly delayed, indicating that the nerve fibres from it had been damaged.
VISUAL-EVOKED POTENTIALS IN COMPRESSION
369
in optic neuritis and multiple sclerosis, where the mean delays were of the order of 35 to 45 ms and the actual delays encountered in individual patients ranged up to 100 ms. Combination of Abnormalities In half the abnormal cases there were multiple abnormalities in the PEPs, and in the 9 abnormal cases with only a single defect, these defects were gross in 7 (either absent response or marked asymmetry).
DISCUSSION
The results on this series of 19 patients with compressive lesions of the anterior visual pathways demonstrate clearly that compression can produce a variety of abnormalities in the pattern-evoked response, and that pathologically altered responses are common. In only one of the present series of cases was the pattern response within normal limits. If the present series is representative, over 90 per cent of patients with compressive lesions can be expected to give abnormal responses. It therefore appears that in this context too, as in primary demyelinating disease, the pattern response may prove to be very much more sensitive than the traditionally usedflashresponse (see Halliday (1975) for a review of the literature). In early cases the pattern response may be significantly altered, even where other clinical signs of visual impairment (visual acuity, fields and fundi) are unaffected.
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Effect of Operation on the PEP Table 3 shows a comparison of the pre- and post-operative records in 9 patients. In 3 there was a marked improvement in the responses, with a loss of a pre-operative asymmetry, accompanied by a return of normal acuity (patients 10, 14 and 16). The dramatic change in the PEPs in Case 10 is shown in fig. 5. The previously absent response from the left eye has returned following the operation, paralleling the improvement of visual acuity in this eye from the perception of hand movements to 6/5. The amplitude of the response in the right eye has also greatly increased with the improved acuity level (6/12 to 6/5), and the previous asymmetry has largely disappeared, although there is still a trace of it. Patient 17 also demonstrated a similar loss of asymmetry post-operatively in the response from both eyes, but the amplitude of the response from the left eye had significantly diminished, paralleling a loss of acuity from 6/5 to 6/9 (fig. 4). Three of the patients were unchanged by the operation (patients 8, 9 and 18) in spite of some change in the acuity level (fig. 2). The 2 other patients were definitely worse (patients 13 and 19) with either loss of the response from one eye, or an increase in the latency and the development of a marked asymmetry. It is clear that with regard to the prognosis for vision, the patients with craniopharyngiomas or pituitary tumours did rather better than those with intracranial meningiomas.
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TABLE 3. CHANGES IN VISUAL ACUITY AND PATTERN EVOKED RESPONSES BETWEEN PRE-OPERATIVE AND POST-OPERATIVE RECORDINGS Vision L
Amplitude R
L
Latency R
L
R
Supraseltar meningloma 8 B. M. 9J.N.
6/9-+6/9 6/6-1-6/5
Craniopharyngioma 10 J. D.
6/60->-NPL HM-K6/60
8-8-+9-8 5-9 ->• 8-4
0 -+ 0 0 -+ 0
104-1-105 UO-n-107
6/12H—• 6/5
0->-3-9
3-3 —• 6 1
6-2 -+ 6-3
GAW ->• 0
• 103
97 —• 129
121 - * 118
17 M. A.
6/5 --4-7
4-6 ->• 5 5 4-3 —6/5
Change m PEP
GAW-)-—
G A W -t- 108
Both responses improved. Pre-operative asymmetry in R. eye response gone
£j
Worse. Grossly abnormal pre-operative response from R. eye abolished post-operatively. L eye response shows slight latency increase and development of marked asymmetry Both responses improved with return to normal waveform and loss of asymmetry Responses improved with loss or asymmetry from each eye. Slight increase in latency in L. eye response Decreased amplitude in L. eye response postoperatively. Loss of asymmelry in the response from each eye ISQ Marked latency increase in both responses posloperativcly
CF = able to count fingers HM = ablc to perceive hand movements
2 X ^ f~
NPL"»no perception of light.
> **• }> 2 O Q H X 2 ^
VISUAL-EVOKED POTENTIALS IN COMPRESSION
371
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The character of the changes encountered in the evoked responses was, however, very different from that seen in the earlier studies on primary demyelinating disease (Halliday, McDonald and Mushin, 1972, 1973a, 1973d). The incidence of delayed responses was surprisingly small (only 4 out of the 19 patients), although the over-all incidence of delay may be masked by the relatively large number of cases in which the response was abolished altogether (as was the case in 6 patients). The serial recordings made on patient 9 and illustrated in fig. 2 suggest that a delayed response may be encountered in the early stages of compression, but may disappear when the amplitude is reduced by the further progress of the lesion. Quite apart from their over-all incidence, the delays encountered differed from those seen in the majority of the patients with demyelinating disease in that they were relatively much smaller. The maximum latency encountered for the major positive component (137 ms in patient 13) only approaches the mean delay of the earlier group. With such a small incidence of delays, however, it is probably unwise to draw any firm conclusions from these results. Only one of the 4 patients with delays was recorded post-operatively; in this patient (13) the acuity in the left eye remained normal and the latency showed a slight increase from 137 ms to 144 ms. The response also developed a marked asymmetry. All that can be said is that the surgical decompression was not associated with a return to normal latency in this case. In addition to the different pattern of delays encountered in this group, there was also a much higher incidence of alterations in the waveform of the response than was encountered in the group with primary demyelinating disease. Minor changes in the waveform of the delayed positivity were certainly encountered in the latter, a broadening and loss of definition being particularly characteristic, but the gross changes in waveform seen in some of the present series of patients, which rendered the major positive component unrecognizable, are not typical of optic neuritis. Nor are the less extreme distortions of the normal waveform, exemplified in fig. 1, at all typical of primary demyelinating disease in our experience. No single change in the pattern response appears, however, to be pathognomonic of compression or of primary demyelination. Delayed latency, altered waveform and reduced amplitude may be met equally in both conditions. It is possible that the prolonged latency may eventually prove to be specifically associated with demyelination of the fibres of the afferent visual pathway, but demyelination can be encountered in association with a number of different pathologies and is not confined to multiple sclerosis or optic neuritis. The higher incidence of binocular abnormalities in the tumours arising in the region of the sella turcica no doubt reflects the increased involvement of chiasmal and post-chiasmal fibres. The majority of the asymmetries were associated with field defects, but in at least two instances, clear asymmetries were seen in the absence of any clinical defect in the eye concerned. None the less, an association emerged between a pattern of crossed asymmetry, typical of cases with bitemporal hemianopia, in contrast to a pattern of uncrossed asymmetry, typical of the cases o
372
A. M. HALLIDAY AND OTHERS
Mechanism of PEP Abnormalities The independence of latency and amplitude changes, already noted in the earlier series (Halliday, McDonald and Mushin, 1973a, 1974a) is an even more striking feature of the present results. It suggests that more than one mechanism must be at work. It has already been suggested that the amplitude changes may reflect in large measure the conduction block in damaged fibres, whereas the delay may reflect the slowed conduction through demyelinated segments of the nerve fibres (Halliday, McDonald and Mushin, 1974a, 1976). Demyelination occurs in the spinal cord as a result of both acute and chronic compression (Holmes, 1906; Gledhill, Harrison and McDonald, 1973), and it seems likely that the same is true for the visual system. A detailed discussion of possible mechanisms for the abnormalities in visual evoked potentials is given by McDonald (1976).
