- Email: [email protected]
Denial of visual perception
BRAIN
AND
COGNITION
16, 29-40 (1991)
Denial of Visual Perception JOEL A. HARTMANN AND WILLIAM A. WOLZ University
of Missouri
DAVID P. ROELTGEN Hahnemann
University AND
FELICEL. LOVERSO Braintree
Hospital
An adult with the diagnosis of cortical blindness, complaining of a complete visual loss of 2 years in duration, was found to have a small preserved visual field and remarkably preserved visual abilities. Although denying visual perception, he correctly named objects, colors, and famous faces, recognized facial emotions, and read various types of single words with greater than 50% accuracy when presented in the upper right visual field. Upon confrontation regarding his apparent visual abilities, the patient continued to deny visual perceptual awareness, typically stating “I feel it.” CT indicated bioccipital lesions sparing the left inferior occipital area but involving the left parietal lobe. The denial of visual perception evidenced by this patient may be explained by a disconnection of parietal lobe attentional systems from visual perception. The clinical presentation is described as representing “inverse Anton’s syndrome.” a 1991 Academic PUSS, 1~.
Cortical blindness is a syndrome resulting from bilateral occipital lesions involving the striate cortex, whereby visual sensation and reflex lid closure are lost, yet normal retinal structure, ocular motility, and reflex pupillary constriction are retained. Patients with large visual field loss (e.g., sparing This paper was presented in part at the Annual Meeting of the International Neuropsychological Society, Denver, CO, 1986. Dr. Roeltgen is the recipient of NIH Teacher Investigator Development Award KOl N500807. The authors thank Bari Searles for manuscript preparation. Correspondence and reprint requests should be addressed to David Roeltgen, Center for Neurological Research, Department of Neurology, Hahnemann University, Broad and Vine, M. S. 423, Philadelphia, PA 19102. 29 0278-2626/91 $3.00 Copyright 0 1991 by Academic Press, Inc. All rights of reproduction in any form reserved.
30
HARTMANN
ET AL.
only small portions of the macular region or small wedge-shaped areas extending from the macula to the periphery) are usually fully aware of both their deficits and their preserved visual ability (Walsh & Hoyt, 1969). However, cases have been presented where individuals report or demonstrate visual perception within a blind visual field (i.e., cases of “blindsight” and covert visual recognition (Bauer, 1984; Tranel & Damasio, 1985). The present case illustrates a phenomenon not clearly documented previously, that of complete denial of intact visual perception in the absence of conversion disorder. Denial of visual loss and confabulation of responses among cortically blind individuals are not rare (Redlich & Dorsey, 1945). Anton (1898, 1899) described four such patients and concluded that the syndrome of denial of sensory deficiency due to cerebral lesions is caused by destruction of association tracts. This condition, commonly referred to as “Anton’s syndrome ,” is not to be confused with cases of more global mental deterioration, hallucinations, or hysterical manifestations. The presentation of denial of sensory deficiency may occur with various psychiatric disturbances or general disorientation; however, such conditions would preclude the diagnosis of Anton’s syndrome. The label “inverse Anton’s syndrome” has been used to describe a condition in which patients with a spared central island of vision deny visual sensation (Walsh & Hoyt, 1969). Reports describing this condition are rare and inadequately detailed in description, and therefore do not clearly document the clinical existence of this syndrome. Three such reports are described briefly below. Forster (1890) described a case that Gloning, Gloning, and Tschabitscher (1962) later cited as a classic presentation of inverse, or “negatives,” Anton’s syndrome. Forster’s patient developed bilateral homonomous hemianopsia as a result of two strokes, occurring 5 years apart. The patient behaved as though he were completely blind in spite of demonstrating preserved central vision (he could read script slowly). In the original paper, there is no indication as to whether this patient acknowledged or denied his residual visual ability. In 1899, Gaupp described a patient with a history of partial cortical blindness who later complained of complete blindness and amnesia following a neurologic event subsequent to running over an elderly woman with a carriage. A careful examination of this patient by Forster revealed a small intact visual field. His vision slowly returned. This patient’s apparent hysteria renders it impossible to determine whether the denial of vision noted in this case clearly represents inverse Anton’s syndrome. Finally, Redlich and Bonvicini (1908) described a patient originally reported by Laqueur (1898) who was cortically blind with secondary
DENIAL
OF VISUAL
PERCEPTION
31
depression. He behaved much like a blind person, requiring assistance to move about. This patient was noted to be surprised when color vision and some degree of visual acuity in the central portion of the visual field were demonstrated. It is not clear whether this represented a sudden awareness of existing but previously denied visual ability or a recovery of visual function over time. We report a patient who had been diagnosed as cortically blind 2 years prior to the present evaluation. He maintained that he was completely unable to see. Upon careful examination, this patient evidenced a small preserved visual field and remarkably preserved visual abilities. In spite of demonstrated visual ability, he continued to deny awareness of visual percepts. This denial demonstrated by our patient represents a clinical presentation of “inverse Anton’s syndrome.” The findings are discussed with reference to related visual disturbances and with regard to the proposition that conscious identification of a percept may not be necessary for semantic activation. CASE REPORT The patient, a 56-year-old right-handed college educated male, reported that 2 years prior he had been “sitting, eating breakfast . . . looked up and everything went black.” The diagnosis was blindness due to bilateral cerebral infarction. The patient stated that he had regained no visual ability since the incident. After the initial hospitalization he was largely independent in living skills, typing grocery lists, cooking his own meals, and taking care of his own affairs with the assistance of a housekeeper. He was able to ambulate in unfamiliar surroundings without assistance. His interests included the buying and selling of horses. When asked how he judged these horses, he stated “by their sound and their feel.” He stated that independent living was very important to him. Only shortly prior to assessment, at the insistence of a friend, had he made contact with the Society for the Blind. He had attended meetings but never had applied for services. In addition, although he was a patient within the Veterans Administration Health Care System, he never attempted to gain benefits or services for impaired vision. In fact, he repeatedly downplayed his complaint of lack of sight, stating that he could compensate for it by “feel,” such as the method by which he judged horses. Medical history was positive for a stroke resulting in speech impairment approximately 1.5 years prior to the present assessment. The patient stated that he fully recovered with “teaching” (speech therapy). He was referred for evaluation at this time in response to a recent sudden onset of “confusion” and left-sided weakness.
