Visual hypoemotionality and prosopagnosia associated with right temporal lobe isolation

Visual hypoemotionality and prosopagnosia associated with right temporal lobe isolation


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Vol. 24, No. 4, PP 57?-582. Bntan.

0028-3932:X6 $3.00+0.00 Pergamon Journals Ltd.




of Neuropsychology,

Clinic of Neurology, (Accepted

4 January






Abstract-Emotional hyporeactivity to visual stimuli (so-called visual hypoemotionality) was observed in a 71-yr-old woman following a cerebral infarction in the territory of the posterior cerebra1 arteries. Other visual disturbances included severe prosopagnosia, dense left hemianopia and mild left hemineglect. There was neither object agnosia nor any invoivement of language, memory or intellectual functions. Hypoemotionality was found only for visual stimuli, since auditory and tactile modalities were totally spared, suggesting a visualLlimbic disconnection mechanism. From CT data, and referring to previous evidence suggesting a right-hemisphere prevalence for emotional functions, it is postulated that the right occipital lesion, leading to a total right temporal lobe isolation, was mainly responsible for the patient’s emotional disturbances.

INTRODUCTION VISUAL hypoemotionality

with prosopagnosia was reported by BAUER [2] temporo-occipital damage. A visual-limbic disconnection was proposed to syndrome and the question was raised as to the nature of the link existing emotional disorders. The present case deals with a similar association in an right-hemisphere lesion.

in a 38-yr-old man after bilateral account for the occurrence of this between prosopagnosia and these older woman with a predominantly

CASE REPORT A 71-yr-old, previously healthy, right-handed female experienced sudden onset vertigo and posterior cephalalgia along with intense palpitations. On admission, she was slightly confused and drowsy and began to complain of blurred vision. Visual field testing revealed a dense left hemianopia with no macular sparing (Fig. 1). Neurological examination was otherwise normal apart from diffusely brisk tendon reflexes. An EEG showed bilateral posterior slow waves. A CT scan was taken 15 days post-stroke and another one 1 yr later (Fig. 2); both showed: (1) a large right occipital-temporal hypodensity consistent with an infarct in the territory of the posterior cerebral artery, extending to the lateral ventricle, encompassing the usual territory of the angular gyrus artery 17, IS]; (2) a much smaller, predominantly subcortical, infarct involving the white matter of the left occipital lobe; (3) a mild global atrophy. Cardiovascular assessment disclosed signs of auricular fibrillation, suggesting cerebral embolism as the probable mechanism of stroke. The patient was first referred for neuropsychological assessment one month after stroke. She was a refined housewife, who had been living in Marseille for 30 yr. Her life had been mostly devoted to her children and grandchildren. She especially appreciated esthetics; she was fond of painting aquarelles and enjoyed taking care of the many flowers that grew in her garden. Since the date of stroke, she chiefly complained of trouble in recognizing faces and places and reported some reading difficulties.

Her main and most insistent complaint was an almost total inability to recognize faces of her relatives as well as to learn new unfamiliar faces. She was particularly upset at failing to recognize her grandchildren. However. she *Address France


to: Dr Habib.


dc Neurologie,






Cedcx 5.