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with homonymous hemianopia. Further consideration of the relationship between the half-field stimulated and asymmetries of the pattern response will be taken up in another paper (Barrett, Blumhardt, Halliday, Halliday and Kriss, 1976). Marked improvement in the pattern evoked response following operation was seen in 3 of the patients (10,14 and 16), all of whom lost a pre-operative asymmetry. An increase in the latency of the response was seen in 3 patients. In 2 (13 and 16) there was an increase of 6 to 7 ms in a previously delayed response; in the third (19) the responses from both eyes, which had been of normal latency pre-operatively, became markedly delayed. The present series was selected on the basis of operatively proven compression and for the most part represents relatively advanced cases. However, in patient 5 (sphenoidal wing meningioma) and 14 (pituitary adenoma) abnormal responses were recorded from the clinically normal eye. This indicates that, as in multiple sclerosis, damage to optic nerve fibres may be detected by the pattern evoked response test before any of the standard clinical tests are abnormal. The pattern of abnormalities encountered in this series of patients showed certain broad correlations with the pathology. Characteristic of intra-orbital tumours was a reduction in amplitude of the response from the affected eye; only one of the 4 cases was delayed. In intracranial meningiomas there was again a preponderance of uniocular abnormalities in the PEP and a particularly high incidence of absent responses in the affected eye (4 out of 5). Both the patients with sphenoidal wing meningiomas also had a pathologically delayed response. In the craniopharyngiomas and pituitary tumours, both arising in the region of the sella turcica, the pattern response was abnormal in both eyes in the vast majority of patients (9 out of 10). All the cases with gross change in the normal waveform were encountered in this group (4 out of 10) and asymmetries in the occipital distribution of the response were typical (9 out of 10).
VISUAL-EVOKED POTENTIALS IN COMPRESSION
373
SUMMARY
ACKNOWLEDGEMENTS Our thanks are due to the Physicians and Surgeons of the National Hospitals and Moorfields Eye Hospital for allowing us to study their patients. We should also like to thank J. R. Pitman for invaluable technical assistance. REFERENCES ARDEN, G. B. (1973) The visual evoked response in ophthalmology. Proceedings of the Royal Society of Medicine, 66, 1037-1043. ASSELMAN, P., CHADWICK, T. W., and MARSDEN, C. D. (1975) Visual evoked responses in the diagnosis and management of patients suspected of multiple sclerosis. Brain, 98, 261-282. BARRETT, G., BLUMHARDT, L., HALLIDAY, A. M., HALLIDAY, ELBE, and KRISS, A. (1976) A paradox
in the lateralisation of the visual evoked response. Nature, London, 261, 253-260. BEHRMAN, JOAN, HALLIDAY, A. M., and MCDONALD, W. I. (1972) Visual evoked responses to flash
and pattern in patients with retrobulbar neuritis. Electroencephalography and Clinical Neurophysiology, 33, 445. FETNSOD, M., ABRAMSKY, O., and AUERBACH, E. (1973) Electrophysiological examinations of the visual
system in multiple sclerosis. Journal of Neurological Sciences, 20, 161-175. and HOYT, W. F. (1975) Subclinical optic neuropathy in multiple sclerosis. Journal of Neurobgy, Neurosurgery and Psychiatry, 38, 1109-1114. GLEDHILL, R. F., HARRISON, B. M., and MCDONALD, W. I. (1973) Demyelination and remyelination
after acute spinal cord compression. Experimental Neurology, 38, 472-487. HALUDAY, A. M. (1972a) Evoked responses in organic and functional sensory loss. In: Activitis evoquies et leur conditionement chez Thomme normal et en pathologie mentale. Edited by A. Fessard and G. Lelord. Paris: Editions INSERM, pp. 189-212. (1972A) Spatial contrast evoked potentials; component analysis and topology. Trace, 6, 39-46. (1972c) Spatial contrast evoked potentials: clinical applications. Trace, 6, 94-99. (1975) The effect of lesions of the visual pathway and cerebrum on the visual evoked response. In: Evoked Potentials. Handbook of Electroencephalography and Clinical Neurophysiology. Edited by W. S. van Leeuwen, F. H. Lopes da Silva and A. Kamp. Vol. 8A. Amsterdam: Elsevier, pp. 119-129.
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Pattern evoked responses have been recorded in 19 patients with compression of the optic nerve, chiasm or tract, verified at operation. These included 4 patients with orbital tumours, 5 with intracranial meningiomas, 2 with craniopharyngiomas and 8 with pituitary tumours. The evoked response was abnormal in all except one of these patients. Trie pattern of abnormalities in the response, however, differed from that in the earlier series of patients with primary demyelinating disease. The incidence of delayed responses was much lower, and the magnitude of the delays was smaller. Absent responses were particularly characteristic of patients with intracranial meningiomas. Tumours arising in the region of the sella turcica were associated with a high incidence of abnormalities of the waveform of the response, and asymmetry of the field of the occipital evoked potential was especially characteristic of this group. Most, but not all, asymmetric cases were associated with field defects.
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HALUDAY, A. M. (1976) Visually evoked cortical potentials in neurological diagnosis. In: Scientific Aids in Hospital Diagnosis. Edited by J. P. Nicholson. New York and London: Plenum Press. In press. BARRETT, G., HALLIDAY, ELISE, and MICHAEL, W. F. (1976) The topography of the pattern
evoked potential. In: New Developments in Visual Evoked Potentials in the Human Brain. Edited by J. F. Desmedt. London: Oxford University Press. In press. HALLIDAY, ELISE, KRISS, A., MCDONALD, W. I., and MUSHIN, JOAN. (1976a) Changes in
(Received November 26,1975)
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the pattern evoked response in compressive lesions of the anterior visual pathways. Electroencephalography and clinical Neurophysiology, 40, 541. (19766) Abnormalities of the pattern evoked potential in compression of the anterior visual pathways. Australian Journal of Ophthalmology. In press. MCDONALD, W. I., and MUSHIN, JOAN (1972) Delayed visual evoked response in optic neuritis. Lancet, 1, 982-985. (1973a) Delayed pattern-evoked responses in optic neuritis in relation to visual acuity. Transactions of the Ophthalmological Society of the UK, 93, 315-324. (1973/?) The use of pattern-evoked responses in the diagnosis of demyelinating disease. Proc. 8th Intemat. Cong. Electroenceph. clin. Neurophysiol. Marseilles. Electroencephalography and Clinical Neurophysiology, 34, 710. (1973c) The incidence of delayed pattern-evoked responses in multiple sclerosis. Proceedings of the 10th International Congress of Neurology. Barcelona: Excerpta Medica. ICS296, 150. (1973a") Visual evoked response in diagnosis of multiple sclerosis. British Medical Journal, 4, 661-664. (1974a) The dissociation of amplitude and latency changes in the pattern-evoked response following optic neuritis. Electroencephalography and Clinical Neurophysiology, 36, 218. " (1974ft) The value of the pattern-evoked response in the diagnosis of multiple sclerosis. Electroencephalography and Clinical Neurophysiology, 36, 551-553. (1974c) Delayed visual evoked responses in progressive spastic paraplegia. Electroencephalography and Clinical Neurophysiology, 37, 328. (\974d) Delayed pattern evoked responses in progressive spastic paraplegia. Neurology (Minneapolis), 24, 360-361. (1976) Visual evoked potentials in patients with demyelinating disease. In: New Developments in Visual Evoked Potentials in the Human Brain. Edited by J. F. Desmedt. London: Oxford University Press. In press. HOLMES, G. (1906) On the relation between loss of function and structural change in focal lesions of the central nervous system, with special reference to secondary degeneration. Brain, 29, 514-523. MCDONALD, W. I. (1976) Pathophysiology of conduction in central nerve fibres. In: New Developments in Visual Evoked Potentials in the Human Brain. Edited by J. F. Desmedt. London: Oxford University Press. In press. MILNER, B. A., REGAN, D., and HERON, J. R. (1974) Differential diagnosis of multiple sclerosis by visual evoked potential recording. Brain, 97, 755-772. NAMEROW, N. S., and ENNS, N. (1972) Visual evoked responses in patients with multiple sclerosis. Journal of Neurology, Neurosurgery and Psychiatry, 35, 829-833. RICHEY, E. T., Kooi, K. A., and TOURTELLOTTE, W. W. (1971) Visually evoked responses in multiple sclerosis. Journal of Neurology, Neurosurgery and Psychiatry, 34, 275-280.