32 Neurological
HARTMANN
ET AL.
Examination
Upon examination, 2 weeks later, the patient was alert, attentive, and cooperative. He was sufficiently attentive that during assessment sessions lasting an hour or more, he rarely, if ever, needed to be redirected to a task or activity. This included 20- to 30-min sessions of tachistoscopic reading. He was oriented to person, place, situation, and in a general sense to time. There was no evidence of confusion. The patient had normal pupillary responses and ocular motility. He demonstrated left-sided weakness and sensory loss, as well as moderate left-sided hypokinesis. A Babinski was also present on the left side. Except for vision, the remainder of the noncognitive aspects of the neurological examination was normal.
Neuropsychological
Examination
Cognitively, the patient demonstrated decreased digit span and slightly decreased short-term memory. He remembered one of three objects at 5 min, but when given the date and day was able to remember it during the testing session and when examined the next day. He clearly recognized and distinguished each of his examiners (three males and one female) without difficulty. This recognition was assessed and appeared to be accurate utilizing either voice or facial characteristics. On oral language examination, he had a mild anemic aphasia. His speech was fluent with occasional semantic paraphasic errors. For conversational speech, he had no difficulty communicating. Repetition ability was intact, and auditory-verbal comprehension was normal for conversational speech. However, comprehension was mildly impaired at the level of complex syntactic commands. Visual naming of common objects was 50% accurate with semantic errors and occasional circumlocutions. Cross model naming between smell (matches, tobacco, soap) and vision was similar. Tactile discrimination of complex stimuli (double simultaneous stimulation) was impaired bilaterally, being more impaired on the left than on the right. The patient was unable to name objects utilizing only tactile processing. However, his naming of an object to its description was correct on 8 of 10 trials. Importantly, the patient showed a striking correlation between his responses and the circumstances of stimulation. For example, for reading assessment, in addition to untimed reading (see below) the patient was tested with tachistoscopic reading. On this task he was asked to fixate on a large red circle prior to each exposure. At exposures greater than 700 msec he had a consistent accuracy rate of 20 to 25% for a standard set of stimuli. This accuracy rate declined in a steady fashion at lOO-msec intervals until 300 msec at which his accuracy dropped below 10%.
DENIAL
FIG.
OF VISUAL
PERCEPTION
33
1. Visual field plots revealing the area of spared vision in the upper right quadrant.
Visual Examination
A striking observation was what appeared to be occasional visual fixation, inconsistent with the patient’s diagnosis of complete cortical blindness and self-report of an inability to see. Residual visual ability was confirmed when testing for optokinetic nystagmus. The patient responded by stating that the test stimulus (a cloth) was moving. It was soon ascertained that he was able to make such identifications by sight. However, when asked how he made them, he denied visual perception and alternatively replied “I feel it, ” “I feel like something is there,” “it clicks,” or “I feel it in my mind.” Over a series of testing sessions lasting almost 2 months, there was an interesting evolution in his responses to these same questions. After 2 or 3 weeks when asked how he was able to read (especially during the tachistoscopic assessment), he began to reply that he didn’t know but that “you (the examiners) told me that I can see it, so I must be able to see it.” However 1 to 2 weeks later, after being told by his primary physicians and the ophthalmologists that he was blind, he reverted to his previous explanations for his ability to appreciate the stimuli. To confrontation testing of the visual fields using a finger counting task, the patient exhibited preserved vision in a wedge-shaped area approximately 30 degrees in size in the right upper quadrant, respecting the vertical meridian and extending to the periphery (Fig. 1). More formal visual field mapping could not be accomplished due to the patient’s poor visual fixation. In this area of intact visual field, acuity, based on analysis of reading ability, was 20/50 or better for both close and distant gaze. Similar to other tasks, this assessment was repeated on multiple occasions and the results were consistent. Visual language (reading) abilities. Several discrete visual tasks were employed to more thoroughly evaluate the patient’s residual visual perceptual and processing abilities. Assessment of written language processing was emphasized to enable simultaneous evaluation of visual perception and language function which was hypothesized to be impaired given his previous left hemisphere stroke. Among the areas evaluated was oral reading, for which the patient was administered portions of the Battery of Linguistic Analysis for Writing and Reading (BLAWR; Roeltgen, Cor-
34
HARTMANN
ET AL.
