INVERTED VISION AFTER FRONTAL LOBE DISEASE

Mark Solms, Karen Kaplan-Solms, Michael Saling and Percy Miller

(Division of Neurosurgery and School of Psychology, University of the Witwat~rsrand, Johannesburg)

In this article we wish to draw attention to a rare and little-known neuro­psychological phenomenon.

We recently had a patient who reported episodes of upside-down vision. In the face of such an unlikely claim, we were reminded of Critchley's (1953) misgivings about the metamorphopsias in general:

"Unfortunately, we are dealing with a phenomenon which lies mainly if not wholly within the province of a subjective experience. The examiner is largely at the mercy of the patient's own description of events" (p. 299).

Nevertheless, a careful perusal of the literature reveals that there is good reason to take this patient's claim seriously.

LITERATURE REVIEW

Twenty-one such cases have previously been reported (Table I). These prior descriptions display some striking similarities: First, the patients all reported the phenomenon of inverted vision during an acute phase in the underlying condi­tion. Indeed, it was often the first sign of disease (Halpern, 1930; Klopp [case J. Bo.], 1951; Luers and Potzl, 1941; Penta [both cases], 1949; Potzl, 1943; Wilder [case 4], 1928). Second, they usually claimed to experience repeated episodes in quick succession, but the complaint was seldom chronic. It invariably disap­peared as general recovery progressed (Bishopp, 1805; Gerstmann, 1926; Horns­ten [both cases], 1974; Klopp [cases F.W. and H.B.], 1951; Penta [second case], 1949; Phleps, 1908; Seitz, unpublished case; Wilder [case 3], 1928). Third, the visual phenomenon itself was said to take a paroxysmal form; that is, the patients reported that their vision suddenly inverted, remained upside-down for a few minutes or seconds, and then rapidly reverted to normal (Bishopp, 1805; Gerst­mann, 1926; Halpern, 1930; Klopp [all three cases], 1951; Phleps, 1908; Potzl, 1943; Wilder [all'three cases], 1928). Fourth, many patients asserted that they were able to abort the inversion by briefly closing one or both eyes (Klopp [all three cases], 1951 ; Penta [second case], 1949). Fift~, the process of inversion itself

Note. In view of current international awareness of the political situation in South Africa, the authors wish to state that they do not support or condone the Apartheid policy.

Cortex, (1988) 24, 499-509

500 Mark Solms, Karen Kaplan-Solms, Michael Saling and Percy Miller

Source

Bishopp (1805)• Uncertain (1904)b Phleps ( 1908)

Pick (1908)

Gerstmann (1926) Wilder (1928)

Seitz (unpublished; cited in Pearson, 1928) Halpern (1930)

Liiers and Potzl (1941) POtzl (1943)

Penta (1949)

Klopp (1951)

HOrnsten (1974)

Bender et al. (1982)

TABLE I

Previously-Reported Cases of Inverted Vision

Case

Female, 22 yrs Male, 8 yrs MarkoV.: male, SO yrs Male, 19 yrs Female Male, 58 yrs Case 2: female, 48 yrs Case 3: female, 62 yrs Case 4: female, 30 yrs Male, 20 yrs

K.S.: female, 38 yrs

Female, 60 yrs

Anton Schmidt: male, 62 yrs Male, 30 yrs Male, 50 yrs

F.W.: male, 22 yrs

J. BO.: male, 39 yrs H.B.: female, 61 yrs Patient 6

Patient 9: male

Unspecified

Diagnosis

"Hysteria" Measles Open head injury

"Dementia praecox"

Localization

Unspecified Right parietal lobe

Unspecified Unspecified Cerebrovascular accident •Left parieto-occipital region Uncertain (multiple sclerosis?) Uncertain Uncertain (chronic nephritis) Uncertain Cerebral tumour Left parieto-occipital region Head injury Uncertain

Cysticercosis

Cerebrovascular accident

Cerebrovascular accident

Cerebral tumor Uncertain (allergy?)

Meningioma

Uncertain Uncertain Cerebrovascular accident

Cerebrovascular accident

Transient ischaemic attack.

Bilateral frontal, parietal and oc­cipital lobes, caudate, putamen, thalamus Uncertain (inferior pons?)