THE PATTERN-EVOKED POTENTIAL IN COMPRESSION OF THE ANTERIOR VISUAL PATHWAYS by A. M. HALLIDAY, ELISE HALLIDAY, A. KRISS, W. I. MCDONALD and JOAN MUSHIN
INTRODUCTION
DEMYELINATION in the optic nerve produced by optic neuritis or multiple sclerosis produces a persistent increase in the latency of the potential evoked in the occipital cortex by pattern stimulation of the retina (Behrman, Halliday and McDonald, 1972; Halliday, 1972a, c, 1976; Halliday, McDonald and Mushin, 1972, I973a-d, \914a-d, 1976; Arden, 1973; Milner, Regan and Heron, 1974; Asselman, Chadwick and Marsden, 1975). Some evidence of delay can also be demonstrated byflashstimulation (Richey, Kooi and Tourtellotte, 1971; Namerow and Enns, 1972; Feinsod, Abramsky and Auerbach, 1973; Feinsod and Hoyt, 1975) but the most striking and consistent results have been obtained with a reversing checkerboard of black and white squares as the retinal stimulus. The method of pattern reversal shows that over 90 per cent of the patients with optic neuritis, and between 60 and 90 per cent of patients with clinically definite MS, have delays, even in the absence of the usual clinical signs of optic nerve disease (Halliday, McDonald and Mushin, 1973a, d; Asselman et ai, 1975). The evoked potential method thus provides the most sensitive means at present available for detecting subclinical lesions of the optic nerve. As such, it is being used increasingly as an aid to the early diagnosis of multiple sclerosis. Since the method has begun to come into routine clinical use, there has been a tendency to imagine that delays are specific to multiple sclerosis and optic neuritis. We have, however, repeatedly emphasized that this is not the case (Halliday et ai, 1973a1, 1976), and in this paper we present our findings in 19 patients with operatively proven compression of the optic nerve, chiasm or tract. The evoked response was abnormal in 18 of them. A preliminary account of this investigation has appeared elsewhere (Halliday, Halliday, Kriss, McDonald and Mushin, 1976a, b).
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(From the Medical Research Council, Institute of Neurology, National Hospital, Queen Square, London WC1)
358
A. M. HALLIDAY AND OTHERS CLINICAL MATERIAL
Since our aim was to establish whether or not compression of the nerve fibres in the optic nerve, chiasm or radiation affected the pattern-evoked potential, we have restricted the clinical material to operatively proven cases of compression. We have examined 19 such cases (Table 1). Four patients had tumours confined to the orbit; 5 patients had an intracranial meningioma, 2 arising from the sphenoid wing and 3 from the region of the anterior clinoid process (suprasellar); 2 patients TABLE 1. PRESENTING SYMPTOMS IN THE 19 PATIENTS WITH COMPRESSIVE LESIONS INCLUDED IN THIS STUDY
Mode of presentation
Se.
47
M
Proptosis and visual distortion nine months
58
M
43
F
Proptosis. Previous excision meningioma one year earlier. Proptosis recurred with blurred vision Blurring of vision one year. Proptosis six months
52
F
Blurring vision plus proptosis ten months
48
F
40
F
Episode of aphasia one year ago. Visual loss three months Diplopia five years. Blurring of vision three years
45
F
59 46
F F
Craniopharyngioma 10 J. D.
29
M
11 N. S.
44
F
Pituitary tumour 12 P. H.
30
M
13 I. G. 14 E. P. 15 L. G.
58 46 57
F F M
16 H. P.
60
M
17 M. A. 18 C. D. 19 A. J.
50 56 39
F F M
Sphenoidal wing meningioma 5 J. G. 6 B. S. Suprasellar meningioma 7 J. B. 8 B. M. 9 J. N.
Right-sided headache three years. Deterioration in vision one year Blurring of vision one year Blurring of vision ten months Fluctuating L. visual loss nine months. Blurring R. vision one month Headaches and visual loss one year Episode of headache and blurring vision thirteen months ago and blurring vision five weeks Visual deterioration nine months Blurring vision two months Asymptomatic. Accidental discovery of enlarged pituitary fossa Impotence two years. Sudden severe headache and visual loss eleven weeks Visual loss two and a half months Blurring of vision two years Headache eight years. Hypopituitarism seven years. Increasing headache and diplopia six years. Visual loss five months
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Age
Case No. and site Orbital 1 R. B. Cavernous hsemangioma 2 A. S. Neurilemmoma 3 I. H. Meningioma 4 L. H. Cavernous haemangioma
VISUAL-EVOKED POTENTIALS IN COMPRESSION
359
had a craniopharyngioma and 8 had pituitary tumours. Four of the latter were histologically proven adenomas (patients 12-15), but in 4 the histology, although consistent with adenoma, was indecisive (patients 16-19). METHOD
Parameters Studied The peak latency of the major positive wave at the mid-occipital electrode, and its peak-to-peak amplitude measured from the immediately preceding negative wave, was determined in every record in which this component could be identified. The form of the potential and its distribution in the occipital region was also noted. Measurements of the latency and amplitude were more difficult in this series of patients with compressive lesions than in the patients with optic neuritis and multiple sclerosis. In the latter group of patients the normal waveform of the response was usually preserved, even when the potential was markedly delayed, and a well-defined positivity was generally recorded at the mid-line occipital electrode. In the present series of patients, however, two types of alteration in the potential made meaningful measurements difficult in some cases and impossible in others. First, the waveform of the response recorded from the mid-occipital electrode was sometimes so much altered that the positive peak was ill-defined or absent, and no precise latency measurements could be made (compare, for instance, the waveform of the response from the affected and unaffected eyes in figs. 1 and 3). Secondly, the distribution of the response was altered and became asymmetric in some cases; in this event significant features were missed if attention was confined to measurements of the response from the mid-occipital electrode (see, for instance, figs. 4 and 5). None the less, the values for latencies and amplitudes given in Tables 2 and 3 are all based on records from the mid-line electrode. We have deliberately chosen to do this for several reasons. First, this is the electrode at which the response is normally largest and best defined, and the values can be compared directly with our previous observations on patients with retrobulbar neuritis and multiple sclerosis (Halliday, McDonald and Mushin, 1972, 1973a). Secondly, many departments of clinical neurophysiology which are introducing the evoked
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The technique was similar to that used in the earlier studies on multiple sclerosis (Halliday, McDonald and Mushin, 1972, \973d). The patient sat facing a circular translucent screen, subtending 32° at the eye, on to which was back-projected the slide of a black-and-white checkerboard. The individual squares subtended 50 minutes and the brightness levels were 227 cd/m2 for the white squares and 8-2 cd/m2 for the black squares. The white squares were about twice as bright as those used in the earlier studies. The recordings were made stimulating each eye separately, with the other eye covered with an eye pad, the subject being asked to fixate a small spot of light in the centre of the screen while the response was being averaged. Pattern reversal was produced, once every 600 ms, by a rapid lateral displacement of the checkerboard through one square (the transition taking approximately 10 ms). The occipital potentials were averaged, using a PDP-12 computer, which was triggered by the pattern reversal. The average response to 100 complementary reversals (200 pattern changes) was recorded at least twice for each eye. The response was measured from a recording made with a mid-occipital/mid-frontal electrode montage, the mid-occipital electrode being placed 5 cm above the inion. In addition, recordings were also made from electrodes 5 cm and 10 cm to the left and right of the mid-line occipital channel, also referred to the common mid-frontal reference. A sixth electrode was placed in the mid-line 5 cm below the inion. In certain cases, where the field of the potential was studied in more detail, the responses were averaged from a larger montage of up to 16 occipital electrodes. In a number of patients flash responses were also recorded. Visual acuity was measured at the time of the recording with a Snelien card, and, where appropriate, field defects were charted on a Goldman perimeter.