dell, & Sevush, 1984). Overall, the patient was correct in reading 118 of 230 (51%) real words varying in class, imageability, regularity, and length. The majority (47%) of his reading errors were visual errors (e.g., “smile” for “while”) as is frequently noted in patients with visual field impairment. In addition, the latter portion of the target word was retained with the errors occurring in the initial portion of the word (e.g., “community” for “opportunity,” and “confidence” for “evidence”), consistent with his mild left hemispatial neglect. When exposure to stimulus words was limited via tachistoscopic presentation, the patient would occasionally state that the words disappeared from his mind or that he could no longer “feel” them although they were still being presented. At other times, he stated that the stimulus word persisted after it had been withdrawn. Visual versus nonvisual object naming. The patient was able to name 5 of the first 10 objects from the Western Aphasia Battery presented visually. He produced infrequent semantic paraphasias in object naming. Performance did not improve by moving the stimulus object within the intact visual field. As mentioned previously, he was unable to name objects via tactile information alone. It is therefore clear that he utilizes, and in fact relies upon, visual ability in object identification. Facial recognition. The patient was able to recognize and accurately describe five of five pictorially depicted facial emotions. He was also able to identify famous faces, although he gave frequent anemic responses (e.g. “a well-known Republican from Arizona” for Barry Goldwater). He also made one semantic error, referring to John F. Kennedy as “Jimmy Carter.” Color Naming. A modified version of the Stroop Task was administered to assess color naming ability. This task consisted of presenting slides of individual color names illustrated in incongruous colors and requiring the subject to make an overt identification of the color. The task is typicaily employed as a measure of perceptual interference. With no time constraints and frequent redirecting by the examiner to aid the patient in overcoming the printed word interference, the patient was able to accurately name the color on 12 of 20 trials. Qualitatively, he maintained that he could “feel” or “hear” the color and his initial responses were consistent with such perceptions. For example, to the color orange he responded “like sky . . . like sunset,” and to green he stated “I feel something clear.” These responses indicated impairment at the level of color naming, as opposed to a perceptual deficit. It is interesting to note that the patient was unable to effectively discriminate whether a room was dark or illuminated, responding at chance levels. Anatomy
CT scan revealed three well-defined lesions (Fig. 2). One involved the lower portion of the right occipital lobe, extending up through the cal-
DENIAL
OF VISUAL
PERCEPTION
0 9 E QD
a 2a. Plot of computerized tomography revealing an extensive lesion of the left inferior parietal lobule and lateral occipital gyrus, also involving the left medial superior occipital region. A second lesion involved the right calcarine region and occipital temporal gyri. A lesion involving the right superior perisylvian region was also present. Darkened area indicates well-defined low density. Stippled area indicates ill-defined low density. (Left side of figure indicates left side of brain.) (Plot angle and level of cuts do not correspond to the angle and level of cuts on the actual CT scan, see Fig. 2b). FIG.
carine fissure. The second lesion involved the left parietal-occipital region, including a small portion of the superior parietal lobule, the angular gyrus, the superior marginal gyrus, and other aspects of the medial and lateral occipital lobe. It ended approximately at the level of the calcarine fissure, sparing the medial-temporal and temporal-occipital areas. This lesion was perhaps continuous with additional ill-defined lucency in the posterior temporal region on the left. The third discrete lesion, apparently related to the most recent stroke, involved the right frontal and parietal opercula. DISCUSSION
Denial of cortical blindness (Anton’s syndrome) has been reported (Anton, 1898, 1899). Reference has also been made to the phenomenon of denial of visual perception, termed “inverse Anton’s syndrome” (Walsh & Hoyt, 1969). We are, however, not aware of reports describing patients with clearly documented preserved vision, particularly to the extent displayed by this patient, who were unaware of their visual abilities. While
36
HARTMANN
ET AL.
FIG. 2b. Representative cuts from the CT scan.
denial of vision has been suggested in previous case studies, confounds such as lack of notation regarding the patient’s awareness of his vision (Forster, 1890; Laqueur, 1898) and apparent patient hysteria (Gaupp, 1899) have obscured the possible diagnosis of this clinical syndrome. Our patient was neither disoriented nor hysterical, yet he maintained being totally unaware of his well-documented visual skills. Also, there was no evidence of any secondary gain. In contrast to seeking secondary gain, this patient had avoided support of any kind for his blindness. We believe this case clearly represents a clinical presentation of inverse Anton’s syndrome. This syndrome may share features with related disorders, namely, “blindsight” and visual agnosia (including prosopagnosia), as discussed below.
DENIAL
OF VISUAL
PERCEPTION
37
Relation to Blindsight A syndrome referred to as “blindsight” has been described in which patients demonstrate primitive visual skills, such as light detection and orientation to a target within a perimetrically blind visual field (Poppel, Held, & Frost, 1973; Weiskrantz, Warrington, Sanders, & Marshall, 1974; Perenin & Jeannerod, 1975, 1978). These patients are unable to make conscious identification of more complex visual stimuli in the “blind” visual field. This phenomenon has been noted in patients with ablations of the geniculostriate, or primary visual pathway. The preserved visual ability is thought to be due to a second, noncalcarine visual system (colliculus-pulvinar-parietal lobe pathway), and is said to function in the detection of events, spatial localization, and the control of orienting responses to visual events (Zihl & Von Cramon, 1979). Like our patient, some patients demonstrating blindsight state that they “feel” objects appearing within the blind visual field, indicating a loss of the subjective experience of visual sensation in the “blind” region (Poppel et al., 1973). In contrast to blindsight, our patient’s visual abilities were examined within an intact portion of the visual field. His visual processing likely incorporated utilization of the primary visual pathway. CT did depict a normal area corresponding to the inferior striate cortex consistent with the preserved visual field. Furthermore his residual visual ability was superior to that indicated from blindsight. The patient was able to correctly identify numerous types of visual information presented within the small intact visual field. Disruption of the “Second” Visual Pathway It is possible that the patient’s lack of awareness of visual perception could be due to a deficit in orienting to visual stimuli. As visual orienting is believed to be a function of the “second” visual pathway, one may propose that this colliculus-pulvinar-parietal lobe pathway had been functionally ablated. The fact that he was unable to discriminate light from dark is consistent with this hypothesis, as this ability is also considered a function of the second visual system. While (by CT analysis) this anatomical pathway was possibly ablated in the left hemisphere in this patient, it was apparently intact on the right. This suggests that either the pathway must be intact in both hemispheres for adequate orienting function to occur or other lesions remote from this pathway may produce a deficit in orienting to visual stimuli. The latter hypothesis is more plausible, as many patients are seen with unilateral lesions of this system without demonstrating denial of vision. Alternatively, the described deficit may be due to impaired attentional or registration mechanisms, as opposed to visual orienting mechanisms. This patient fulfills neither the criteria for blindsight nor disruption of
38
HARTMANNETAL.
