Journal of Neuro-Ophthalmology, December 1992, Volume 12, Issue 4

The unidirectionality of cerebral polyopia.

Polyopia, visual perseveration in space, has been associated with seizure activity, afterimage formation, and the presence of visual field defects. It can be interpreted both as a positive and a negative visual phenomenon. A patient with polyopia associated with the acute onset of hemianopsia is presented. The phenomenon has been investigated objectively with a simple procedure. The polyopia was highly correlated to movement of the eyes into the hemianoptic visual field and to increased contrast but not duration of the stimulus. This type of polyopia could be the result of incomplete visual processing due to poor visuospatial localization in a hemianopic field.

Joumal of Clinical Neuro- ophthalll",/ ogy 12( 4): 257- 262. 1992. The Unidirectionality of Cerebral Polyopia D. Gottlieb, M. D. © 1992 Raven Press, Ltd .. New York Polyopia, visual perseveration in space, has been asso­ciated with seizure activity, afterimage formation, and the presence of visual field defects. It can be interpreted both as a positive and a negative visual phenomenon. A patient with polyopia associated with the acute onset of hemianopsia is presented. The phenomenon has been investigated objectively with a simple procedure. The polyopia was highly correlated to movement of the eyes into the hemianoptic visual field and to increased con­trast but not duration of the stimulus. This type of poly­opia could be the result of incomplete visual processing due to poor visuospatial localization in a hemianopic field. From the Neurology Service, Massachusetts General Hospital and Spaulding Rehabilitation Hospital. Boston, and Depart­ment of Neurology, Harvard Medical School. Cambridge, Mas­sachusetts, U. S. A. Address correspondence and reprint requests to Dr. D. Gottlieb, P. O. Box 9438, Jerusalem 91093, Israel. 257 Perseveration is a common manifestation of neu­rological impairment. It is usually defect- specific, so that, for example, patients with aphasia will show language perseveration, and patients with apraxia will show motor perseveration. The mech­anism of these perseverations is unknown. How­ever, its defect specificity suggests that it is prob­ably related to dysfunction in processing informa­tion along specific input channels and not in some supramodal integrative center. Despite the general recognition of perseverations and the common oc­currence of visuoperceptive deficits after posterior cerebral lesions, visual perseveration is rarely re­ported with such lesions. A patient with visuospa­tial perseveration, or polyopia, caused by a right parietal infarct, is the subject of this report. The method by which the polyopia was examined is a simple bedside procedure that allows a quantita­tive and qualitative investigation of the phenome­non. CASE PRESENTATION A 74- year- old woman underwent coronary ar­tery bypass graft. There was no previous history of neurological or visual complaints. Postoperatively she became lethargic and developed a right central facial palsy and left visual field defect. Brain com­puted tomography revealed multiple bilateral le­sions, the largest in the right parietal region, sug­gesting an embolic etiology, and anticoagulants were administered. Over the following days she regained a normal state of consciousness and she could walk with assistance, but some confusion and difficulty with vision remained. Three weeks after the operation she was transferred to a reha­bilitation department. On admission she was alert and interactive but had a memory deficit. Her general level of atten­tion, verbal language functions, and abstract rea­soning were intact. A dense left visual field defect was found on confrontation. There was mild 258 D. GOTTLIEB weakness of the right arm and leg. Despite func­tional visual acuity ( 00 16/ 40, 16/ 100, OS 16/ 50, 16/ 100, with pinhole and with correction, respec­tively) and no abnormalities in formal ophthalmo­logic examination, she had trouble with her vision. Goldmann perimetry showed a macular- sparing left homonymous hemianopsia ( Fig. 1). She was slow to identify visually some objects that she readily identified by touch, and she read correctly but slowly. She also had a mild tendency to isolate the components of a thematic picture. Color vision was intact. Smooth eye pursuit and saccades, as well as eye- hand coordination were normal. Dur-ing the following week the mild object agnosia dis­appeared and she could identify 30 pictures of dif­ferent generic and unique objects, faces, and mon­uments, but she was unable to match any face on the facial recognition test ( 1). A striking aspect of her visual perception that was not evident initially was now observed in her daily behavior. She would try to grasp objects previously seen by her right visual field as if they were present on the left. She admitted having been disturbed by these illu­sory visions, since her vision had improved. Given the task of counting the number of objects in front of her she would see the same object appearing .. .. '( I , • .- 1 .... a, , ". ._.~~ __ Dfl _ Z ~. t:.~"" ' I • '" e:..... 1' 111111 •• ' h •• "" ( A) FIG. 1. ( A, B) Goldmann perim­etry showing a macular sparing homonymous hemianopsia. I. ) I Oill Neuro- ophthalmol. Vol. 12. No. 4. 