Neuropsychologia,Vol.33, No. 11, pp. 1373--138201995 ~ ) Copyright© 1995ElsevierScienceLtd Printedin GreatBritain.All rightsreserved 0028-3932195$9.50+ 0.00 Pergamon 0028-3932(95)00070-4 IMAGERY WITHOUT PERCEPTION--A CASE S T U D Y OF ANOSOGNOSIA FOR CORTICAL BLINDNESS GEORG GOLDENBERG,*I WOLF MTOLLBACHERt and ANDREAS NOWAK, "f2nd Neurological Department, Hospital Rosenhtigel, Vienna, Austria and/;Ophthalmological Department of the Hospital Lainz, Vienna, Austria (Received 25 April 1994; accepted 10 February 1995) A b s t r a c t - - A patient with complete cortical blindness after bilateral posterior cerebral artery infarctions denied her blindness. Her pretended visual experiences could frequently be traced back to synaesthetic translations of acoustic or tactile perceptions into mental visual images. Possibly, the belief to see resulted from a confusion of mental visual images with real percepts. The patient manifested preserved visual imagery also by correct responses to questions concerning the shapes of letters and the shapes and colours of objects. MRI showed an almost complete destruction of primary visual cortex with sparing of only small remainders of cortex at the occipital tip of the left upper calcarine lip, In the literature there are a few cases of denial of blindness with similarly severe damage to primary visual cortex but none with unequivocal evidence of complete destruction of primary visual cortex. We conclude that severe damage to primary visual cortex is compatible with visual imagery but that there is a possibility that islands of visual cortex must be spared to permit the generation of mental visual images. Key Words: imagery; blindness; anosognosia; visual cortex. INTRODUCTION The idea that similarities between visual imagery and visual perception are due to the involvement of identical cerebral structures found support in physiological studies which demonstrated activation of occipital cortex in healthy subjects engaged in visual imagery [6, 9, 11, 16-19, 21, 22, 30]. Recent advantages in PET and functional MRI imaging make it possible to distinguish the contributions of different cortical areas to occipital brain activity. Studies with both of these techniques showed activation of primary visual cortex in mental imagery [21, 22] in addition to activity in higher order visual cortex. The significance of these findings has, however, been called into question. On the one hand, other PET studies failed to find activation of primary visual cortex in mental visual imagery [31]. On the other hand, it has been argued that activation of an area during visual imagery does not necessarily prove that this area is critical to imagery [24]. The activation may reflect concomitant cognitive activities or shifts of attention which do not contribute to the generation of mental visual images. If primary visual cortex contributes to the mental experience of visual imagery, loss of it should impair or abolish imagery. Clinical data on this issue are scarce as case *Address for correspondence: Neurologisches Krankenhaus Rosenhiigel, Riedelgasse 5, A 1130 Wien, Austria. 1373 1374 G. GOLDENBERG, W. MOLLBACHER and A. NOWAK studies o f d i s o r d e r s o f m e n t a l i m a g e r y w e r e largely c o n d u c t e d o n p a t i e n t s in w h o m the lesions a f f e c t e d s e c o n d a r y v i s u a l a r e a s r a t h e r t h a n the p r i m a r y v i s u a l c o r t e x [see 14 f o r review]. A c o n d i t i o n w h i c h m i g h t a l l o w i n s i g h t i n t o the role o f p r i m a r y v i s u a l c o r t e x in v i s u a l i m a g e r y is a n o s o g n o s i a f o r b l i n d n e s s o r A n t o n ' s s y n d r o m e [2]. P a t i e n t s w i t h A n t o n ' s s y n d r o m e b e l i e v e t h a t t h e y a r e a b l e to see d e s p i t e a b s o l u t e blindness. T h e p a t i e n t s d o n o t s i m p l y d i s r e g a r d t h e i r b l i n d n e s s b u t p o s i t i v e l y r e p o r t v i s u a l p e r c e p t i o n s [2--4, 8, 12, 20, 23, 27, 29, 33]. P o s s i b l y , t h e s e d e s c r i p t i o n s refer to m e n t a l v i s u a l i m a g e s . A n t o n ' s s y d r o m e c a n o c c u r w i t h o c u l a r diseases o r o p t i c n e r v e a t r o p h y [7, 12, 26, 27, 29] as well as w i t h c o r t i c a l b l i n d n e s s [1-5, 8, 2 5 - 2 8 , 34-36]. P r e s e r v e d v i s u a l i m a g e r y in p a t i e n t s w i t h b l i n d n e s s d u e to d e s t r u c t i o n o f t h e p r i m a r y visual c o r t e x w o u l d be a s t r o n g a r g u m e n t a g a i n s t a c r i t i c a l i n v o l v e m e n t o f p r i m a r y visual c o r t e x in i m a g e r y . We recently observed a patient with transient cortical blindness and Anton's syndrome. T h i s g a v e us t h e o p