FIG. 1. Visual fields demonstrating


dense left hemianopia




immediateiy recognized them when they spoke. Recognition of pictures of iamous peopie was very poor: French Presidents and previously well-known artists were not identified. Pope John-Paul II, although photographed in a suggestive posture, was not recognized unless the examiner drew her attention to some details as the cross or the calottc. Matching f~oni and lak~al views of the same fakes was normal. Facial expressions were imperfectly identified (loathing: “she doesn’t look very satisjied”; anger: “she doesn’r smile”). Visual evocation of faces was also very poorly performed. Other visuul testings Picture naming gave rise to some misidentifications; errors occurred on stimuli from an ‘ambiguous’category (i.e. displaying few differential cues among a given category, for instance Rowers, insects, etc.), but the category itself was always easily identified. Naming of real objects was unimpaired but she seemed incapable ofacknowledging her own objects as belonging to her: personal objects-her nightdress, her own coffee cup, or her towels-were not recognized as being hers. Once back home, she reported that everything looked unfamiliar to her. She also had difficulties distinguishing her different dresses from each other; in order to achieve this, she needed to look for cues such as design details or buttoning. Finally, among three written samples, she failed to recognize her own writing. Concerning spatial orientation, there was a profound impairment of topographical memory. Well-known buildings, either actual or on pictures, were not recognized. Likewise, since she faalled to learn new orientation cues, she had to use verbalizable landmarks in order to get her bearings. However, she easily drew the floor plan of her apartment as well as mapping out or evoking a familiar route. A left spatial neglect was shown on drawing of geometric figures and copy of the Rey-Osterreith figure, accounting for her reading difficulties. Colour perception (100 Hue Farnsworth&Munsell test), colour matching and naming, form perception of complex drawings (De Renzi-Poppelreuter test) were normal. Emotionul


As early as the first interview, the patient complained ofemotional changes which persisted to this day. These were reported as a lack ofemotive reaction elicited by visual stimuli that formerly aroused a powerful feeling ofwell-being or contentment: “I loved flowers so much bejiwe. Their charm doesn’t enter my mind unymore. Looking at the lundscape through me. Ererythiny

the window, I see the hills, the trees, the colours, hut all those thmqs cannot conoeq’ their beauty to looks ordinary, indejinite. Iftiel ind&wnt about it. What I lack isfeelmy”. Except for these

complaints, the patient did not seem to have any defect or disturbance in affective behaviour; she was perfectly aware of her deficit and on several occasions, tears came to her eyes when she evoked personal memories with emotional content. Thus, these features are consistent with a selective impairment of visually-evoked emotion. Accordingly, there was no involvement of the auditory modality: familiar voices, especially on phone were perfectly identified. Identification of famous people’s voices was performed better than the average of controls. Finally, she was asked to listen to tape-recordings of familiar scenes with emotional content (laughing and crying baby. fair and market

FIG. 2. CT scan: eight succesive, 5-mm thick slices taken parallel to the orbito-meatal plane, showing a right-hemisphere lucency consistent with an infarct in the territory of the right posterior cerebral artery (open arrows, 6 and 7). Note the extent of the hypodensity to the usual territory of the angular gyrus artery (closed arrows, 6,7 and 8) compromising the callosal outflow from the intact left visual region to the right temporal lobe. A much smaller hypodense area situated in the subcortical white matter of the left occipital lobe, probably involves the left inferior longitudinal fasciculus (4). Y \o



atmospheres. .):her expression and comments revealed quite normal-perhaps increased--emotional reactivity to these auditory stimuli. Moreover, she brought repeated evidence suggesting a compensatory behaviour: one year after the beginning of the illness, she reported that she used to ‘speak to herself in order to appreciate the esthetic content of the visual environment. She may even use the intact tactile channel to experience emotions: thus, she reported she got used to touching and stroking flowers to compensate for the visual enjoyment they normally provide. Language


Spontaneous speech, comprehension of spoken language, word finding, repetition, spontaneous and dictated writing, reading words and short sentences were strictly normal. Text reading was only impaired because of difficulties to go to the next line in relation to left hemianopia and visual neglect.

Intellectual functions, repeatedly tested, were found to be strictly normal, even beyond those of age-matched controls. Memory function, as assessed on Wechsler Memory Scale, was also better than controls: Memory Quotient = 130; visual score= 11 (controls average: 5.3); verbal score= 16 (controls average: 7.3).