1992 CEREBRAL POLYOPIA 259 many times toward her left. This visuospatial per­severation of the image occurred as often with monocular as with binocular vision and while shifting fixation from one eye to the other. The polyopia was induced by horizontal scanning of an array of visual targets but not by vertical scanning. It was easier to induce it by shifting the gaze to­ward the left visual field than toward the right. The original background ( e. g., white paper, brown desk) would carry over with the main visual illu­sion. The illusory images did not change in shape or color from the original but became blurred and smaller in size. The whole phenomenon would last 5 to 10 seconds and extend to the extreme of left hemispace. Thus, observing a picture with some people on the background of a landscape, she would see a " multitude" of identical people in a similar background extending all the way toward the left. She did not present evidence for visual perseveration in time, in particular the type that includes a stimulus- free interval. The only sugges­tion of temporal visual perseveration occurred when she observed tachistoscopic stimuli and saw multiple previous stimuli in proceeding screens. When observing a flashlight in a dark room, she did not show a reduced threshold for afterimage formation, in comparison to the examiner. Electroencephalograms ( EEG) and visual evoked potentials, done during the fifth postoperative week, were normal. On formal neuropsychological evaluation she obtained the following WAIS- R re­sults: her estimated premorbid IQ was 100 +; the actual verbal IQ was 88; the performance IQ was 68. General memory was estimated 79, with simi­lar scores for verbal and visual memory ( 86 and 81, respectively) and a lower score on delayed recall ( 75). On general attention and concentration she received a score of 80. During the 4th and 5th weeks after her stroke the patient underwent a se­ries of tests to further investigate the polyopia. EXPERIMENTS Experiment 1 Purpose The purpose of the first experiment was to in­vestigate the effect of the direction of eye scanning on the production of the polyopic images. Method The patient was asked to count 100 different ar­rays of visual stimuli. She was not limited in time. The arrays contained different types of stimuli. For example: 8 one- inch, black, capital letters; 10 black dots; 5 wool pieces of different colors; a picture showing 9 children, standing side by side. She was asked to scan and count each array twice. Once from left to right and once from right to left. Each time she counted the total number of components in an array a note was taken on how many addi­tions she had added to the actual number of com­ponents. These were considered polyopic images. The number of additions divided by the total num­ber of array components times 100 was the percent of polyopia that the patient showed while scan­ning the array in that specific direction. This dou­ble test was repeated 100 times with different types of arrays, in a random mode so that the same array did not appear in the opposite direction immedi­ately after the first time it was presented. For each array two scores were obtained: ( a) percent of polyopia when scanning and counting to the left and ( b) percent of polyopia when scanning and counting to the right. The mean percent of polyo­pia was calculated for each direction, and the dif­ference between the means was assessed for sig­nificance using Student's t- test. Results The mean percent of polyopia, counting an array from right to left, was 26.6 ( SD 26.72; SEM 2.80). The mean percent of polyopia when counting from left to right was only 1.24 ( SO 4.35; SEM 0.46). The difference was highly significant at the P = 0.000 level. Experiments 2 to 9 Purpose The purpose of experiments 2 to 9 was to inves­tigate the effect of different modes of exposure and stimulus characteristics on the production of poly­opic images. Methods The same procedures of counting the number of stimuli, random order of scanning direction and test category, and scoring system, as described for experiment 1, were used. Only the scores in scan­ning toward the hemianoptic visual field ( left) were analyzed. Experiment 2. The purpose of the 2nd test was to establish the presence of polyopia in monocular vision, since the rest of the tests were done in bin- I elin Neuro- ophthalmol, Vol. 12, No. 4, 1992 260 D. GOTTLIEB ocular vision. The subject scanned identical arrays monocularly versus binocularly. Experiment 3. The purpose of the 3rd test was to investigate the additional influence of head move­ment on the effect of eye movement. The subject scanned identical arrays presented to the left of body midline versus to the right of body midline versus in front of her. Experiment 4. The purpose of the 4th test was to investigate the effect of longer duration of expo­sure to all the stimuli ( simultaneous exposure) ver­sus shorter duration ( sequential exposure). The subject scanned identical arrays in two modes: Sequential exposure: All the stimuli except the first were covered and then each consecutive stimulus would be uncovered while she would go on count­ing. If she perseverated, the uncovering procedure would be repeated until she stopped counting. Simultaneous exposure: All the stimuli of the array would be shown while she counted them. Experiment 5. The purpose of the 5th test was to investigate the effect of stronger versus weaker contrast of the stimulus. The subject scanned iden­tical arrays, except the degree of contrast between stimulus and background was weaker. High­contrast stimuli