the second visual pathway. More accurately, his impairment appears related to the fact that the identification of the visual stimuli was not a conscious process for this individual. While able to attribute meaning to the visual information, as evidenced by the reading and naming of visually presented material, he maintained that he was not aware of any visual sensation. It is suggested that the patient’s visual perception is disconnected from the awareness of the visual construct. Relation
to Prosopagnosia
At one level, perception without awareness has been demonstrated in a distinct clinical population. Patients with prosopagnosia, a specific form of visual agnosia, have perception but no conscious awareness of meaning. Some of these patients have been found, via physiological indices (e.g., galvanic skin resistance), to have at least some recognition of faces that they state they do not recognize (Bauer, 1984; Tranel & Damasio, 1985). This was accomplished via an adaptation of the “guilty knowledge test” (Lykken, 1960), whereby electrodermal responses were compared with verbal naming responses using familiar and unfamiliar faces as stimuli. These patients evidenced recognition of familiar faces through increased electrodermal responding, although their overt naming was severely compromised. This suggests that some patients with prosopagnosia activate some semantic representations of these faces in memory, but remain unable to make overt identifications of these faces. Similarly, our patient demonstrated the ability to access and utilize visual information. However, he was unaware that the input modality was in fact visual. Clearly, this deficit was not in recognition, as he was able to make appropriate responses to visual information, thus distinguishing his presentation from visual agnosia. By definition, visual agnosia represents a failure of recognition whereby a normal percept is stripped of its meaning (Teuber, 1968). Using parallel terminology, our patient may be said to acquire meaning stripped of its percept. Attentional
versus Semantic Disconnection
A possible explanation for the discrepancy between the demonstrated preserved visual ability in our patient and his denial of such ability includes the involvement of attentional mechanisms. Although sufficient quantity and quality of visual information were available to register and interact with linguistic and semantic systems (for reading and naming), important cerebral interactions of some other type were lacking. This may be similar to the demonstration of semantic activation via tachistoscopic presentation of stimuli. It has been suggested that under such a condition, a semantic activator bypasses attentional systems and is processed at the semantic level. Anatomic correlates of attentional and semantic processing mechanisms are, in general, poorly defined. However, the inferior parietal
DENIAL
OF VISUAL
PERCEPTION
39
lobule is known to be an important mechanism in attention (Lynch, Mountcastle, Talbot, & Yin, 1977; Mountcastle, 1978). Some of the most severe forms of hemispatial neglect occur from inferior parietal lobule lesions, more commonly from right hemispheric lesions, but also from left hemispheric lesions. The CT scan of our patient indicates the presence of a lesion involving the majority of the left inferior parietal lobule. In addition, the extension of a second right hemispheric posterior lesion was such that it may have functionally disconnected the right occipital lobe from the relatively intact right inferior parietal lobule. Thus, the limited visual information from the left inferior occipital lobe may not have been able to gain access to the right parietal lobe. This may have prevented the visual information from accessing the attentional systems. McGlynn and Schacter (1989) have suggested that awareness of impairment may be secondary to either a disruption of a posterior conscious awareness system or a disruption of an anterior executive system. They alternatively suggest that lack of awareness might occur secondary to inadequately activated information being transmitted to the conscious awareness system. Our patient’s frontal lobes were largely intact. Therefore, a disturbance of the anterior executive system is unlikely. However, our patient’s deficits and lesions are compatible with the contention that awareness for vision was disrupted because of a disturbance of the conscious awareness system, a disconnection of the visual information from the conscious awareness system, or both. In contrast, this same visual information did reach the patient’s memory systems, as he was able to report familiarity with visual items that were presented to him on previous occasions. In this respect, it is possible that our patient differs from those with prosopagnosia in that his visual perception is disconnected from attentional and awareness systems rather than from memory systems. REFERENCES Anton, G. 1898. Uber Herderkrankungen des Gehirnes, welche vom Patienten selbst nicht wahrgenommen werden. Wiener Klinische Wochenschriff. 11, 227-229. Anton, G. 1899. Uber die Selbstwahrnehmung der Herderkrankungen des Gehirns durch den Kranken bei Rindenbhndheit und Rindentaubheit. Archiv fur Psychiatric und Nervenkrankheiten, 32, 86-127. Bauer, R. M. 1984. Autonomic recognition of names and faces in prosopagnosia: A neuropsychological application of the guilty knowledge test. Neuropsychologia, 28, 457470. Forster, 0. 1980. Ueber Rindenblindheit. Albrecht von Gruefes Archiv fur Ophthalmologic, 36, 94-108. Gaupp, R. 1899. Uber corticaie Blindheit. Monatsschriff fur Psychiatric und Neurologie, 5, 28-41. Gloning, I., Gloning, K., & Tschabitscher, H. 1962. Die occipitale Blindheit und vascularer Basis: Untersuchungsergebnisse von 16 eigenen Fallen. Albrecht von Graefe’s Archiv fur Ophthalmologic vereinigt mit Archiv fur Augenheilkunde, 165, 138-177. Laqueur, L. 1898. Ein Fall von doppelseitiger homonymer Hemianopsie mit Erhaltung eines
