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Unilateral left prosopometamorphopsia: A neuropsychological case study
Neuropsychologia 47 (2009) 942–948
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Neuropsychologia journal homepage: www.elsevier.com/locate/neuropsychologia
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Unilateral left prosopometamorphopsia: A neuropsychological case study Luigi Trojano a,b,∗ , Massimiliano Conson a , Sara Salzano a , Valentino Manzo c , Dario Grossi a a
Neuropsychology Laboratory, Dept. of Psychology, Second University of Naples, Via Vivaldi 43, 81100 Caserta, Italy Salvatore Maugeri Foundation, Scientific Institute of Telese Terme, IRCCS, Italy c Dept. of Neurology, A.O.R.N. Cardarelli, Via Cardarelli 45, Naples, Italy b
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Article history: Received 16 September 2008 Received in revised form 24 November 2008 Accepted 12 December 2008 Available online 24 December 2008 Keywords: Prosopometamorphopsia Face processing Occipital lobe
a b s t r a c t We describe a patient who suddenly developed prosopometamorphopsia after a childbirth; she claimed that the left half of well-known and unfamiliar faces looked distorted. Brain MR was normal, whereas SPECT showed hypoperfusion of the left infero-lateral occipital cortex. No visual recognition defects for objects or faces were present. In three matching tasks with half-faces (Experiment 1), chimeric faces (Experiment 2), or chimeric objects (Experiment 3), the patient was impaired only when she matched pairs of chimeric faces differing in their left half; the same results were obtained after 1 year. This is the first behavioural demonstration of selective chronic metamorphopsia for the left side of faces, and provides new insights for models of face processing. © 2009 Elsevier Ltd. All rights reserved.
Metamorphopsia encompasses a wide spectrum of visual perceptual distortions (Critchley, 1953), such as alteration of perceived object size (micropsia and macropsia) or, rarely, altered perception of faces (prosopometamorphopsia; ffytche & Howard, 1999). Prosopometamorphopsia (PMO) can involve the whole face, as in the classical description by Bodamer (1947), but also only one side of face, usually after a right hemisphere damage (Brust & Behrens, 1977; Ebata, Ogawa, Tanaka, Mizuno, & Yoshida, 1991; Young, de Haan, Newcombe, & Hay, 1990; for a review see, Miwa & Kondo, 2007). For instance, Brust and Behrens (1977) observed a patient with a right posterior temporal damage who had episodes of visual illusions during which the right half of faces seemed to melt, “like clocks in a Dalì painting”. An example of stable unilateral face distortion (the right side of a face appearing smaller than the left) has been reported by Ebata et al. (1991) in a patient with a small haematoma in the right retrosplenial region. In such cases, visual distortion did not involve perception of objects other than faces, and tasks assessing apperceptive or associative face processing did not show relevant impairments. Unilateral PMO after a left hemisphere lesion has been described only in four patients who however also showed metamorphopsia for objects or body parts (Imai, Nohira, Miyata, Okabe, & Hamaguchi, 1995; patient M.Z., Nijboer, Ruis, van der Worp, & De Haan, 2008; Satoh, Suzuki, Miyamura, Katoh, & Kuzuhara, 1997; Shiga, Makino, Ueda, & Nakajima, 1996). For instance, patient M.Z. described by Nijboer et al. (2008) had a left
∗ Corresponding author at: Dept. of Psychology, Second University of Naples, Via Vivaldi 43, 81100 Caserta, Italy. Tel.: +39 0823 274774; fax: +39 0823 274774. E-mail address: [email protected] (L. Trojano). 0028-3932/$ – see front matter © 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2008.12.015
temporo-occipital lesion and unilateral contralesional metamorphopsia; however, in an object confrontation task, she reported that objects presented on her right side appeared distorted as well. From the above overview, it should appear that only right hemisphere lesions can determine selective unilateral PMO, consistent with the idea of a right specialization for face processing. However, the analysis of selective PMO has always been based upon patients’ subjective complaints, thus preventing any attempt to comprehend its mechanisms. Here we describe a neuropsychological study on a patient with selective unilateral PMO. Our aim was to explore the cognitive basis of this rare disorder and its implications for cognitive models of face processing.