360
A. M. HALLIDAY AND OTHERS
potential technique in the routine assessment of visual function, record only the mid-occipital channel because of the limited channel capacity of their small on-line averagers, and we wish to give some idea of the frequency and type of abnormality that may be detected with relatively simple equipment at a recording session of reasonable length.
RESULTS
TABLE 2. PATTERN EVOKED RESPONSE FINDINGS Side of lesion
L
R
Amplitude L R
L
Orbital 1 R. B.
L
6/24
6/9
6-8
9-6
115
106
2 AS.
L
6/36
6/5
5-7
13-9
127
117
3 I. H.
R
6/5
6/36
10-6
6-3
98
101
4 L. H.
L
6/6
6/9
11 5
18-3
102
98
L
NPL
6/6
79
-
127
R
6/9
6/9
110
104
134
C
6/5
6/36
14-5
0
100
R R
6/9 6/6
6/60 HM
8-8 5-9
0 0
104 110
Cranlopharyngloma 10 J. D.
C
HM
6/12 +
11 N. S
C
6/5
6/12
Sphenoidal wing meningioma 5 J. G.
6 B. S. Suprasellar meningioma 7 J. B. 8 B. M. 9 J. N.
Acuity
5-0
Latency R
3-3
-
GAW
93
Comments Not definitely beyond normal bnuts Marginal increase in latency of L eye response compared with other eye (9 ms difference). Major component of smaller amplitude and slightly altered waveform Reduction in amplitude (P < 0-001) and delay in L. eye response Reduction in amplitude ( P < 0 0 5 ) in R. eye Reduction in amplitude of L. eye response ( P < 0-001) associated with marked decrease of preceding negative wave
Responses from both eyes abnormal. Absent response from L. eye Asymmetrical and delayed response from R. eye (normal acuity) Reduced ( P < 0 001), asymmetrical and delayed response from R eye Absent pattern response and definitely delayed flash response from R. eye Absent response from R. eye 2nd record—Absent response from R. eye; marked deterioration since 1st record six months before (1st record showed an abnormal response from R. eye with greatly broadened positivity)
97
Responses from both eyes abnormal. Absent response from L eye Small asymmetrical response from R. eye GAW Responses from both eyes abnormal. Small asymmetrical responses, with grossly abnormal waveform from R. eye
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Table 2 gives the amplitude and latency measurements of the major positive component of the pattern evoked potential from each eye, recorded at the mid-occipital electrode for the 19 patients listed in Table 1. The visual acuity in each eye is also noted. Definitely abnormal values appear in bold type in the table, borderline abnormalities being indicated by italics. Under 'comments' are noted any asymmetries in the distribution of the response and any notable abnormalities in its waveform.
VISUAL-EVOKED POTENTIALS IN COMPRESSION
361
TABLE 2 (cont.) Side of Acuity lesion L Pituitary tumour 12 P. H.
C
L
Amplitude R
Latency L
6/6
GAW
GAW
GAW
13 I. G.
6/6
6/36
6-2
GAW
137
14 E. R.
6/9
6/36
GAW
GAW
GAW
15 L. G.
6/6
6/6
5-4
101
116
16 H P
6/6
6/5
55
6-9
123
17 M A.
6/5
6/5
22-4
241
107
18 C D.
6/24
6/18
0
4-6
—
19 A. J
6/18pt
6/9pt
37
4-3
113
Comments
GAW Responses from both eyes abnormal Very small abnormal response from L. eye. Larger response from R eye with marked asymmetry GAW Responses from both eyes abnormal. Delayed response from L eye. Small abnormal response from R. eye GAW Responses from both eyes abnormal. Asymmetrical responses from both eyej. The response from the right eye is of much smaller amplitude 109 Reduced response from L eye (P < 005) with abnormal waveform (broad posiuvity) and marked asymmetry. Normal response from R. eye 121 Responses from both eyes abnormal. Asymmetrical response from each eye 105 Responses from both eyes abnormal Asymmetrical response from each eye 124 Responses from both eyes abnormal. Absent response from L eye. Small delayed, asymmetrical response from R. eye 111 Responses from both eyes abnormal. Asymmetrical responses from each eye
GAW = grossly abnormal waveform. Definitely abnormal values are printed in bold type, borderline abnormalities in italics.
. Abnormal PEPs were found in 18 of the 19 cases with proven compression (95 per cent). The single case with a normal response (patient 1) had an intracranial cavernous haemangioma of the left orbit, and visual acuity was reduced in the left eye to 6/24. Although not beyond normal limits, the response from the affected eye showed a marginal increase in latency (9 ms) compared with the other eye, and the major component was of smaller amplitude and slightly altered waveform. A variety of more definite abnormalities was found in the remaining cases. The other 3 patients with intra-orbital lesions all showed a significantly smaller amplitude of response from the affected eye (Table 2). In one case (patient 2), where there was an orbital neurofibroma, the positivity was also abnormally delayed. The reduction in amplitude in patients 3 and 4 was associated with a major positive peak of entirely normal latency and waveform. In patient 4 the reduction in amplitude of the major positive component was largely due to a loss of the preceding negative peak from which it was measured. In the 4 patients with intra-orbital tumours, the abnormality was limited to the response from the affected eye. The remaining 15 patients had intracranial space-occupying lesions, 2 arising from the sphenoidal wing and the remainder from the region of the sella turcica, and in this group the responses from more than one eye could be affected. Of the 5 intracranial meningiomas, the majority
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CF
R
362
A. M. HALLIDAY AND OTHERS
had only a uniocular abnormality of the PEP, and only one had definitely abnormal responses from each eye (patient 5). Serial recording suggested, however, that patient 9 also showed a slight alteration in the response on the less affected side, as compared with a previous record six months before {see fig. 2). In contrast to the meningiomas, 9 of the 10 patients in whom compression of the visual pathway arose from an extension of either an intrasellar or parasellar tumour had marked abnormalities in the response from both eyes (the exception being patient 15). Complete abolition of the PEP was none the less much commoner among the cases with intracranial meningioma, occurring in 4 out of 5 patients.