Bilateral ventrobasal cerebel­lum Left parietal lobe Uncertain (membranous laby­rinth?) Left parasagittal fronto-parietal region Uncertain Uncertain Lateral medulla (Wallenberg area) Lateral medulla (Wallenberg area) v ertebro-basilar arterial field

•This case has sometimes been attributed to Winslow (1868), who paraphrased Bishopp's original report (cf. Gerstmann, 1926; POtzl, 1943; Wilder, 1928). bAccording to Pearson (1928) this case was reported in the New York Medical Journal on December 18, 1904. We have been unable to trace the report as the reference appears to be incorrect.

was said to take the form of an actual torsion of the visual scene in the coronal plane around a central axis1 (Hornsten [both cases], 1974; Klopp [cases F.W. and H.B.], 1951; Penta [first case], 1949; Pick [first case], 1908). Sixth, in all cases in which the direction of this torsion was noted, it was described as clockwise (Klopp [all three cases], 1951; Penta [second case], 1949). Seventh, all patients reported that their vision rotated through exactly 180° -which is, of course, the defining characteristic of inverted vision. However three patients described associated episodes of 90°coronal rotations (Hornsten [patient 9], 1974; Klopp [case J. Bo.], 1951; Pick [second case], 1908), and associated rotations of 90° and

1 However, in one case (Klopp [case J. Bi\ ), 195 I) th~ visual scene was said to flip over in the sagittal plane and take the form of an upside-down mirror image (i.e. equivalent to the experimental inverted vision of Kohler, 195 I).

Inverted vision 501

180° in the horizontal plane (Gerstmann, 1926) and sagittal plane (Klopp [case J. Bo.], 1951; Penta [second case], 1949) have also been reported. 2 This suggests that illusory rotations of the visual scene tend to be orientated along one of the principal orthogona1s. Eighth, the rotations involved the entire visual array; that is the internal consistency of allocentric space was usually said to have been maintained. 3 Ninth, associated proprioceptive changes were frequently noted, and many patients felt as if their bodies were dangling in space (Halpern, 1930; Klopp [cases F.W. and J. Bo.], 1951; Luers and Potzl, 1941; Penta [both cases], 1949; Potzl, 1943). Tenth, the subjective experience of inverted vision was usually accompanied by nausea, vomiting, dizziness, or a general feeling of malaise4

(Halpern, 1930; Hornsten [both cases], 1974; Klopp [all three cases], 1951; Luers and Potzl, 1941; Penta [both cases], 1949; Potzl, 1943; Wilder [all three cases], 1928). Nystagmus is another commonly associated feature (Bender et al., 1982; Horns ten [both cases], 1974; Klopp [all three cases], 1951; Luers and Potzl, 1941; Penta [second case], 1949; Potzl, 1943; Wilder [all three cases],1928). Lastly, in all cases in which the site of the lesion was documented, it involved one of two anatomical structures; either the parieto-occipital region (Gerstmann, 1926; Halpern, 1930; Klopp [case F.W.], 1951; Penta [first case], 1949; Phleps, 1908; Wilder [case 4], 1928) or the vestibulocerebellar system [Bender et al., 1982; Horsten [both cases], 1974; Klopp [case J. Bo.], 1951; Luers and Potzl, 1941; Penta [second case], 1949; Potzl, 1943).5

The relatively uniform clinical picture that emerges from this body of liter­ature suggests that inverted vision is a valid neuropsychological entity, and lends substantial credibility to our own patient's assertion that he had seen the world upside-down. It is within this context that we investigated the case, and that we now present the following report.

CASE REPORT

History and Routine Investigations

W.B., a 12 year old, dextral, Tswana-speaking male from a small rural comunity, was admitted to our neurosurgical unit in June 1985. He complained of severe frontal headache and nausea, following an episode of frontal sinusitis. He had gross neck-stiffness, bilateral papilloedema, and pyrexia; but he was fully conscious and orientated, and displayed no motor deficits. There was nothing noteworthy in his previous medical history. A C.T. scan demonstrated a large left basal frontal abscess and a smaller right mediobasal frontal abscess (Figure 1 ). The left-sided abscess was drained on the day of admission and a

20nly one investigator (Halpern, 1930) described an instance of nonorthogonal associated rotation (60° - 70° in the sagittal plane).