p o r t u n i t y to i n v e s t i g a t e t h e r o l e o f m e n t a l v i s u a l i m a g e s in A n t o n ' s s y n d r o m e a n d to assess t h e e x t e n t o f d a m a g e to p r i m a r y v i s u a l c o r t e x . CASE REPORT H.S., a 46-year-old woman with 8 years of schooling suffered bilateral posterior cerebral infarction in November 1992. Ultrasonography showed occlusion of the tip of the basilar artery. Cardiac embolism was suspected but could not be proven. When taken to a rehabilitation unit 1 month after the accident, H.S. was cortically blind. Pupillar reaction to light was preserved but she could not discriminate between light and dark. Mobility was severely restricted because of tetraspasticity and ataxia, the latter being most marked on the left limbs and the trunk. In contrast to her repeatedly proven absolute blindness the patient spontaneously reported that sometimes she could see. She said that her sight was unreliable. Sometimes things around her would suddenly appear very clearly but after a few minutes they would vanish again. She never saw things which she believed to be unreal or unlikely to be visible, but when she grasped for a thing she had seen, for example a cup on the table, she could not find it where she expected it to be. She considered her visual abilities as being of little value in daily life, and when asked what her greatest problems were, she responded that these were her immobility and her 'bad sight'. She said that she had little hope of ever regaining normal vision. While mobility improved, her blindness remained unchanged during the following 3 months. Neuropsychological assessment, examination of visual evoked potentials and three video-taped explorations of her visual behavionr were performed during that time (see below). MRI was performed near the end of this period. The patient then returned in care of her family. When seen again 2 months later, her visual behaviour had changed. Her husband reported that she now actually saw things. She could describe them and reach them with her hands. The patient herself confirmed that her sight had improved and that now she could see things which previously she had not seen. On examination it was found that sight had indeed recovered within a narrow area of the right lower visual field. On Goldmann perimetry, the visual fields were restricted to the central 5 deg of the fight lower quadrant being slightly wider on the right eye than on the left. Within the intact field, visual acuity was 1.25 with the right, and 1.0 with the left eye. A second MRI was done, visual evoked potentials and the neuropsychological assessment were repeated, and two explorations of her visual behaviour were video-taped (see below). General neuropsychologicalfindings Only verbal tests could be given. Their results are summarized in Table 1. Her verbal IQ was 85 at the first examination in the period of anosognosia and 86 at the second examination after recovery of vision. At the first examination there was a marked memory deficit with delayed recall being nil for a list of 15 words as well as for the paragraphs of the Wechsler Memory Scale. However, recognition memory for words was better, and the patient was oriented to place, situation and approximate time and could remember day-to-day events. At the second examination there was only a slight improvement of episodic memory. Semantic memory, as assessed by sentence verification, was defective for both knowledge about non-visual and visual properties of objects. On the first examination, H.S.'s score was below the range of controls (13, 15) on lowimagery sentences and shape imagery sentences, and in the lower range on colour imagery sentences. On the second examinations, all scores were at the lower margin of the normal range. IMAGERY WITHOUT PERCEPTION Fig. 1. Coronal slices T 1 weighted MRI images with gadolinium enhancement. The right side of the images corresponds to the left side of the brain. Normal cerebral tissue appears grey, liquor cerebrospinalis black. The white structures are gadolinium enhanced and correspond to vessels in scar tissue and in the tentorium cerebelli. See text for the anatomical analysis of lesions. 