B.S. Age: 40 30.6.72
r
Left Eye
Right Eye
5MV
L
I
1
1
FIG. 1. Pattern responses from each eye of a patient with a right sphenoidal wing meningioma showing the distortion of the normal waveform and the delayed latency of the response from the affected eye. Visual acuity was 6/9 in each eye at the time of the recording. Time scale 10, 50 and 100 ms.
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Relationship of PEP and Visual Acuity All patients except one presented with visual symptoms; in patient 15 an enlarged pituitary fossa was discovered accidentally as a result of a routine skull x-ray. In spite of the normal acuity in this case, the amplitude of the PEP from one eye was significantly reduced. In the other patients also, the incidence of abnormalities did not correlate well with the acuity level on testing. Patient 5, for instance, showed a pathologically delayed response from the right eye at a time when the acuity level was 6/6. Patient 6 had an acuity level of 6/9 in each eye, but, whereas stimulation of the left eye produced a response of normal waveform and latency, the response from the right eye was pathologically reduced and delayed. The waveform was also greatly altered (fig. 1).
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The 6 patients with absent responses from one eye had quite a wide range of visual acuities in this eye, varying from no perception of light (patient 5) to the perception of hand movements (patients 9 and 10), 6/60 (patient 8), 6/36 (patient 7) and 6/24 (patient 18). As with multiple sclerosis and optic neuritis, abnormalities in the PEP were also found in the absence of abnormality in the corresponding visual fields (patients 5 and. 14), optic discs (patients 4, 5, 10, 12, 14, 17 and 19) and acuity (patients 4, 5, 6, 12, 13 and 15). There was one case in which all three clinical parameters were normal (patient 5). Absent Responses
Pre-operative J.N. Age: 45
17.11.72
Post-operative 4.6.73
23.5.73
I "
• ••••
Left Eye
Right Eye 5uV
..I.
FIG. 2. Pattern responses recorded on three different occasions in a patient with a right anterior clinoid meningioma. Note the alteration in waveform of the major positive component from the right eye in the first record. Visual acuity at this time was 6/9 in the right eye and there was some temporal pallor of the right optic disc. Six months later, when the second record was taken, acuity in the right eye was reduced to the perception of hand movements and the pattern response is virtually abolished; the response from the left eye shows some reduction in amplitude and loss of the initial negative component when compared with the previous recording. The post-operative recording shows a full recovery of the response from the left eye, but no return of the response from the right eye, in spite of an improvement of the visual acuity in this eye to 6/60. Time marks 10, 50 and 100 ms.
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The PEP was absent from the eye with the more reduced acuity in 6 cases, including 4 of the 5 intracranial meningiomas and 2 cases of chiasmal compression, one by a craniopharyngioma (patient 10) and one by a pituitary tumour (patient 18). In all these patients the field loss involved central vision. In patient 9, two pre-operative records were obtained at an interval of six months. In thefirstthe response on the affected side was still present but of altered waveform and reduced amplitude. Six months later it was abolished on this side (fig. 2). The values given in Table 2 are those for the second record.
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Abnormal Waveform In addition to amplitude and latency changes, the waveform of the response recorded from the mid-occipital channel was altered in many cases. As has already been mentioned, in 4 cases the distortion was so great that no meaningful measurements of latency or amplitude could be made (patients 11, 12, 13 and 14). An example of one such record is shown in fig. 3, where the major positive component appears to be completely replaced by a broad negative wave in the response from the right eye. An example of a less florid change in waveform, which made the identification of the major positive component problematical, is shown in fig. 1. Cross-correlation between the responses from the two eyes reinforced the suggestion arrived at on visual inspection, that the clear bifid positivity seen in the response from the left eye is delayed and that there is a relative loss of the earlier positivity (corresponding to the major component) in the affected right eye. In patient 9 an alteration in the shape of the major positive component, which became broadened and rounded with an ill-defined peak, was
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Reduced Amplitude of Response In addition to the 6 patients who had an absent response from one eye, a further 9 had a relatively decreased amplitude when compared with the other eye. In 4 of these the waveform was so altered that the major positivity was unrecognizable on one side, and comparable measurements could not be made; the reduction was seen as an over-all diminution in the peak-to-peak amplitude of the response on one side as compared with the other. Only where the positivity was present and measurable could its relationship to the limits of normal be defined. There is considerable variation in the amplitude of the major positive component of the response in different healthy individuals and unless the absolute amplitude is less than 20 /xV it cannot be regarded as unequivocally abnormal. However, the size of the responses from the two eyes in any given subject is usually very similar. Under the standardized conditions of the test used here the amplitude ratio of the major positive component from the two eyes in 30 healthy individuals had a mean of 1 03 and a standard deviation of 0-15. Comparison of the responses from the two eyes in a given patient may thus allow identification of a unilateral reduction in amplitude which exceeds that of the normal population at either the 5 per cent or the 1 per cent level. Such a difference was observed in patients 2, 3, 4, 6 and 15. In patients 3 and 4 a reduction in amplitude was the only abnormality in the PEP. No probability level can, of course, be assigned to the marked amplitude difference observed in the 4 other cases in whom no major positivity could be identified (patients 11,12,13 and 14). It is notable that the pattern response was either absent or reduced on one side in all except one of the cases with orbital tumours, meningiomas or craniopharyngiomas. Even the one exception (patient 1) had a smaller amplitude in the affected eye, although this did not quite exceed the limits of normal variability at the 5 per cent level of probability.
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I.G. Age: 58 28.2.74 Left Eye
5MV
FIG. 3. Pattern responses from each eye of a patient with a pituitary adenoma. VAL 6/6, VAR 6/36. Note the grossly altered waveform of the response from the right eye with loss of the major positive component and a reduction in the over-all amplitude. The response from the left eye, which has a reasonably well-preserved waveform, is pathologically delayed.
the earliest change recorded in association with a right anterior clinoid meningioma (fig. 2, left-hand record), and was seen at a time when the visual acuity was only slightly reduced to 6/9 in the right eye. Six months later, when vision had deteriorated to the perception of hand movements, the response from this eye was virtually abolished (fig. 2, middle record). After surgical removal of the tumour, the vision in this eye improved slightly to 6/60, but the response remained absent (fig. 2, right-hand record). Abnormal Distribution of Responses In addition to alterations of the waveform recorded from the mid-line channel, the lateral distribution of the response evoked from one or other eye was often asymmetrical. Examples are illustrated in figs. 4 and 5 (pre-operative records). The PEP from patient 17, for instance, showed a marked asymmetry pre-operatively, the major positive component being clearly present at the electrodes 5 and 10 cm to the left of the mid-line, whereas there was a relative flattening of the response from the right side of the head (fig. 4, left hand records). This pattern was associated with an acuity of 6/5 in each eye, but there was an incongruent right homonymous hemianopia. The left-sided positivity here presumably corresponds to pattern stimulation of the preserved left half of the visual field. An ipsilateral positivity is characteristic of stimulation of those areas of the halffieldadjoining the horizontal meridian (Halliday, 19726; Halliday, Barrett, Halliday and Michael, 1976).