'Some of the previous reports were ambiguous in this respect, but break-up of the visual scene was explicitly noted in only one instance (Klopp (case J. Bii.], 1951).

4Nausea and feelings of bodily inversion have also been reported with experimentally-inverted vision, induced by the wearing of prism lenses (Stratton, 1896, 1897). Stratton (1897, p. 350) also seems to have experienced an episode of associated disorientation through 180° in the horizontal plane.

'However it should be noted that most of these localizations were made on clinical grounds alone; almost all of these cases were reported before the advent of modem in vivo imaging techniques, and autopsy data were available in only two instances (Halpern, 1930; Piitz!, 1943).

502 Mark Solms, Karen Kaplan-Solms, Michael Saling and Percy Miller

Fig. 1 ---,-- Contrast -enhanced cranial C. T. scan of patient W.B., taken on date of initial admission, demonstrating bila­teral frontal lobe abscesses.

Fig. 2- Contrast-enhanced cranial C. T. scan of patient WB., taken 26 weeks after initial admlsswn, demon­strating patches of low density ('gliosis') in and around the sites of the previous bifrontal abscesses.

fronto-ethmoidectomy was then performed. Antibiotics and prophylactic anti-epileptics were administered. On the basis of ongoing C.T. findings, the abscess was re-aspirated twice during the next three weeks. The patient then made a full clinical recovery. A neurological examination seven weeks after admission elicited nothing out of the ordinary. Brief neuropsychological assessment at this stage also produced nothing unexpected. Only one feature of this assessment warrants mention, because it acquired special significance at a later stage: On the copy trial of the Complex Figure Test (Osterrieth, 1944; Rey, 1941, 1959) the patient rotated his drawing through 90°. After this assessment, he was dis­charged. The patient recuperated at home for three weeks, then returned to school and

Inverted vision 503

passed his end-of -year examinations. In January 1986 he returned to our out-patient clinic for follow-up investigations. A C.T. scan now demonstrated bilateral patches of low density ('gliosis') in the frontal lobes, in and around the sites of the previous lesions (Figure 2). Neuropsychological investigation at this stage elicited the following: There were no impressive signs of disinhibition, perseveration, or adynamia, and there was no obvious personality change. The patient was able to inhibit inappropriate responses on conflict­reaction tasks, and to organize motor activity in accordance with complex verbal instruc­tions. However there was evidence of slight impulsivity and he was mildly unreflective in his planning of complex activities. The attention-span and immediate memory were normal. Learning of new verbal material was protracted and disorganized, but not sug­gestive of a true recent memory disorder. Visual memory was roughly equivalent, and remote memory seemed normal. Narrative speech was fluent, verbal repetition was intact, there was no deficit in comprehension of spoken or written language, and no dysgraphia. Primary arithmetical operations were understood and performed with ease, but there was slight difficulty with complex problem-solving and consecutive calculations. These errors were sequential rather than spatial. Finger gnosis was intact. Right-left orientation in personal space was normal, but there was a systematic reversal with respect to the examiner's body. Topographical orientation was unimpaired. Visual and tactile gnosis were normal. Graphomotor and three-dimensional constructional behaviour were slightly careless but not at all dyspraxic. Orientation in concrete space was normal. There were no indications of hemispatial neglect under any conditions.

There is, in general, nothing remarkable about this neuropsychological picture. We only describe the profile to demonstrate that it corroborated the radiological evidence for an unequivocal frontal lesion. On the other hand, the patient's performan'?(! on one particular test was most unusual. The patient's drawing on the copy trial of the Complex Figure Test was not surprising under the circumstances (Figure 3), but on the immediate recall trial of this test he drew the entire figure upside-down (Figure 4). The patient did not seem to be aware that he had inverted the design, which he had drawn swiftly and with ease.