were black on white, while low­contrast stimuli were yellow on white. Experiment 6. The purpose of the 6th test was to investigate the effect of stimulus size. The subject scanned identical arrays, but the size of the stim­ulus was varied. Larger stimuli ( letters, dots, geo­metrical forms) were 2 in. in height while smaller identical smaller stimuli were 0.5 in. in height. Experiment 7. The purpose of the 7th test was to investigate the effect of duration of eye movement. The subject scanned identical arrays, but the stim­ulus interval was varied. Wider stimulus spaces were 2 to 5 in., while narrower spaces were 0.5 to 1 in. Experiment 8. The purpose of the 8th test was to investigate the effect of number of stimuli inde­pendently from other factors. The subject scanned identical arrays with varying numbers of stimuli. While the stimulus interval remained constant, the arrays were either short ( less than 5 stimuli) or long ( more than 10 stimuli). Experiment 9. The purpose of the 9th test was to investigate the effect of form. The subject scanned I CI1" ,' Veu"" 0l'hthaI7llo/' Vol. 12, No, 4. 1992 identical arrays, but the pattern of the stimuli var­ied. The stimuli were either simple and uniform ( dots) or complex and multiform ( letters, numbers, geometrical forms). Experiment 10. The purpose of the 10th and final test was to investigate the influence of higher cog­nitive demands ( identifying versus only recogniz­ing) on the production of polyopia. The patient had to count the stimuli, as she was doing before, or to name them ( identify the letters, numbers, geometrical forms). Results The results of experiments 2 to 10 are presented in Table 1. In addition to the statistical analysis presented in the table, a multiple regression anal­ysis, including all the tests, was computed. Only three factors of significance were found: ( a) high contrast of stimuli ( correlated positively), ( b) sim­ple pattern of stimuli ( correlated positively), ( c) identifying the stimuli, instead of just counting them ( correlated negatively). The equation pre­dicted the percent of polyopia, with P = 0.02. DISCUSSION The main conclusion of these tests was that there was a strong correlation between the occur­rence of polyopia and eye movement toward the hemianopic visual field. From the different condi­tions tested, only three conditions influenced the occurrence of this unidirectional polyopia. Increas­ing the contrast of the stimulus increased the ten­dency to perseverate. Increasing the duration, size, stimulus interval, and number of stimuli did not influence the production of polyopia. Simpli­fying the task by using simply patterned stimuli to recognize and count or complicating it by requiring identification of the stimulus instead of just recog­nition, correlated, positively and negatively, re­spectively, to increased polyopia. Two types of visual perseveration have been de­scribed. Visual perseveration in time, or palinop­sia, and visual perseveration in space, or polyopia ( 2,3). Although the first descriptions of these phe­nomena were presented more than 100 years ago ( 4), not only their pathophysiology remains un­known ( 5,6), but also some of their clinical charac­teristics are not yet established. Their occurrence, usually after posterior cerebral lesions, is consid­ered a rarity by some investigators ( 3,6,7) and not infrequent by others ( 8). In one series of patients with posterior cerebral lesions, visual persevera- CEREBRAL POLYOPIA TABLE 1. Results and statistical analysis of experiments 2 to 10 Test Condition Mean SD SEM 2: Exposure, n = 8 Monocular 45.57 21.79 8.24 Binocular 32.57 26.89 10.16 3: Location, n = 8 Left 26.83 16.62 6.78 In front 27.83 25.87 10.56 Right 25.50 23.95 9.78 4: Exposure. n = 8 Simultaneous 54.40 28.59 12.79 Sequential 32.20 17.58 7.86 5: Stimulus contrast, n = 9 High 29.00 19.70 6.96 Low 10.50 9.64 3.41 6: Stimulus size, n = 8 Large 23.33 16.45 6.72 Small 19.17 17.20 7.02 7: Stimulus interval, n = 9 Large 28.89 20.28 6.76 Small 17.78 20.48 6.83 8: Stimuli number, n = 7 Large 76.67 80.42 3283 Small 26.67 26.58 10.85 9: Stimulus pattern, n = 9 Simple 29.50 29.61 10.47 Complex 31.63 21.00 7.43 10: Task, n = 8 Counting 37.80 26.28 11.75 Naming 2.60 5.81 2.60 n, number of double tests; NS. nonsignificant; S, significant. 261 Statistical difference P = 0.34 NS P = 0.98 NS P = 0.17 NS P = 0.02 S P = 0.67 NS P = 0.26 NS P = O. 17NS P = 0.87 NS P = 0.02 S tion was found in 5 of 11 cases ( 8). Judging from the incidence of perseveration in other aspects of neurological impairment, such as aphasia or apraxia, this rate does not seem exaggerated. It is also unclear whether patients with visual persever­ation in time will also show visual perseveration in space, and vice versa. Most authors believe this is the rule ( 6), but some claim the opposite ( 3,9). This is important, since, in some cases, a common mechanism has been suggested for both types of visual perseveration, assuming they are the same phenomenon. Even in the case of visual persever­ation in time, one must distinguish between the type that occurs immediately after exposure to a visual stimulus and the type that occurs after a delay ( 6,9,10). It may be that these two types of palinopsia have different mechanisms, and only the former may appear in association with polyo­pia, while the latter is more common as a solitary phenomenon. A similar distinction between im­mediate poststimulus perseveration and delayed