1375 IMAGERY WITHOUT PERCEPTION 1377 Table 1. Results o f neuropsychological testing First examination Second examination Wais--R (age scaled scores) Information Digit span Vocabulary Arithmetics Comprehension Similarities 9 6 8 6 9 8 8 9 -4 8 11 7 0 9 1 4-6-5-6-5 0 6-8-6-7-7 1 12/2 10/4 10/0 14/7 Wechsler logical memory Immediate recall Delayed recall Learning of a 15-word list recall 5 Trials Delayed Recognition (correct/false positive) After 5th trial Delayed Verification of low- and high-imagery sentences (maximum score=25, change= 12.5) Low-imagery sentences Shape imagery sentences Colour imagery sentences 16 17 19 20 19 18 Range of controls 18-25 19-24 18-25 On neither examination did H.S. commit any errors when asked to describe the shape o f capital letters and to say which o f them had curved or straight lines. Visual evoked potentiais Flash stimuli were generated by a stroboscope with a flicker rate of 1 Hz and were presented to both eyes with eyelids closed. Checker board pattern were generated on a mirror with a reversal rate of 1 Hz and presented to both eyes separately. On the first examination no reproducible responses could be obtained by either checkerboard or flash stimulation. On follow-up after recovery o f vision checker board stimulation revealed normal cortical responses from both eyes. Magnetic Resonance Imaging There was no change in the M R I findings from the first to the second examination. Figure 1 shows images of the second examination. On the right side the parahippocampal and the temporo-occipital gyrus (Brodman's areas 28, 35, 36 and 37) are atrophic. The corresponding regions of the left hemisphere are preserved. In the fight hemisphere, areas 19 and 18 are destroyed, whereas in the left hemisphere area 19 and possibly also parts o f area 18 seem to be spared. Destruction o f the calearine cortex (area 17) is bilateral but near the occipital tip isolated fragments o f cortex can be seen more on the left than on the right side. Finally, there is a lesion o f the lateral thalamus on the fight side and a very small symmetric one on the right. Exploration of visual behaviour during period of blindness Sessions were conducted in daylight. The examiner (G.G.) sat opposite the patient with a table between them. The following transcript gives an impression of the patient's spontaneous statements about her visual abilities and her visual sensations: G.G.: Why are you here? H.S.: I had a stroke, I could not see anymore. G.G.: How are you now? H.S.: I am seeing a little, only contours. G.G.: Are you, for example, seeing me? H.S.: I see you as a contour. G.G.: What can you see of me? 1378 G. GOLDENBERG, W. MOLLBACHER and A. NOWAK H.S.: The head a n d . . , you are wearing a white coat* G.G. (covers his face with a black fan--the part of the conversation printed in italics takes place while the face is hidden behind the fan): Do you see my eyes? H.S.: Yes. G.G.: Do I wear glasses? H.S.: I think not. G.G.: Do you see whether I wear glasses? H.S.: I think that you don't wear glasses but I am not sure whether this is right. G.G.: Do you see whether I have a beard? H.S.: I don't think so. G.G.: Is there anything particular about my face? H.S.: No. G.G.: Do you see my face? H.S.: Yes. G.G.: Is my face light or dark? H.S.: You got some brown tan, not very light. G.G.: Are my hairs long or short? H.S.: A normal haircut. H.S. always described visual percepts which had a good likelihood o f being encountered in reality. Acoustic or taetual information about the identity of objects induced corresponding visual percepts: G.G.: (moves a bunch of small keys, producing sound) I am holding an object. Do you have any idea what it might be? H.S.: Could that be a key? G.G. (silently moves the keys beneath the table. The part of the conversation printed in italics takes place while the keys are hidden from view). What does it look like? H.S.: On top there is a big ring, and it has a dark key-bit. G.G.: Do you see the key well? H.S.: I am seeing that it is a key. G.G. (opens and shuts scissors): Do you have an idea what that might be? H.S.: Are those scissors? G.G.: Do you see them? H.S.: Only vaguely. I guessed a little. G.G. (silently hides the scissors beneath the table): What can you see o f these scissors? H.S.: Upside are the handles where you take them, and below them is the part f o r cutting. G.G.: Are you seeing this? H.S.: Yes. The patient insisted upon the visual nature of her sensation. She recognized that her visual sensations were not like normal visual perceptions, but at the same time would not accept the possibility that they were only mental images. H.S. was given a comb and recognized it from touch. G.G: Are you seeing that comb? H.S.: Only very little, I can only guess that it is a comb. G.G.: But this you could also guess from touch. H.S.: Yes, only from sight I could not recognize it definitely. G.G.: Are you really seeing it, or is it only a mental image? H.S.: I think I am seeing it a little, very weakly. I am seeing you too, sitting there in front of me, but also weakly. G.G.: Weakly? H.S.: Yes. G.G.: What does "weakly" mean? H.S.: It is vague a n d . . , somehow farther away, blurred. G.G.: How far away would you estimate that I am? H.S.: I would say that you are not directly in front of me. G.G.: A m I in a reaching distance? H.S.: Yes. G.G.: So this is about one meter or so? H.S.: Yes. G.G.: So, what do you mean by "farther away"? H.S.: Well, about two to three meters. G.G.: That's what it looks like? H.S.: Yes. G.G.: Although you know that I am only one meter away from you? H.S.: Yes, it looks rather farther away. G.G.: How do you recognize that it is farther away? H.S.: You are somehow smaller than if you were there where I know that you are. G.G.: Am I a real, concrete image? H.S.: I do see you, yes. *This happened to be true. Doctors usually wear white coats anyway. IMAGERY WITHOUT PERCEPTION 1379 Visual sensations could also be induced by telfing the patient that in front of her was a visible object. If there were no extra-visual clues to the nature of the object or if there was no object at all the patient most frequently believed to see pieces of stationery. By further questioning she could be induced to describe visual details of the presumed objects. G.G. (holds a comb): Can you recognize anything? H.S.: An exercise book or a book. G.G.: What are you s~ing? Can you describe that? H.S.: It looks like an exercise book. G.G.: Is it big or small? H.S.: A small exercise book, a normal one, like those you use in school. G.G.: Does it have a colour? H.S.: I think it is brown. G.G.: Is there anything on its cover7 H.S.: I think there is something written on it. G.G.: What could that be? H.S.: I don't know. G.G.: Do you see what type of writing that is? H.S.: I don't know how to call that type of writing. There arc small letters. G.G.: Capital letters? H.S.: No, no capital letters. G.G.: Latin Script? H.S.: Yes. G.G.: Do you know this exercise book7 H.S.: No. Just a school exercise book. G.G.: Does it look like an exercise book which you owned once? H.S.: Yes. G.G.: Could that be an old exercise book of yours? H.S.: Yes. G.G. (hides the comb beneath the table): Could it be that the image of this exercise book comes from your memory, and that in reality there is no exercise book? H.S.: I do see that there is an exercise book. G.G.: Can you tell me where you see it? H.S.: There, rather on the right (points into the right lower quadrant of her visual field).* G.G.: Above or below? H.S.: Up there, above (raises hand to height of eyes). At the height of my eyes. G.G.: Who is holding the exercise book? H.S.: You. G.G.: With which hand? H.S.: With the left. G.G.: Am I moving the exercise book? H.S.: I don't think so. G.G.: Are you seeing my hand? H.S.: Only vaguely. G.G.: But is it really what you are seeing? H.S.: Yes. Visual behaviour after recovery o f sight Due to the severe restriction of visual fields the patient had great problems in finding objects, but whatever fell into her intact visual field was normally described and recognized. She denied any sight of objects outside the intact visual field. If she recognized invisible objects by sound or touch she could not be induced to believe that she had seen them. G.(J. (holds a comb into the blind part of the patient's visual field): I am holding an object in front of you. Do you recognize that there is something? H.S.: No. G.G. (Moves the teeth of the comb to produce a sound): Can you recognize what it is? H.S.: A comb. G.G.: Do you see it now? H.S.: No. G.G.: Are you still not seeing it? H.S.: No. G.G.: Do you know that it is there? H.S.: Yes, I heard it. G.G.: But are you really sure that you don't see it? H.S.: Yes. GG.: Can you imagine how it looks like? *On other occasions she would grasp to her left side when searching for an object which she pretended to see. 1380 G. GOLDENBERG, W. MI]LLBACHER and A. NOWAK H.S.: Perhaps a pocket-comb? G.G.: If you are imagining that, can you see it? H.S.: No. G.G. 0aolds a toothbrush into the blind part of the visual field): I am now holding something else. C a n you see it? H.S.: Perhaps you could move it a bit? G.G. (strokes the bristles to produce sound): Do you have an idea what it could be? H.S.: Yes, from hearing. Perhaps a brush? G.G.: If you are hearing it now, can you imagine how it looks like? H.S.: Well, probably yes. A hair-brush perhaps. G.G.: D o you see it in front of you? H.S.: No. G.G.: A n d if you imagine it, do you see it? H.S.: There are m a n y kinds of hair-brushes. I can imagine how they look like but not the one which you have in your hand. G.G.: Do you have in front of you an image as if there was a hair-brush? H.S.: I heard the brush but in front of me I see the wall. DISCUSSION Mental visual images are hidden from external observation. There is thus only indirect evidence that H.S. did have mental visual images and mistook them for real percepts. H.S. insisted upon the visual nature of her perceptions while admitting that her visual sensation were "weaker" and "farther away" than real percepts. It is unlikely