When we next saw W.B. (three weeks later), he recounted the following experience in response to a direct question about his vision: One morning, a few days after he had been discharged from hospital, he was sitting at home at the kitchen table going over some school-work he had missed while he was away. He got up to make himself a cup of tea, and, when he returned to the table, he suddenly gained the impression that everything he had written in his exercise book was upside-down. Alarmed by this, he turned his glance away from the book, only to discover that the kitchen stove was also upside-down. He then realized, to his dismay, that the entire kitchen was inverted; the floor was at the top and the ceiling at the bottom. He stood up and walked- a little unsteadily- towards the kitchen door, which now appeared to hang from the ceiling. (Only the external visual scene seemed to be inverted; the patient himself did not feel any changes in his body position). When he reached the door and looked outside, he saw that the whole world was upside-down, with the sky at the bottom and the landscape at the top. He sat down on the doorstep and stared disbelievingly at this scene for a few minutes. Sitting there, a wave of nausea overcame him. He closed his eyes and rubbed them with his hands. When he re-opened them his vision had re-orientated itself. This entire episode lasted for approximately four minutes. He did not report the experience to his parents when they returned home from work later that day. On the morning of the next day the phenomenon re-appeared. The patient was playing in the garden at the time. His attention was suddenly drawn to a tree which seemed to be moving. As he looked at the tree it rotated slowly, in a clockwise direction, until it was completely upside-down. The patient then briefly closed his eyes, and the inverted vision immediately disappeared. When asked to describe the ,illusion in more detail, he reported that the tree did not rotate in isolation; the entire external visual scene turned through 180° in the coronal plane. Again, he did not report the experience to his parents. During the ensuing months episodes like these recurred "a few more times"; but the patient refused further discussion on the matter. This was the first time that he had described the experience to anyone, and he clearly did not enjoy talking about it. When we next saw him,

504 Mark Solms, Karen Kaplan-Solms, Michael Saling and Percy Miller

Fig. 3- Complex Figure of Rey (1959), copy trial, drawn by patient W.B.

Fig. 4- Complex Figure of Rey (1959), immediate recall trial, drawn upside-down by patient W.B.

Inverted vision 505

20 weeks later, we again asked him about his inverted vision. He then insisted that the phenomenon had long since stopped.

Special Investigations

After hearing the above description, we obtained opthalmological and electroence­phalographic assessments (no abnormalities were detected), and we conducted a number of special neuropsychological investigations of W.B.'s visuospatial perception.

As part of these investigations, the Complex Figure Test was administered three more times. The reader will recall that during the copy trial of the first administration (seven weeks after the initial admission) the patient had rotated Rey's figure through 90°, and that he had inverted it on the immediate recall trial during the second administration (39 weeks after admission). Three weeks later, during the third administration, he rotated Taylor's ( 1959) version of the complex figure through 90° on the recall trial. Twenty weeks later (62 weeks after admission) he again rotated his copy of Rey's figure through 90°. During the last administration, two years after the initial admission, he rotated Taylor's figure through 90° on both the copy and immediate recall trials. Every time that he rotated the figure through 90° he placed it on its flat side, so that the triangular side faced upwards.

W.B.'s performance on the Visual Retention Test (Benton, 1974) displayed an equi­valent deficit. On administration A of the test he scored 0110 correct (14 errors), and on administration D he scored 5110 correct (6 errors); eight of his 20 errors were rotations of major figures. This tendency declared itself again during the administration of Butters and Barton's ( 1970) Stick Test. On the copy condition of this test he scored 7 I 10, and two of his three incorrect constructions took the form of upside-down mirror images of the models. His performance on the rotation condition of this test was very defective (31 10).

We designed a test which required the patient to sort 30 pairs of simple geometric figures according to whether they were "the same" or "different". The series included 10 identical figures, 10 equivalent but rotated figures, and 10 mirror images. The patient correctly sorted eight of the 10 identical pairs as "the same", and all 10 of the pairs which included one design which was a rotated equivalent of the other were correctly classified as "different"; but he incorrectly identified eight of the 10 figures which were mirror images of each other as "the same".