1. Case report D.G., a 24-year-old right-handed (no familiar history of lefthandedness; score on Edinburgh Handedness Inventory = 90; Oldfield, 1971) housewife with 8 years of formal education, suddenly developed severe migraine, confusional state, and blurred vision, mainly in her right visual hemifield, after child delivery. Consciousness returned normal and migraine subsided in a few hours, but the visual disturbances persisted longer. Repeated EEG recordings showed theta-wave slowing over posterior regions of the left hemisphere. Pattern reversal and flash VEPs were within normal limits 6 months after the stoke. Repeated MR did not disclose pathological areas. Brain SPECT (performed 30 min after the injection of 740 MBq of Tc-99m HMPAO) showed reduced blood flow in the inferior and lateral cortex of the left occipital lobe (Fig. 1).
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Fig. 1. Axial (on the left) and left paramedian sagittal (on the right) brain SPECT scans showing reduced blood flow in the inferior and lateral cortex of the left occipital lobe (regional blood flow reduced by 25.8% with respect to contralateral cortex).
The patient came to our observation 6 months after the stroke. At that time she was alert and cooperative, had recovered most of her visuo-perceptual abilities and was autonomous in her daily activities. The patient did not show visual field defects on Goldmann perimetry, but she complained that the left half of people’s faces (the part on her right side) appeared “out of shape”. D.G. claimed that “the left eye looks elongated towards left ear, the nose appears to be bended towards left cheek and the mouth towards the chin” (Fig. 2), irrespectively of whether she looked at familiar or unknown people, or even at herself in a mirror. Nonetheless, she reported to be able to recognize relatives and famous people by face, and also to visualise familiar faces in her mind without distortions. A general neuropsychological assessment did not reveal intellectual or language disturbances; the patient could correctly describe a complex scene, draw figures, read and write (words and nonwords). A specific battery for visuospatial abilities (BVA, known in Italy as TERADIC; Angelini & Grossi, 1993) did not disclose impairments in visuospatial perceptual skills; in particular, patient’s performances on tasks tapping discrimination of line length, line orientation and angle size were within the normal range.
Assessment of face processing was performed by means of the Benton Face Recognition Task (Benton, De Hamsher, Varney, & Spreen, 1992) and by a face recognition task requiring the patient to identify black and white images of 56 famous faces. Five normal right-handed females, matched to D.G. for age (range 22–26) and education, were tested for obtaining reference values for recognition of famous faces; the patient’s performance was compared with that of the normal subjects according to Crawford and Garthwaite’s (2002) statistical method. Moreover, we assessed visual object recognition by a naming task (Laiacona, Barbarotto, Trivelli, & Capitani, 1993) and the Poppelreuter-Ghent’s Overlapping Figures Test (Della Sala, Laiacona, Trivelli, & Spinnler, 1995). D.G. achieved a normal score on the Benton Face Recognition Task (44/54; cut-off = 38) and did not differ from normal controls in recognizing famous faces (D.G. = 46, controls = 48, S.D. 2.6; t = −1.053, two-tailed p = 0.352). The patient performed within normal range on the object naming task (raw score = 78/80, cut-off score = 61) and on the Poppelreuter-Ghent’s Overlapping Figures Test (raw score = 71; normal range = 51.5–71). These data demonstrated that D.G. did not show overt prosopoagnosic defects or object recognition impairments. 2. Special neuropsychological assessment A special neuropsychological assessment was performed to investigate the patient’s abilities to process information from the two sides of faces and objects. To this scope, D.G. underwent three experiments, requiring to match pairs of half-faces (Experiment 1), of chimeric faces (Experiment 2), and of chimeric objects (Experiment 3). Five normal right-handed females, matched to D.G. for age (range 21–29) and education, were tested to obtain reference values for the experimental tests. Also in this case we compared the patient’s performance with that of the normal subjects according to Crawford and Garthwaite’s (2002) statistical method. 2.1. Experiment 1: matching of half-faces
Fig. 2. Patient’s drawing of a face to depict her own subjective complaint.