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minimalen zentralen Gesichtsfeldes mit Sektionsbefund. Bericht aus der OpthalmoloGesellschaft zu Heidelberg, 218. Lykken, D. T. 1960. The validity of the guilty knowledge technique: The effects of faking. Journal of Applied Psychology, 44, 485-534. Lynch, J. C., Mountcastle, V. B., Talbot, W. H., & Yin, T. C. T. 1977. Parietal lobe mechanisms for directed visual attention. Journal of Neuropsychology, 4, 362-389. McGIynn, S. M., & Schacter, D. L. 1989. Unawareness of deficits in neuropsychological syndromes. Journal of Clinical and Experimental Neuropsychology, 11, 143-205. Mountcastle, V. B. 1978. Brain mechanisms for directed visual attention. Journal of the Royal Society of Medicine, 71, 14-28. Perenin, M. T., & Jeannerod, M. 1975. Residual vision in cortically blind hemifields. Neuropsychologia, 13, l-7. Perenin, M. T., & Jeannerod, M. 1978. Visual function within the hemianopic field following early cerebral hemicortication in man. I. Spatial localization. Neuropsychologia, 16, l13. Poppel, E., Held, R., & Frost, D. 1973. Residual visual function after brain wounds involving the central visual pathways in man. Nature, 243, 295-296. Redlich, E., & Bonvincini, G. 1908. Ueber das Fehlen der Wahmehmung der eigenen Blindheit bei Hirnkrankheiten. Jahrbucher fur Psychiatric und Neurologie, 29, 1-133. Redhch, F. C., & Dorsey, J. F. 1945. Denial of blindness by patients with cerebral disease. Archives of Neurology and Psychiatry, 53, 407-417. Roeltgen, D. P., CordelI, C., & Sevush S. 1984. A battery of linguistic analysis for writing and reading. Paper presented at the international Neuropsychological Society, Houston. Abstract published in The INS Bulletin, October, 1983. Teuber, H.-L. 1968. Alteration of perception and memory in man. In L. Weiskrantz (Ed.), Analysis of Behavioral Change. New York: Harper and Row. Tranel, D., & Damasio, A. R. 1985. Knowledge without awareness: An autonomic index of facial recognition by prosopagnosics. Science, 228, 1453-1454. Walsh, F. B., & Hoyt, W. F. 1969. Clinical Neuro-Ophthalmology, Third Edition. Baltimore: Williams & Wilkins. Pp. 1629-1926. Weiskrantz, L., Warrington, E. K., Sanders, M. D., & Marshall, J. 1974. Visual capacity in the hemianopic field following a restricted occipital ablation. Brain, 97, 719-728. Zihl, J., & Von Cramon, D. 1979. The contribution of the ‘second’ visual system to directed visual attention in man. Brain, 102, 835-856. gische
AND
COGNITION
16, 29-40 (1991)
Denial of Visual Perception JOEL A. HARTMANN AND WILLIAM A. WOLZ University
of Missouri
DAVID P. ROELTGEN Hahnemann
University AND
FELICEL. LOVERSO Braintree
Hospital
An adult with the diagnosis of cortical blindness, complaining of a complete visual loss of 2 years in duration, was found to have a small preserved visual field and remarkably preserved visual abilities. Although denying visual perception, he correctly named objects, colors, and famous faces, recognized facial emotions, and read various types of single words with greater than 50% accuracy when presented in the upper right visual field. Upon confrontation regarding his apparent visual abilities, the patient continued to deny visual perceptual awareness, typically stating “I feel it.” CT indicated bioccipital lesions sparing the left inferior occipital area but involving the left parietal lobe. The denial of visual perception evidenced by this patient may be explained by a disconnection of parietal lobe attentional systems from visual perception. The clinical presentation is described as representing “inverse Anton’s syndrome.” a 1991 Academic PUSS, 1~.
Cortical blindness is a syndrome resulting from bilateral occipital lesions involving the striate cortex, whereby visual sensation and reflex lid closure are lost, yet normal retinal structure, ocular motility, and reflex pupillary constriction are retained. Patients with large visual field loss (e.g., sparing This paper was presented in part at the Annual Meeting of the International Neuropsychological Society, Denver, CO, 1986. Dr. Roeltgen is the recipient of NIH Teacher Investigator Development Award KOl N500807. The authors thank Bari Searles for manuscript preparation. Correspondence and reprint requests should be addressed to David Roeltgen, Center for Neurological Research, Department of Neurology, Hahnemann University, Broad and Vine, M. S. 423, Philadelphia, PA 19102. 29 0278-2626/91 $3.00 Copyright 0 1991 by Academic Press, Inc. All rights of reproduction in any form reserved.
30
HARTMANN
ET AL.
only small portions of the macular region or small wedge-shaped areas extending from the macula to the periphery) are usually fully aware of both their deficits and their preserved visual ability (Walsh & Hoyt, 1969). However, cases have been presented where individuals report or demonstrate visual perception within a blind visual field (i.e., cases of “blindsight” and covert visual recognition (Bauer, 1984; Tranel & Damasio, 1985). The present case illustrates a phenomenon not clearly documented previously, that of complete denial of intact visual perception in the absence of conversion disorder. Denial of visual loss and confabulation of responses among cortically blind individuals are not rare (Redlich & Dorsey, 1945). Anton (1898, 1899) described four such patients and concluded that the syndrome of denial of sensory deficiency due to cerebral lesions is caused by destruction of association tracts. This condition, commonly referred to as “Anton’s syndrome ,” is not to be confused with cases of more global mental deterioration, hallucinations, or hysterical manifestations. The presentation of denial of sensory deficiency may occur with various psychiatric disturbances or general disorientation; however, such conditions would preclude the diagnosis of Anton’s syndrome. The label “inverse Anton’s syndrome” has been used to describe a condition in which patients with a spared central island of vision deny visual sensation (Walsh & Hoyt, 1969). Reports describing this condition are rare and inadequately detailed in description, and therefore do not clearly document the clinical existence of this syndrome. Three such reports are described briefly below. Forster (1890) described a case that Gloning, Gloning, and Tschabitscher (1962) later cited as a classic presentation of inverse, or “negatives,” Anton’s syndrome. Forster’s patient developed bilateral homonomous hemianopsia as a result of two strokes, occurring 5 years apart. The patient behaved as though he were completely blind in spite of demonstrating preserved central vision (he could read script slowly). In the original paper, there is no indication as to whether this patient acknowledged or denied his residual visual ability. In 1899, Gaupp described a patient with a history of partial cortical blindness who later complained of complete blindness and amnesia following a neurologic event subsequent to running over an elderly woman with a carriage. A careful examination of this patient by Forster revealed a small intact visual field. His vision slowly returned. This patient’s apparent hysteria renders it impossible to determine whether the denial of vision noted in this case clearly represents inverse Anton’s syndrome. Finally, Redlich and Bonvicini (1908) described a patient originally reported by Laqueur (1898) who was cortically blind with secondary