that she would have stressed these qualities which call into question the reality of her pretended vision if she had invented descriptions of visual percepts solely to justify the denial of blindness. It does appear much more plausible that she actually experienced visual sensations, and that the denial of blindness was a consequence of these experiences. H.S.'s visual experiences could be provoked by verbal stimulation and by acoustic or tactile perceptions. It has been noted in previous descriptions of the syndrome that pretended visual perceptions of patients with Anton's syndrome can sometimes be traced back to synaesthetic translation of acoustic or tactile perceptions into mental visual images [12, 23, 27]. Redlich and Bonvicini wrote: "By confusing memory images with perceptions the patient has sufficient material for his pretended vision. When he hears the sound of lighting a match or feels its warmness he believes to see it" [27, p. 950]. A patient described by one of us [12] claimed that he could watch television but remarked that his vision was abnormal in that he could see the screen and at the same time see a person walking between the screen and himself. This strange visual illusion could be explained by a synaesthetic translation of acoustic perceptions into mental visual images. Sound is transparent. One can perceive and distinguish sounds emitted by two sources located one behind the other. Spontaneous synaesthetic visual imagery is not a rare phemomenon in healthy subjects. There are persons who cannot think of a visible thing without seeing it as a mental visual image [16, 18, 32]. In adventiously blinded persons, the lack of interference from actual visual perception may enhance the frequency and vividness of spontaneous visual imagery. Additional evidence for H.S.'s preserved ability to form mental visual images was provided by her performance on imagery tasks. She could perfectly answer questions concerning the shape of letters. The number of correct responses to high-imagery sentences was at the lower margin of the normal range or even lower, but the number of correct responses to low-imagery sentences was not all higher. This pattern of results would point to a general deterioration of semantic memory, or, respectively, to general difficulties with sentence verification but not to specific problems with visual imagery. By contrast, in a patient with loss of visual imagery a marked difference in favour of low-imagery sentences was obtained with the same set of questions [13]. As indicated by the low score on WAIS--R digit span, H.S.'s verbal short-term memory was reduced, and because she was IMAGERY WITHOUT PERCEPTION 1381 blind she could not read the sentences in addition to hearing them. She may have had particular difficulties with keeping the sentences in working memory. From the first to the second examination, an increase in digit span was accompanied by an increase in the number of correct responses to low-imagery and shape-imagery sentences. In sum, there is evidence that H.S. could generate mental visual images, and it does appear plausible that her denial of blindness resulted from a confusion between mental visual images and real percepts. If H.S.'s denial of blindness was indeed a sequel of spontaneous visual imagery, then her case demonstrates that an almost complete destruction of primary visual cortex still allows for the generation of mental visual images which are vivid enough to be mistaken for visual perceptions. Destruction of primary visual cortex was, however, not complete. MRI demonstrated preservation of islands of intact cortex the largest of which was located at the occipital tip of the upper left calcarine lip. In the further course vision recovered in a part of the visual field which corresponded to the location of this island. In the literature we could find only a handful of cases of anosognosia for occipital blindness in whom the anatomy of the lesion was assessed by neuroradiological imaging or post-mortem [2, 4, 5, 8, 25, 27, 28, 34-36]. Total destruction of the calcarine cortex was diagnosed in two of them [5, 25], and in these cases the diagnosis was based on CT-scans which may not be sufficient to exclude the persistence of small remainders of cortex. In two autopsied cases destruction of the calcarine cortex was almost complete. In one of them the left calcarine cortex was completely destroyed while on the right side "smallest remainders of the cortex of the calcarine fissure were preserved but completely isolated" [28, p. 30], and in the other "some fragments of calcarine cortex could be identified only in the poles of the occipital lobes but these contained hardly any fibres" [34, p. 142]. 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