DISCUSSION Emotional disturbances are well-documented consequences of right-hemisphere damage in man [4, 10, 13, 201. Other recent evidence also points to a right-hemisphere dominance for emotional function [9, 5, 221. These data, however, cannot account for the visual specificity of our patient’s emotional disorders, which strongly suggests a disconnection mechanism. Visual agnosia and emotional disorders occur in monkeys after removal of the temporal lobes [4] or removal of the temporal neocortex alone [l]. GESCHWIND [1 l] proposed to ascribe these symptoms to a disconnection between visual inputs and limbic structures. This view was confirmed by subsequent experiments in which partial isolation of the temporal lobe produced similar disturbances [14, 15, 161. In particular, these animals seemed to be unable to become emotionally aroused by visual stimuli: “. It was as though all emotional reactions were available to the animal but uisua[ cues could not elicit them” 1151. In man, a decrease in drive and affective reactions has been described after various temporal lobe lesions [21], sometimes as a part of a human Khiver-Bucy syndrome [ 19,231. But actually, emotional hyporeactivity specific to the visual modality has been reported in only one instance [2]; this young man, who was prosopagnosic just like our patient, similarly described a feeling of dullness in front of natural scenery. Interestingly however, he was mainly affected by a loss ofemotional reaction to erotic visual stimuli, while other modalities (auditory and tactile) remained effective. Bilateral temporo-occipital lesions in that case led the author to suggest a dual visualLlimbic disconnection, namely a disruption of the medial limbic-hippocampal circuit as a cause of prosopagnosia, and involvement of the basolateral limbic-amygdaloid connections resulting in hypoemotionality. A similar disconnection theory may apply to our case. First, our patient’s large right-hemisphere infarct was responsible for a total left hemianopia so that the left hemisphere was the only one to receive direct visual input. Moreover, the extent of the lesion to the paraventricular with matter, in the usual territory of the angular gyrus artery [7, 181, destroyed the callosal radiations-the so called forceps major and forceps minor [8]-preventing all commissural transfer of visual information from the left occipital lobe to the right temporal lobe. Thus, the righthemisphere infarction seemed to entail a complete isolation of the right temporal lobe from visual afference. On the other hand, the small left infarct, involving the deep white matter of the occipital lobe, was likely to damage the inferior longitudinal fasciculus, the main subcortical connection between visual cortex and limbic structures [8]. We could therefore explain our patient’s emotional changes by a bilateral visual&limbic disconnection. However, it is worthy of note that the right-hemisphere lesion was much larger than the left one, so that the disconnection was likely to occur in a rather asymmetrical way, the right hmbic structures being much more disconnected from visual information than the left ones. This could be related to the above-mentioned evidence pointing to a righthemisphere specialization for emotional functions; one may thus speculate that our patient’s right temporal lobe was crucial for emotional processes so that its isolation from visual input was determinant in generating a total suppression of emotional response to visual stimuli. Visual hypoemotionahty in this patient may be related to an unusually strong lateralization ofemotional functions, perhaps as a result ofher own cognitive style and the special interest she always displayed towards esthetically relevant sights. However, one cannot rule out definitely the possibility that bilateral lesions would be a necessary condition; the anterior commissure, probably intact in our patient, was a possible pathway through which visual information could reach the right temporal lobe [12]. The deep left occipital lesion, interrupting the inferior longitudinal fasciculus, may have deprived the anterior commissure from visual afferences. Features of visual agnosia in this patient are quite consistent with DAMASIO’Sanalysis of prosopagnosia [6] in that not only faces but also other items from ‘ambiguous’ categories were misrecognized, suggesting a defect in recognition of the contextual relation of the object to the subject. Prosopagnosia is also usually ascribed to a



disruption of \~suaI hmbic pathways 13. 41. It 1s highly probable that visual hypoemotionality both lie on sml~lar mechanisms, but the specific relation between them remams unclear. Further reactivity in documented cases of visual agnosla could help resolvmg this problem.

and prosopagn<~s~a studies ofemotlonal

A~kno~vlPdyemen~sThe author wishes to thank Mrs M. Balzamo who performed neuropsychological assessements. Dr G. Boudouresques who referred the patient and Drs M. Poncct and .I. R. Duhamel for helpful suggestions.

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