DENIAL
OF VISUAL
PERCEPTION
31
depression. He behaved much like a blind person, requiring assistance to move about. This patient was noted to be surprised when color vision and some degree of visual acuity in the central portion of the visual field were demonstrated. It is not clear whether this represented a sudden awareness of existing but previously denied visual ability or a recovery of visual function over time. We report a patient who had been diagnosed as cortically blind 2 years prior to the present evaluation. He maintained that he was completely unable to see. Upon careful examination, this patient evidenced a small preserved visual field and remarkably preserved visual abilities. In spite of demonstrated visual ability, he continued to deny awareness of visual percepts. This denial demonstrated by our patient represents a clinical presentation of “inverse Anton’s syndrome.” The findings are discussed with reference to related visual disturbances and with regard to the proposition that conscious identification of a percept may not be necessary for semantic activation. CASE REPORT The patient, a 56-year-old right-handed college educated male, reported that 2 years prior he had been “sitting, eating breakfast . . . looked up and everything went black.” The diagnosis was blindness due to bilateral cerebral infarction. The patient stated that he had regained no visual ability since the incident. After the initial hospitalization he was largely independent in living skills, typing grocery lists, cooking his own meals, and taking care of his own affairs with the assistance of a housekeeper. He was able to ambulate in unfamiliar surroundings without assistance. His interests included the buying and selling of horses. When asked how he judged these horses, he stated “by their sound and their feel.” He stated that independent living was very important to him. Only shortly prior to assessment, at the insistence of a friend, had he made contact with the Society for the Blind. He had attended meetings but never had applied for services. In addition, although he was a patient within the Veterans Administration Health Care System, he never attempted to gain benefits or services for impaired vision. In fact, he repeatedly downplayed his complaint of lack of sight, stating that he could compensate for it by “feel,” such as the method by which he judged horses. Medical history was positive for a stroke resulting in speech impairment approximately 1.5 years prior to the present assessment. The patient stated that he fully recovered with “teaching” (speech therapy). He was referred for evaluation at this time in response to a recent sudden onset of “confusion” and left-sided weakness.
32 Neurological
HARTMANN
ET AL.
Examination
Upon examination, 2 weeks later, the patient was alert, attentive, and cooperative. He was sufficiently attentive that during assessment sessions lasting an hour or more, he rarely, if ever, needed to be redirected to a task or activity. This included 20- to 30-min sessions of tachistoscopic reading. He was oriented to person, place, situation, and in a general sense to time. There was no evidence of confusion. The patient had normal pupillary responses and ocular motility. He demonstrated left-sided weakness and sensory loss, as well as moderate left-sided hypokinesis. A Babinski was also present on the left side. Except for vision, the remainder of the noncognitive aspects of the neurological examination was normal.
Neuropsychological
Examination
Cognitively, the patient demonstrated decreased digit span and slightly decreased short-term memory. He remembered one of three objects at 5 min, but when given the date and day was able to remember it during the testing session and when examined the next day. He clearly recognized and distinguished each of his examiners (three males and one female) without difficulty. This recognition was assessed and appeared to be accurate utilizing either voice or facial characteristics. On oral language examination, he had a mild anemic aphasia. His speech was fluent with occasional semantic paraphasic errors. For conversational speech, he had no difficulty communicating. Repetition ability was intact, and auditory-verbal comprehension was normal for conversational speech. However, comprehension was mildly impaired at the level of complex syntactic commands. Visual naming of common objects was 50% accurate with semantic errors and occasional circumlocutions. Cross model naming between smell (matches, tobacco, soap) and vision was similar. Tactile discrimination of complex stimuli (double simultaneous stimulation) was impaired bilaterally, being more impaired on the left than on the right. The patient was unable to name objects utilizing only tactile processing. However, his naming of an object to its description was correct on 8 of 10 trials. Importantly, the patient showed a striking correlation between his responses and the circumstances of stimulation. For example, for reading assessment, in addition to untimed reading (see below) the patient was tested with tachistoscopic reading. On this task he was asked to fixate on a large red circle prior to each exposure. At exposures greater than 700 msec he had a consistent accuracy rate of 20 to 25% for a standard set of stimuli. This accuracy rate declined in a steady fashion at lOO-msec intervals until 300 msec at which his accuracy dropped below 10%.
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1. Visual field plots revealing the area of spared vision in the upper right quadrant.