perseveration, occurring after a stimulus- free in­terval, exists in other modalities of perseveration, and different mechanisms have been proposed for each ( 11). The pathophysiology of visual perseveration is unknown. Using Jackson's terminology, some in­vestigators have viewed visual perseveration as a positive sign of neurological impairment ( 6), while others have considered its association with nega­tive signs ( 3). The evidence for viewing visual per­severation as a positive phenomenon representing hyperactive brain activity is based on its frequent association with seizure activity ( 10) and on one study that investigated the characteristics of after-image in palinopsia ( 12). It should be noted that palinopsia has rarely been reported as an integral component of an epileptic episode- it does not re­spond to treatment with antiepileptics-- and in some case reports the patients were visually per­severating while under normal EEG recording ( 10,13). Still, some delayed episodes of palinopsia have a paroxysmal presentation and hyperactive brain activity is then likely. It has also been sug­gested that, in the presence of a normal EEG re­cording, this activity may be a type of hallucination caused by release from cortical inhibition ( 13,14). The afterimage theory also proposes that the role of cerebral damage in visual perseveration is re­leasing normal afterimage mechanisms from corti­cal inhibition, allowing their production at a lower threshold ( 12). The association between visual per­severation and afterimage phenomena is based on two cases in which all the physical characteristics of the former were found in the latter. However, other investigators failed to find these characteris­tics in their patients ( 5,6,13,15). Our patient also belongs to this larger group of patients in which some but not all the characteristics of an afterimage occurred during visual perseveration. Hence in­creased contrast was, but increased duration was not, correlated with the rate or frequency of per­severation. There was no reversal of colors, and increased size of stimulus on a more distant back­ground could not be tested. As in other reports ( 5,13), she did not show an increased tendency to produce afterimages when stimulated with a bright stimulus in a dark room. Alternatively, visual perseveration may be con­sidered a negative manifestation of cerebral dam- JClin Neuro- ophthalmol, Vol. 12, No. 4, 1992 262 D. GOTTLIEB age. This is supported by the presence of some degree of impaired visual perception in most cases of palinopsia or polyopia ( 3,5- 7,9,10,16). The strongest clinical correlation found in patients with visual perseveration is with a visual field defect ( 3,5,7- 10,14), and it has been claimed that the vi­sual field defect is always in a state of evolution or resolution for the perseveration to occur ( 5). The perseverated image appears in most cases in the defective visual field. The attempt to process a vi­sual stimulus through a partially impaired visual system is thus strongly associated with the pro­duction of visual perseveration. Still, this rule may be applicable only to the cases of immediate post­stimulus visual perseveration. In cases of delayed palinopsia, the visual stimulus that produced it is clearly not being processed and must be coming from memory storage. It seems then that the pathophysiology of visual perseveration, at least the immediate poststimulus type, cannot be de­scribed exclusively in terms of either a positive or a negative visual phenomenon, but rather is a com­bination of both. Another factor allegedly important in the induc­tion of poststimulus visual perseveration is mo­tion. Either moving the eyes along an array of stimuli ( our patient) ( 6,8) or moving a stimulus in front the eyes ( 5,6,8,10) may induce polyopia. The descriptions of previous such cases and the results of the directional tests done on our patient show that motion- induced polyopia is highly unidirec­tional. This characteristic may indicate that visual perseveration in space results from incomplete vi­sual processing due to poor visuospatial localiza­tion in the hemianopic visual field. The visual pro­cessing of an object in motion demands both its identification and its localization in space. Visuo­spatial localization depends on the congruency of afferent and efferent information. The efferent in­formation comes through collaterals of the efferent impulses to the oculomotor system ( 17,18). The af­ferent information is in part retinal and in part ex­traretinal. The role of the retinal information, also termed the " local retinal sign" ( 18), can be com­pared to the role of proprioceptive information in the somatosensory system. It may be assumed that i~ hemianopsi~ the retina is partially unable to pro­VIde an effectIve " local retinal sign." This is be­cause, through evolution, the human retina has evolved into a . bifunctional system ( 19). In this sys­tem the fovea IS more responsible of identification while the peripheral retina, half of which is in~ volved in hemianopsia, is more responsible for 10- / Clin Neuro- ophthalmol, Vol. 12. No. 4, 1992 calization of stimuli of interest, which are later fo­veated and identified. The movement of an eye into a hemianopic field, while scanning an array of stimuli, does not produce accurate retinal informa­tion about the position in space of the targets that are being consecutively foveated. 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