A re-assessment of W.B.'s reading confirmed our earlier finding that he could read fluently with comprehension. However, a more detailed investigation demonstrated an unusual form of literal alexia consistent with the above-described perceptual deficit. We randomized the lower case alphabet and presented its letters individually to the patient, asking him to name them. In this task, which was repeated across 10 trials, he misread the letter d as "p" (on 31 10 presentations); pas "d" (31 1 0) or "b" (21 1 0); b as "g" ( 41 10), "d" (1/10), or "q" (1/10); q as "b" (3/10); and mas "w" (1/10). When these letters were contextualized in words, however, he did not make any errors, and he made no errors when reading spatially-ambiguous words like mom, wow, bop, and pod. Equivalent errors also did not arise when the patient produced individual letters to dictation and when he was asked to copy letters that he had misread. We then constructed a further test which required the patient to sort letters according to whether they were "the right-way-up" or "upside-down". We randomly mixed the standard alphabet with an upside-down alphabet (excluding invertible letters like H and X) and presented the letters individually to the patient. Upper and lower cases were done separately. W.B. correctly identified 65% (22134) of the "right-way-up" letters and 18% (6134) of the "upside-down" letters; and incorrectly classified 35% (12134) of the right-way-up letters as "upside-down" and 82% (28134) of the inverted letters as "the right-way-up". However, the misclassified letters were not misread. In other words, although he thought that an inverted t and an inverted A were "the right-way-up", he nevertheless knew that they were a "t" and an "A". We then costructed a test which required the patient to sort pairs of upper and lower case letters (e.g. a, A; G, g; and h, Z) according to whether they represented "the same" or "different" sounds. We mixed a full alphabet of matched pairs with another of mismatched pairs and

506 Mark Solms, Karen Kaplan-Solms, Michael Saling and Percy Miller

presented the pairs individually to the patient. He made no errors on this test. We concluded that his apparent literal alexia was actually a perceptual abnormality, rather than a true reading disorder.

W.B.'s performance on the Judgement of Line Orientation Test (Benton, Hamsher, Varney and Spreen, 1983) was also abnormal. His score was in the severely defective range (10/30 correct), but displayed an atypical pattern of errors. He performed significantly better on items where the pair of stimulus-lines included one line that was in an orthogonal orientation (he correctly matched 9/16 such items as opposed to 1/14 of the items in which both stimulus-lines were oblique). His errors also included seven mirror-like transposi­tions across the vertical midline.

On the basis of these special investigations, we gained the general impression that W .B. had difficulty establishing the spatial orientation of an isolated configuration in the absence of a well-established contextual framework.

DISCUSSION

There are obvious parallels between our patient's description of inverted vision and the descriptions contained in previous case-reports.

Nevertheless, there is one striking difference between this case and those described in earlier reports. In all previous cases in which a suspected location for the symptomatic lesion was specified, it was said to involve either the parietal lobes (Gerstmann, 1926; Halpern, 1930; Klopp [easel], 1951; Penta [case 1], 1949; Phleps, 1908; Wilder [case 3], 1928), or the vestibulocerebellar system (Benderetal., 1982; Homsten[bothcases], 1974; Klopp[case2], 1951; Luers and Potzl, 1941; Penta [case 2], 1949; Potzl, 1943). Our patient's lesions were unam­biguously located in the frontal lobes, and there was no radiological or clinical evidence of involvement of the parietal lobes or the vestibulocerebellar system at any stage during his illnes. As unlikely and bizarre as the phenomenon of inverted vision might appear to be, it is at least theoretically plausible that it should be associated with occipito-parietal or vestibulocerebellar dysfunction; but for its presence in a case of frontal lobe disease, there seems to be little justification. Apart from the general role of the frontal lobes in the directing of visual attention, the only established knowledge concerning the functions of the frontal lobes that might specifically account for the presence of inverted vision in our case, is the observation of Teuber and Mishkin (1954) that frontally-lesioned patients are particularly defective on Aubert's (1861) test of visual-postural integration. However, although abnormal visual-proprioceptive interaction may go some way towards explaining the gross phenomena of inverted vision, it would probably not be able to account for the more subtle visuo-spatial abnormalities displayed by our patient. These abnormalities seem to have more in common with the phenomena of 'perceptual equivalence' and bther visual anisotropies of infancy and childhood (Bomstein, 1982).