Visual Examination
A striking observation was what appeared to be occasional visual fixation, inconsistent with the patient’s diagnosis of complete cortical blindness and self-report of an inability to see. Residual visual ability was confirmed when testing for optokinetic nystagmus. The patient responded by stating that the test stimulus (a cloth) was moving. It was soon ascertained that he was able to make such identifications by sight. However, when asked how he made them, he denied visual perception and alternatively replied “I feel it, ” “I feel like something is there,” “it clicks,” or “I feel it in my mind.” Over a series of testing sessions lasting almost 2 months, there was an interesting evolution in his responses to these same questions. After 2 or 3 weeks when asked how he was able to read (especially during the tachistoscopic assessment), he began to reply that he didn’t know but that “you (the examiners) told me that I can see it, so I must be able to see it.” However 1 to 2 weeks later, after being told by his primary physicians and the ophthalmologists that he was blind, he reverted to his previous explanations for his ability to appreciate the stimuli. To confrontation testing of the visual fields using a finger counting task, the patient exhibited preserved vision in a wedge-shaped area approximately 30 degrees in size in the right upper quadrant, respecting the vertical meridian and extending to the periphery (Fig. 1). More formal visual field mapping could not be accomplished due to the patient’s poor visual fixation. In this area of intact visual field, acuity, based on analysis of reading ability, was 20/50 or better for both close and distant gaze. Similar to other tasks, this assessment was repeated on multiple occasions and the results were consistent. Visual language (reading) abilities. Several discrete visual tasks were employed to more thoroughly evaluate the patient’s residual visual perceptual and processing abilities. Assessment of written language processing was emphasized to enable simultaneous evaluation of visual perception and language function which was hypothesized to be impaired given his previous left hemisphere stroke. Among the areas evaluated was oral reading, for which the patient was administered portions of the Battery of Linguistic Analysis for Writing and Reading (BLAWR; Roeltgen, Cor-
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dell, & Sevush, 1984). Overall, the patient was correct in reading 118 of 230 (51%) real words varying in class, imageability, regularity, and length. The majority (47%) of his reading errors were visual errors (e.g., “smile” for “while”) as is frequently noted in patients with visual field impairment. In addition, the latter portion of the target word was retained with the errors occurring in the initial portion of the word (e.g., “community” for “opportunity,” and “confidence” for “evidence”), consistent with his mild left hemispatial neglect. When exposure to stimulus words was limited via tachistoscopic presentation, the patient would occasionally state that the words disappeared from his mind or that he could no longer “feel” them although they were still being presented. At other times, he stated that the stimulus word persisted after it had been withdrawn. Visual versus nonvisual object naming. The patient was able to name 5 of the first 10 objects from the Western Aphasia Battery presented visually. He produced infrequent semantic paraphasias in object naming. Performance did not improve by moving the stimulus object within the intact visual field. As mentioned previously, he was unable to name objects via tactile information alone. It is therefore clear that he utilizes, and in fact relies upon, visual ability in object identification. Facial recognition. The patient was able to recognize and accurately describe five of five pictorially depicted facial emotions. He was also able to identify famous faces, although he gave frequent anemic responses (e.g. “a well-known Republican from Arizona” for Barry Goldwater). He also made one semantic error, referring to John F. Kennedy as “Jimmy Carter.” Color Naming. A modified version of the Stroop Task was administered to assess color naming ability. This task consisted of presenting slides of individual color names illustrated in incongruous colors and requiring the subject to make an overt identification of the color. The task is typicaily employed as a measure of perceptual interference. With no time constraints and frequent redirecting by the examiner to aid the patient in overcoming the printed word interference, the patient was able to accurately name the color on 12 of 20 trials. Qualitatively, he maintained that he could “feel” or “hear” the color and his initial responses were consistent with such perceptions. For example, to the color orange he responded “like sky . . . like sunset,” and to green he stated “I feel something clear.” These responses indicated impairment at the level of color naming, as opposed to a perceptual deficit. It is interesting to note that the patient was unable to effectively discriminate whether a room was dark or illuminated, responding at chance levels. Anatomy
CT scan revealed three well-defined lesions (Fig. 2). One involved the lower portion of the right occipital lobe, extending up through the cal-
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a 2a. Plot of computerized tomography revealing an extensive lesion of the left inferior parietal lobule and lateral occipital gyrus, also involving the left medial superior occipital region. A second lesion involved the right calcarine region and occipital temporal gyri. A lesion involving the right superior perisylvian region was also present. Darkened area indicates well-defined low density. Stippled area indicates ill-defined low density. (Left side of figure indicates left side of brain.) (Plot angle and level of cuts do not correspond to the angle and level of cuts on the actual CT scan, see Fig. 2b). FIG.
carine fissure. The second lesion involved the left parietal-occipital region, including a small portion of the superior parietal lobule, the angular gyrus, the superior marginal gyrus, and other aspects of the medial and lateral occipital lobe. It ended approximately at the level of the calcarine fissure, sparing the medial-temporal and temporal-occipital areas. This lesion was perhaps continuous with additional ill-defined lucency in the posterior temporal region on the left. The third discrete lesion, apparently related to the most recent stroke, involved the right frontal and parietal opercula. DISCUSSION
Denial of cortical blindness (Anton’s syndrome) has been reported (Anton, 1898, 1899). Reference has also been made to the phenomenon of denial of visual perception, termed “inverse Anton’s syndrome” (Walsh & Hoyt, 1969). We are, however, not aware of reports describing patients with clearly documented preserved vision, particularly to the extent displayed by this patient, who were unaware of their visual abilities. While
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FIG. 2b. Representative cuts from the CT scan.
denial of vision has been suggested in previous case studies, confounds such as lack of notation regarding the patient’s awareness of his vision (Forster, 1890; Laqueur, 1898) and apparent patient hysteria (Gaupp, 1899) have obscured the possible diagnosis of this clinical syndrome. Our patient was neither disoriented nor hysterical, yet he maintained being totally unaware of his well-documented visual skills. Also, there was no evidence of any secondary gain. In contrast to seeking secondary gain, this patient had avoided support of any kind for his blindness. We believe this case clearly represents a clinical presentation of inverse Anton’s syndrome. This syndrome may share features with related disorders, namely, “blindsight” and visual agnosia (including prosopagnosia), as discussed below.