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Right Eye
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366
Post-operative
Pre-operative Left Eye
i.........i.
i
.......i
.
Right Eye
i.........i
Common reference
MA Age: 50
10 uV
FIG. 4. Pre-operative and post-operative pattern responses recorded from each eye of a patient with a pituitary tumour. The pre-operative records show a clear uncrossed asymmetry in the occipital distribution of the response, which has a left-sided predominance whichever eye is stimulated. The patient had an incongnient right homonymous hemianopia. Note the loss of asymmetry following the operation; however, the amplitude of the response from the left eye is significantly reduced, and the acuity in this eye was reduced from 6/5 to 6/9. In the pre-operative record there is a suggestion of a phase reversal of the positivity in the channel furthest out on the right side.
Hence, both visual field defect and evoked response suggest a lesion of the left optic tract. At subsequent operation the left optic nerve was reported to be pushed right forward by a tumour mass between it and the carotid. The chiasm was prefixed. Patient 10 had an absent response from the left eye, where vision was reduced to the perception of hand movements (fig. 5, left hand record). In the right eye, which had an acuity better than 6/12, there was a temporal cut sparing the mid-line. The mid-line and contralateral occipital response was small but of normal latency, while the channels ipsilateral to the stimulated eye showed a small but well-formed negative component occurring a few milliseconds later than the mid-line positivity and followed by a positive wave. This may represent either an asynchronous phase reversal of the mid-line response on this side or a rather more delayed positivity. Delayed positivities in the channels ipsilateral to the stimulated eye were seen clearly in 5 cases (patients 5, 10, 15, 16 and 19) and doubtfully in a further 2 (patients 6 and 18). In 2 of the patients this took the form of a crossed asymmetry,
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.
Left Eye
Right Eye
VISUAL-EVOKED POTENTIALS IN COMPRESSION Post-operative
Pre-operative Left Eye
367
Right Eye
Left Eye
Right Eye
J.D. Age: 29
|
5 M
V
FIG. 5. Pre-operative and post-operative pattern responses in a patient with a craniopharyngioma. There is no response pre-operatively from the left eye, in which the visual acuity was reduced to the perception of hand movements. In the right eye the response is small and asymmetric, the reduced major positivexomponent appearing at normal latency in the mid-line and left-sided channels, while the channels to the right of the mid-line show a slightly later negative component followed by a positivity. Acuity in the right eye was better than 6/12 and there was a temporal field defect sparing the mid-line. Post-operatively both responses are markedly improved, paralleling the return of normal acuity.
the delayed ipsilateral positivity being seen for stimulation of either eye, but on opposite sides. The patient who showed this more clearly (patient 19) had a bitemporal hemianopia; the other patient (patient 16) had a temporal hemianopia in the right eye, while in the left eye islands of vision were preserved in the upper nasal and lower temporal quadrants. Such crossed asymmetries were in contrast to the uncrossed asymmetries seen in patient 17 (fig. 4) and in one other case (patient 12). In these the pattern of asymmetry was similar for stimulation of each eye. In patient 17 the left optic tract was compressed, producing an incongruent right homonymous hemianopia. Patient 12 had incongruent partial right field defects, viz. a nasal hemianopia in the left eye and an upper temporal cut in the right eye. Two further cases had doubtful asymmetries (patients 11 and 18), the first associated with a left homonymous hemianopia, the second with a bitemporal hemianopia. Two patients gave asymmetric responses from one eye in the absence of any associated field defect (patients 5 and 14).
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Common reference
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A. M. HALLIDAY AND OTHERS
Increased Latency of Response In 4 patients (patients 2, 5, 6 and 13) there was a clear-cut delay in the mid-line response, which had a recognizable major positive component. In 2 other cases (1 and 18) the latencies were at the upper end of normal for the patient's age. Moreover, one further patient who had latencies within the normal range showed a 9 ms difference between the latency of the response from the two eyes (patient 1). In patient 6 (sphenoidal wing meningioma) a delayed response of reduced amplitude was associated with some distortion of the waveform (fig. 1). Because of the difficulty of recognizing the major positive component in this record, latency measurements were also carried out using a cross-correlation technique. This .confirmed the cursor measurements given in Table 2. In at least one other instance there was difficulty in distinguishing between a change in the waveform and a true delay. The details given in Table 2 for patient 9, who had an anterior clinoid meningioma, are those for the immediate pre-operative record, and, as already mentioned, a previous record had been taken six months before (fig. 2). At the time of thefirstrecording the response from the right eye was still present and had a clearly recognizable major positivity of altered waveform, measuring 61 ^.V. Formal measurements of the peak suggested that this was slightly delayed (122 ms), but inspection will show that the distinction between a true delay and a broadening of the waveform is almost a semantic one, the onset of the major positivity being hardly any later than on stimulation of the unaffected eye. The acuity of the right eye at the time was 6/9 and there was already temporal pallor of the optic disc. The longest latency recorded in this series of patients was 137 ms (patient 13) and none of the patients was delayed more than 20 ms beyond the upper limit of the normal latency range for their age. This is in contrast to the earlier results
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Asymmetries occurred in the response from one eye where the response from the other eye was either absent (patients 5, 10 and 18) or normal (patients 15 and 6). It is clearly only when both eyes showed asymmetries that these could be characterized as either crossed (patients 16 and 19) or uncrossed (patients 12 and 17). Even when this was so, however, the waveform could be so abnormal and so different for the two eyes that this differentiation was impossible (patient 14). Overall, 9 patients showed a clear asymmetry (patients 5, 6, 10, 12, 14, 15, 16, 17 and 19) and there were some less definite asymmetrical features in another 2 (11 and 18). Five of the 9 cases with marked asymmetry had evidence at operation of involvement of the chiasm (10, 12, 15, 16 and 19) and in 2 others both optic nerves were involved (6'and 14). In patient 5, who had a sphenoidal wing meningioma, the operation note did not mention the state of the chiasm or the optic nerve from the eye with surviving vision. It is of interest that the potential from this eye (which was clinically otherwise normal) was markedly delayed, indicating that the nerve fibres from it had been damaged.
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in optic neuritis and multiple sclerosis, where the mean delays were of the order of 35 to 45 ms and the actual delays encountered in individual patients ranged up to 100 ms. Combination of Abnormalities In half the abnormal cases there were multiple abnormalities in the PEPs, and in the 9 abnormal cases with only a single defect, these defects were gross in 7 (either absent response or marked asymmetry).
DISCUSSION
The results on this series of 19 patients with compressive lesions of the anterior visual pathways demonstrate clearly that compression can produce a variety of abnormalities in the pattern-evoked response, and that pathologically altered responses are common. In only one of the present series of cases was the pattern response within normal limits. If the present series is representative, over 90 per cent of patients with compressive lesions can be expected to give abnormal responses. It therefore appears that in this context too, as in primary demyelinating disease, the pattern response may prove to be very much more sensitive than the traditionally usedflashresponse (see Halliday (1975) for a review of the literature). In early cases the pattern response may be significantly altered, even where other clinical signs of visual impairment (visual acuity, fields and fundi) are unaffected.