Notwithstanding these theoretical problems, in consideration of the discre­pancy in the sites of the lesions in our patient and previous cases, we shall review some of the earlier data. First, in Halpern's (1930) case of cysticercosis, the inverted vision was attributed to the presence of bilateral multiple cysts in the parieto-occipital divisions of the cortex. However, cysticerci were also found in both frontal lobes, and the patient suffered from bilateral anosmia and episodes of nonfluent speech. Second, in Klopp's (1951) case of left parasagittal fronto­parietal meningioma, the inverted vision might just as well have been attributable

Inverted vision 507

to the frontal as to the parietal component of the lesion. Indeed, Klopp remarked that no parietal signs were elicited upon examination of this patient but noted that he was emotionally labile and socially inappropriate. Third, in Wilder's (1928) case of cerebral tumour, the lesion was localized to the left parieto­occipital region on clinical grounds; but intra-operative observation of this region produced no signs of the tumour. In our opinion, the clinical picture in this case suggests a deep left temporal lobe lesion with significant mass effect on the left frontal lobe and many other structures. This would be more consistent with Wilder's observations of "psychical changes" (p. 225), left-sided anosmia, epi­sodes of hyposomnia and amnesia, complex seizures with olfactory aura, right­sided partial epilepsy, right-superior homonymous quadrantanopia, left-anterior ageusia, horizontal nystagmus on deviation to the left, right abducens and facial paresis, bilateral papilloedema, and exopthalmus. There is, therefore, some evi­dence of frontal lobe involvement in at least three previous cases of inverted vision. However, our case seems to be the first instance with an unequivocal frontal lesion.

A second important feature of the present case is that the general neuro­psychological status of the patient was investigated in some detail. Only two previous patients with inverted vision have been described from a neuropsycho­logical point of view (Gerstmann, 1926; Halpern, 1930). Both of these patients displayed a degree of right-left disorientation, and some difficulty in the local­ization of visually-perceived objects. In both cases the right-left disorientation seems to have primarily concerned extrapersonal space. This is consistent with the nature of the right-left deficit in our own case. However our patient did not have any difficulty localizing objects in space and nor did he display any of the related topographical deficits observed in Gerstmann's case. The graphomotor constructional abnormality that Halpern documented was also not present in our case, and nor was the spatial dysgraphia described by Gerstmann. The only common sign, therefore, seems to be right-left disorientation in extrapersonal space.

In our case this right-left orientational deficit seems to have been part of a broader neuropsychological disorder. Special investigations in this regard indi­cated that he had general difficulty in establishing the orientation of isolated visuo-spatial configurations in the absence of an obvious contextual framework. It certainly seems plausible that this disorder was in some way directly related to the gross phenomenon of inverted vision, in our patient at least; but this con­stellation of deficits may not be present in other cases. Unfortunately, the lack of neuropsychological data in previous reports does not permit us to draw any definite conclusions in this regard. One can only hope that this problem, and the many other questions that arise in relation to the heuristically-intriguing phe­nomenon of inverted vision, will eventually be answered when further cases are identified and investigated.

After the submission of this article, Steiner, 1., Shahin, R., and Melamed, E. reported a further case of inverted vision ('Acute "upside down" reversal of vision in transient vertebrobasilar ischemia'. Neurology, 37: 1685-1686, 1987). As the title of the report

508 Mark Solms, Karen Kaplan-Solms, Michael Saling and Percy Miller

suggests, their case is very similar to the one described by Bender et aL, 1982 (see Table 1). The clinical picture is entirely consistent with the typical presentation described by us in this article.

ABSTRACT.

A case of bifrontal abscesses is reported. The patient claimed that he sometimes saw the world as if it were upside-down. A review of the literature reveals that, since 1805,21 similar cases have been documented. The present case is unusual in that the neuropsy­chological status of the patient is investigated in some detail, and in that it seems to be the first report of inverted vision in a case of frontal lobe disease.

Acknowledgements. Dr. E. Doctor, School of Psychology, University of the Witwa­tersrand, advised on the assessment and evaluation of W.B.'s reading. Prof. D. Saffer, Department of Neurology, Baragwanath Hospital, interpreted the E.E.G. readings. Dr. C. Martu, St. John's Eye Hospital, Baragwanath Hospital, conducted the opthalmological investigations.

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Mark Solms, School of Psychology, University of Witwatersrand, P.O. Wits, Johannesburg 2050, South Africa.