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Relation to Blindsight A syndrome referred to as “blindsight” has been described in which patients demonstrate primitive visual skills, such as light detection and orientation to a target within a perimetrically blind visual field (Poppel, Held, & Frost, 1973; Weiskrantz, Warrington, Sanders, & Marshall, 1974; Perenin & Jeannerod, 1975, 1978). These patients are unable to make conscious identification of more complex visual stimuli in the “blind” visual field. This phenomenon has been noted in patients with ablations of the geniculostriate, or primary visual pathway. The preserved visual ability is thought to be due to a second, noncalcarine visual system (colliculus-pulvinar-parietal lobe pathway), and is said to function in the detection of events, spatial localization, and the control of orienting responses to visual events (Zihl & Von Cramon, 1979). Like our patient, some patients demonstrating blindsight state that they “feel” objects appearing within the blind visual field, indicating a loss of the subjective experience of visual sensation in the “blind” region (Poppel et al., 1973). In contrast to blindsight, our patient’s visual abilities were examined within an intact portion of the visual field. His visual processing likely incorporated utilization of the primary visual pathway. CT did depict a normal area corresponding to the inferior striate cortex consistent with the preserved visual field. Furthermore his residual visual ability was superior to that indicated from blindsight. The patient was able to correctly identify numerous types of visual information presented within the small intact visual field. Disruption of the “Second” Visual Pathway It is possible that the patient’s lack of awareness of visual perception could be due to a deficit in orienting to visual stimuli. As visual orienting is believed to be a function of the “second” visual pathway, one may propose that this colliculus-pulvinar-parietal lobe pathway had been functionally ablated. The fact that he was unable to discriminate light from dark is consistent with this hypothesis, as this ability is also considered a function of the second visual system. While (by CT analysis) this anatomical pathway was possibly ablated in the left hemisphere in this patient, it was apparently intact on the right. This suggests that either the pathway must be intact in both hemispheres for adequate orienting function to occur or other lesions remote from this pathway may produce a deficit in orienting to visual stimuli. The latter hypothesis is more plausible, as many patients are seen with unilateral lesions of this system without demonstrating denial of vision. Alternatively, the described deficit may be due to impaired attentional or registration mechanisms, as opposed to visual orienting mechanisms. This patient fulfills neither the criteria for blindsight nor disruption of
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the second visual pathway. More accurately, his impairment appears related to the fact that the identification of the visual stimuli was not a conscious process for this individual. While able to attribute meaning to the visual information, as evidenced by the reading and naming of visually presented material, he maintained that he was not aware of any visual sensation. It is suggested that the patient’s visual perception is disconnected from the awareness of the visual construct. Relation
to Prosopagnosia
At one level, perception without awareness has been demonstrated in a distinct clinical population. Patients with prosopagnosia, a specific form of visual agnosia, have perception but no conscious awareness of meaning. Some of these patients have been found, via physiological indices (e.g., galvanic skin resistance), to have at least some recognition of faces that they state they do not recognize (Bauer, 1984; Tranel & Damasio, 1985). This was accomplished via an adaptation of the “guilty knowledge test” (Lykken, 1960), whereby electrodermal responses were compared with verbal naming responses using familiar and unfamiliar faces as stimuli. These patients evidenced recognition of familiar faces through increased electrodermal responding, although their overt naming was severely compromised. This suggests that some patients with prosopagnosia activate some semantic representations of these faces in memory, but remain unable to make overt identifications of these faces. Similarly, our patient demonstrated the ability to access and utilize visual information. However, he was unaware that the input modality was in fact visual. Clearly, this deficit was not in recognition, as he was able to make appropriate responses to visual information, thus distinguishing his presentation from visual agnosia. By definition, visual agnosia represents a failure of recognition whereby a normal percept is stripped of its meaning (Teuber, 1968). Using parallel terminology, our patient may be said to acquire meaning stripped of its percept. Attentional
versus Semantic Disconnection
A possible explanation for the discrepancy between the demonstrated preserved visual ability in our patient and his denial of such ability includes the involvement of attentional mechanisms. Although sufficient quantity and quality of visual information were available to register and interact with linguistic and semantic systems (for reading and naming), important cerebral interactions of some other type were lacking. This may be similar to the demonstration of semantic activation via tachistoscopic presentation of stimuli. It has been suggested that under such a condition, a semantic activator bypasses attentional systems and is processed at the semantic level. Anatomic correlates of attentional and semantic processing mechanisms are, in general, poorly defined. However, the inferior parietal
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lobule is known to be an important mechanism in attention (Lynch, Mountcastle, Talbot, & Yin, 1977; Mountcastle, 1978). Some of the most severe forms of hemispatial neglect occur from inferior parietal lobule lesions, more commonly from right hemispheric lesions, but also from left hemispheric lesions. The CT scan of our patient indicates the presence of a lesion involving the majority of the left inferior parietal lobule. In addition, the extension of a second right hemispheric posterior lesion was such that it may have functionally disconnected the right occipital lobe from the relatively intact right inferior parietal lobule. Thus, the limited visual information from the left inferior occipital lobe may not have been able to gain access to the right parietal lobe. This may have prevented the visual information from accessing the attentional systems. McGlynn and Schacter (1989) have suggested that awareness of impairment may be secondary to either a disruption of a posterior conscious awareness system or a disruption of an anterior executive system. They alternatively suggest that lack of awareness might occur secondary to inadequately activated information being transmitted to the conscious awareness system. Our patient’s frontal lobes were largely intact. Therefore, a disturbance of the anterior executive system is unlikely. However, our patient’s deficits and lesions are compatible with the contention that awareness for vision was disrupted because of a disturbance of the conscious awareness system, a disconnection of the visual information from the conscious awareness system, or both. In contrast, this same visual information did reach the patient’s memory systems, as he was able to report familiarity with visual items that were presented to him on previous occasions. In this respect, it is possible that our patient differs from those with prosopagnosia in that his visual perception is disconnected from attentional and awareness systems rather than from memory systems. REFERENCES Anton, G. 1898. Uber Herderkrankungen des Gehirnes, welche vom Patienten selbst nicht wahrgenommen werden. Wiener Klinische Wochenschriff. 11, 227-229. Anton, G. 1899. Uber die Selbstwahrnehmung der Herderkrankungen des Gehirns durch den Kranken bei Rindenbhndheit und Rindentaubheit. Archiv fur Psychiatric und Nervenkrankheiten, 32, 86-127. Bauer, R. M. 1984. Autonomic recognition of names and faces in prosopagnosia: A neuropsychological application of the guilty knowledge test. Neuropsychologia, 28, 457470. Forster, 0. 1980. Ueber Rindenblindheit. Albrecht von Gruefes Archiv fur Ophthalmologic, 36, 94-108. Gaupp, R. 1899. Uber corticaie Blindheit. Monatsschriff fur Psychiatric und Neurologie, 5, 28-41. Gloning, I., Gloning, K., & Tschabitscher, H. 1962. Die occipitale Blindheit und vascularer Basis: Untersuchungsergebnisse von 16 eigenen Fallen. Albrecht von Graefe’s Archiv fur Ophthalmologic vereinigt mit Archiv fur Augenheilkunde, 165, 138-177. Laqueur, L. 1898. Ein Fall von doppelseitiger homonymer Hemianopsie mit Erhaltung eines
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