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Effect of Operation on the PEP Table 3 shows a comparison of the pre- and post-operative records in 9 patients. In 3 there was a marked improvement in the responses, with a loss of a pre-operative asymmetry, accompanied by a return of normal acuity (patients 10, 14 and 16). The dramatic change in the PEPs in Case 10 is shown in fig. 5. The previously absent response from the left eye has returned following the operation, paralleling the improvement of visual acuity in this eye from the perception of hand movements to 6/5. The amplitude of the response in the right eye has also greatly increased with the improved acuity level (6/12 to 6/5), and the previous asymmetry has largely disappeared, although there is still a trace of it. Patient 17 also demonstrated a similar loss of asymmetry post-operatively in the response from both eyes, but the amplitude of the response from the left eye had significantly diminished, paralleling a loss of acuity from 6/5 to 6/9 (fig. 4). Three of the patients were unchanged by the operation (patients 8, 9 and 18) in spite of some change in the acuity level (fig. 2). The 2 other patients were definitely worse (patients 13 and 19) with either loss of the response from one eye, or an increase in the latency and the development of a marked asymmetry. It is clear that with regard to the prognosis for vision, the patients with craniopharyngiomas or pituitary tumours did rather better than those with intracranial meningiomas.
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TABLE 3. CHANGES IN VISUAL ACUITY AND PATTERN EVOKED RESPONSES BETWEEN PRE-OPERATIVE AND POST-OPERATIVE RECORDINGS Vision L
Amplitude R
L
Latency R
L
R
Supraseltar meningloma 8 B. M. 9J.N.
6/9-+6/9 6/6-1-6/5
Craniopharyngioma 10 J. D.
6/60->-NPL HM-K6/60
8-8-+9-8 5-9 ->• 8-4
0 -+ 0 0 -+ 0
104-1-105 UO-n-107
6/12H—• 6/5
0->-3-9
3-3 —• 6 1
6-2 -+ 6-3
GAW ->• 0
• 103
97 —• 129
121 - * 118
17 M. A.
6/5 --4-7
4-6 ->• 5 5 4-3 —6/5
Change m PEP
GAW-)-—
G A W -t- 108
Both responses improved. Pre-operative asymmetry in R. eye response gone
£j
Worse. Grossly abnormal pre-operative response from R. eye abolished post-operatively. L eye response shows slight latency increase and development of marked asymmetry Both responses improved with return to normal waveform and loss of asymmetry Responses improved with loss or asymmetry from each eye. Slight increase in latency in L. eye response Decreased amplitude in L. eye response postoperatively. Loss of asymmelry in the response from each eye ISQ Marked latency increase in both responses posloperativcly
CF = able to count fingers HM = ablc to perceive hand movements
2 X ^ f~
NPL"»no perception of light.
> **• }> 2 O Q H X 2 ^
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The character of the changes encountered in the evoked responses was, however, very different from that seen in the earlier studies on primary demyelinating disease (Halliday, McDonald and Mushin, 1972, 1973a, 1973d). The incidence of delayed responses was surprisingly small (only 4 out of the 19 patients), although the over-all incidence of delay may be masked by the relatively large number of cases in which the response was abolished altogether (as was the case in 6 patients). The serial recordings made on patient 9 and illustrated in fig. 2 suggest that a delayed response may be encountered in the early stages of compression, but may disappear when the amplitude is reduced by the further progress of the lesion. Quite apart from their over-all incidence, the delays encountered differed from those seen in the majority of the patients with demyelinating disease in that they were relatively much smaller. The maximum latency encountered for the major positive component (137 ms in patient 13) only approaches the mean delay of the earlier group. With such a small incidence of delays, however, it is probably unwise to draw any firm conclusions from these results. Only one of the 4 patients with delays was recorded post-operatively; in this patient (13) the acuity in the left eye remained normal and the latency showed a slight increase from 137 ms to 144 ms. The response also developed a marked asymmetry. All that can be said is that the surgical decompression was not associated with a return to normal latency in this case. In addition to the different pattern of delays encountered in this group, there was also a much higher incidence of alterations in the waveform of the response than was encountered in the group with primary demyelinating disease. Minor changes in the waveform of the delayed positivity were certainly encountered in the latter, a broadening and loss of definition being particularly characteristic, but the gross changes in waveform seen in some of the present series of patients, which rendered the major positive component unrecognizable, are not typical of optic neuritis. Nor are the less extreme distortions of the normal waveform, exemplified in fig. 1, at all typical of primary demyelinating disease in our experience. No single change in the pattern response appears, however, to be pathognomonic of compression or of primary demyelination. Delayed latency, altered waveform and reduced amplitude may be met equally in both conditions. It is possible that the prolonged latency may eventually prove to be specifically associated with demyelination of the fibres of the afferent visual pathway, but demyelination can be encountered in association with a number of different pathologies and is not confined to multiple sclerosis or optic neuritis. The higher incidence of binocular abnormalities in the tumours arising in the region of the sella turcica no doubt reflects the increased involvement of chiasmal and post-chiasmal fibres. The majority of the asymmetries were associated with field defects, but in at least two instances, clear asymmetries were seen in the absence of any clinical defect in the eye concerned. None the less, an association emerged between a pattern of crossed asymmetry, typical of cases with bitemporal hemianopia, in contrast to a pattern of uncrossed asymmetry, typical of the cases o
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Mechanism of PEP Abnormalities The independence of latency and amplitude changes, already noted in the earlier series (Halliday, McDonald and Mushin, 1973a, 1974a) is an even more striking feature of the present results. It suggests that more than one mechanism must be at work. It has already been suggested that the amplitude changes may reflect in large measure the conduction block in damaged fibres, whereas the delay may reflect the slowed conduction through demyelinated segments of the nerve fibres (Halliday, McDonald and Mushin, 1974a, 1976). Demyelination occurs in the spinal cord as a result of both acute and chronic compression (Holmes, 1906; Gledhill, Harrison and McDonald, 1973), and it seems likely that the same is true for the visual system. A detailed discussion of possible mechanisms for the abnormalities in visual evoked potentials is given by McDonald (1976).
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with homonymous hemianopia. Further consideration of the relationship between the half-field stimulated and asymmetries of the pattern response will be taken up in another paper (Barrett, Blumhardt, Halliday, Halliday and Kriss, 1976). Marked improvement in the pattern evoked response following operation was seen in 3 of the patients (10,14 and 16), all of whom lost a pre-operative asymmetry. An increase in the latency of the response was seen in 3 patients. In 2 (13 and 16) there was an increase of 6 to 7 ms in a previously delayed response; in the third (19) the responses from both eyes, which had been of normal latency pre-operatively, became markedly delayed. The present series was selected on the basis of operatively proven compression and for the most part represents relatively advanced cases. However, in patient 5 (sphenoidal wing meningioma) and 14 (pituitary adenoma) abnormal responses were recorded from the clinically normal eye. This indicates that, as in multiple sclerosis, damage to optic nerve fibres may be detected by the pattern evoked response test before any of the standard clinical tests are abnormal. The pattern of abnormalities encountered in this series of patients showed certain broad correlations with the pathology. Characteristic of intra-orbital tumours was a reduction in amplitude of the response from the affected eye; only one of the 4 cases was delayed. In intracranial meningiomas there was again a preponderance of uniocular abnormalities in the PEP and a particularly high incidence of absent responses in the affected eye (4 out of 5). Both the patients with sphenoidal wing meningiomas also had a pathologically delayed response. In the craniopharyngiomas and pituitary tumours, both arising in the region of the sella turcica, the pattern response was abnormal in both eyes in the vast majority of patients (9 out of 10). All the cases with gross change in the normal waveform were encountered in this group (4 out of 10) and asymmetries in the occipital distribution of the response were typical (9 out of 10).
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SUMMARY
ACKNOWLEDGEMENTS Our thanks are due to the Physicians and Surgeons of the National Hospitals and Moorfields Eye Hospital for allowing us to study their patients. We should also like to thank J. R. Pitman for invaluable technical assistance. REFERENCES ARDEN, G. B. (1973) The visual evoked response in ophthalmology. Proceedings of the Royal Society of Medicine, 66, 1037-1043. ASSELMAN, P., CHADWICK, T. W., and MARSDEN, C. D. (1975) Visual evoked responses in the diagnosis and management of patients suspected of multiple sclerosis. Brain, 98, 261-282. BARRETT, G., BLUMHARDT, L., HALLIDAY, A. M., HALLIDAY, ELBE, and KRISS, A. (1976) A paradox
in the lateralisation of the visual evoked response. Nature, London, 261, 253-260. BEHRMAN, JOAN, HALLIDAY, A. M., and MCDONALD, W. I. (1972) Visual evoked responses to flash
and pattern in patients with retrobulbar neuritis. Electroencephalography and Clinical Neurophysiology, 33, 445. FETNSOD, M., ABRAMSKY, O., and AUERBACH, E. (1973) Electrophysiological examinations of the visual
system in multiple sclerosis. Journal of Neurological Sciences, 20, 161-175. and HOYT, W. F. (1975) Subclinical optic neuropathy in multiple sclerosis. Journal of Neurobgy, Neurosurgery and Psychiatry, 38, 1109-1114. GLEDHILL, R. F., HARRISON, B. M., and MCDONALD, W. I. (1973) Demyelination and remyelination
after acute spinal cord compression. Experimental Neurology, 38, 472-487. HALUDAY, A. M. (1972a) Evoked responses in organic and functional sensory loss. In: Activitis evoquies et leur conditionement chez Thomme normal et en pathologie mentale. Edited by A. Fessard and G. Lelord. Paris: Editions INSERM, pp. 189-212. (1972A) Spatial contrast evoked potentials; component analysis and topology. Trace, 6, 39-46. (1972c) Spatial contrast evoked potentials: clinical applications. Trace, 6, 94-99. (1975) The effect of lesions of the visual pathway and cerebrum on the visual evoked response. In: Evoked Potentials. Handbook of Electroencephalography and Clinical Neurophysiology. Edited by W. S. van Leeuwen, F. H. Lopes da Silva and A. Kamp. Vol. 8A. Amsterdam: Elsevier, pp. 119-129.
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Pattern evoked responses have been recorded in 19 patients with compression of the optic nerve, chiasm or tract, verified at operation. These included 4 patients with orbital tumours, 5 with intracranial meningiomas, 2 with craniopharyngiomas and 8 with pituitary tumours. The evoked response was abnormal in all except one of these patients. Trie pattern of abnormalities in the response, however, differed from that in the earlier series of patients with primary demyelinating disease. The incidence of delayed responses was much lower, and the magnitude of the delays was smaller. Absent responses were particularly characteristic of patients with intracranial meningiomas. Tumours arising in the region of the sella turcica were associated with a high incidence of abnormalities of the waveform of the response, and asymmetry of the field of the occipital evoked potential was especially characteristic of this group. Most, but not all, asymmetric cases were associated with field defects.
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HALUDAY, A. M. (1976) Visually evoked cortical potentials in neurological diagnosis. In: Scientific Aids in Hospital Diagnosis. Edited by J. P. Nicholson. New York and London: Plenum Press. In press. BARRETT, G., HALLIDAY, ELISE, and MICHAEL, W. F. (1976) The topography of the pattern
evoked potential. In: New Developments in Visual Evoked Potentials in the Human Brain. Edited by J. F. Desmedt. London: Oxford University Press. In press. HALLIDAY, ELISE, KRISS, A., MCDONALD, W. I., and MUSHIN, JOAN. (1976a) Changes in
(Received November 26,1975)
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the pattern evoked response in compressive lesions of the anterior visual pathways. Electroencephalography and clinical Neurophysiology, 40, 541. (19766) Abnormalities of the pattern evoked potential in compression of the anterior visual pathways. Australian Journal of Ophthalmology. In press. MCDONALD, W. I., and MUSHIN, JOAN (1972) Delayed visual evoked response in optic neuritis. Lancet, 1, 982-985. (1973a) Delayed pattern-evoked responses in optic neuritis in relation to visual acuity. Transactions of the Ophthalmological Society of the UK, 93, 315-324. (1973/?) The use of pattern-evoked responses in the diagnosis of demyelinating disease. Proc. 8th Intemat. Cong. Electroenceph. clin. Neurophysiol. Marseilles. Electroencephalography and Clinical Neurophysiology, 34, 710. (1973c) The incidence of delayed pattern-evoked responses in multiple sclerosis. Proceedings of the 10th International Congress of Neurology. Barcelona: Excerpta Medica. ICS296, 150. (1973a") Visual evoked response in diagnosis of multiple sclerosis. British Medical Journal, 4, 661-664. (1974a) The dissociation of amplitude and latency changes in the pattern-evoked response following optic neuritis. Electroencephalography and Clinical Neurophysiology, 36, 218. " (1974ft) The value of the pattern-evoked response in the diagnosis of multiple sclerosis. Electroencephalography and Clinical Neurophysiology, 36, 551-553. (1974c) Delayed visual evoked responses in progressive spastic paraplegia. Electroencephalography and Clinical Neurophysiology, 37, 328. (\974d) Delayed pattern evoked responses in progressive spastic paraplegia. Neurology (Minneapolis), 24, 360-361. (1976) Visual evoked potentials in patients with demyelinating disease. In: New Developments in Visual Evoked Potentials in the Human Brain. Edited by J. F. Desmedt. London: Oxford University Press. In press. HOLMES, G. (1906) On the relation between loss of function and structural change in focal lesions of the central nervous system, with special reference to secondary degeneration. Brain, 29, 514-523. MCDONALD, W. I. (1976) Pathophysiology of conduction in central nerve fibres. In: New Developments in Visual Evoked Potentials in the Human Brain. Edited by J. F. Desmedt. London: Oxford University Press. In press. MILNER, B. A., REGAN, D., and HERON, J. R. (1974) Differential diagnosis of multiple sclerosis by visual evoked potential recording. Brain, 97, 755-772. NAMEROW, N. S., and ENNS, N. (1972) Visual evoked responses in patients with multiple sclerosis. Journal of Neurology, Neurosurgery and Psychiatry, 35, 829-833. RICHEY, E. T., Kooi, K. A., and TOURTELLOTTE, W. W. (1971) Visually evoked responses in multiple sclerosis. Journal of Neurology, Neurosurgery and Psychiatry, 34, 275-280.