The first experiment was aimed at verifying whether the patient’s subjective defect in perceiving the left half of faces could be evidenced in a task where she had to identify left (or right) half-faces. To this purpose, we devised a half-face matching task, in which the patient was required to match a target face with half-faces (right or left) in free-viewing condition without time constraints. This procedure allowed to assess the patient independently
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Fig. 3. Examples of “different” pairs used in the Experiment 1 (matching of half-faces). The target face is in the upper row and the half-face (the left or the right side) in the lower row.
from visual perceptual hemifield, in an experimental paradigm as similar as possible to ecological setting (see also Young et al., 1990). 2.1.1. Materials and methods The patient was presented with 40 pairs of stimuli. The two stimuli in each pair, aligned one above the other on an A4 sheet, consisted in black and white pictures of faces portrayed in canonical perspective (Fig. 3). The target stimulus depicting a whole face was printed in the upper half of the sheet, while the half-face stimulus depicting a half-face (the left or the right-hand side) was printed in the lower half of the sheet. In 20 trials, half-faces were different from the target (“different” pairs; 10 left half-faces and 10 right half-faces), while in the remaining trials half-faces were identical to the target (“same” pairs). The 40 stimuli were presented one at a time in random order. The patient had to judge whether faces depicted in the two stimuli were the same or different.
2.1.2. Results and comment The patient scored 38/40 correct; her performance was errorless on “same” pairs, whereas the two errors in “different” trials were observed for one right half-face pair and one left half-face pair. D.G.’s performance did not significantly differ from that of the control group (mean = 39.4, S.D. = 0.8; t = −1,598, one-tail p = 0.37). These results demonstrated that in spite of the patient’s subjective complaint of distorted perception of the left side of face, her ability to process half-faces, either left or right halves, was spared. The lack of impairment on this task could suggest, consistent with
formal assessment of face processing, that basic perceptual processes were spared and that unilateral PMO cannot be considered as a symptom germane to prosopagnosia. Alternatively, one could hypothesise that processing an half-face did not put in motion the same specialized cognitive mechanisms as processing whole faces, and that the task can be solved by resorting to non-specific visual feature analysis. Such non-specific processes had been demonstrated to be spared in D.G. thanks to her flawless performance on object processing, as well as on naming, reading and drawing tasks. To disentangle these two possibilities we performed a matching task on chimeric faces, in which the left and the right halves of different faces were assembled. If the patient had completely spared face perceptual processes, she should perform correctly on this second task too. Alternatively, an impairment in this task would favour the hypothesis that our patient’s subjective defect in perceiving the left half of face was related to a specific cognitive impairment, that would reveal itself when information from the two halves of a face stimulus have to be integrated. 2.2. Experiment 2: matching of chimeric faces To verify whether the patient was impaired in integrating features from the two halves of face we adopted a chimeric face recognition paradigm (Butler et al., 2005; Levy, Heller, Banich, &
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Fig. 4. Examples of “different” pairs used in the Experiment 2 (matching of chimeric faces). The target face is in the upper row and the chimeric face (the difference is in the left or the right side) in the lower row.
Burton, 1983; Young et al., 1990). Such a paradigm has been used to verify whether normal subjects are biased towards one side of face when required to recognize it; in the present context, the paradigm tapped our patient’s ability to recognize faces taking into account either the right or the left side of faces. 2.2.1. Materials and methods The patient was presented with 30 pairs of stimuli. As in the previous experiment, the two stimuli in the pair, aligned one above the other on an A4 sheet, consisted in black and white face pictures portrayed in canonical perspective. The target face was printed in the upper half of the sheet, while the chimeric face was printed in the lower half of the sheet. Ten chimeric faces were obtained assembling a right half-face identical to the target presented in the upper half of the sheet, and a left half-face from a different picture, while in other 10 chimeric faces the left half was identical to the target and the right was different (Fig. 4). Therefore, these two sets of pairs were composed by a chimeric face different from the target (“different” pairs), but the difference was in left or in the right part of the chimeric stimulus, respectively. In the remaining 10 chimeric stimuli both halves were from the same picture as the target (“same” pairs).
The 30 stimuli were presented one at a time in random order. The patient was required to judge whether the two faces of each pair were the same face or different. As above, no time constraint was imposed and the patient was free of moving her head and eyes.
2.2.2. Results and comment The patient scored 22/30 correct. Her performance was errorless (10/10) on “same” pairs and on “different” pairs in which the chimeric face differed in the right side from the target face. On the contrary, the patient scored 2/10 in “different” trials where the left side of the chimeric face differed from the target. Differences in the distribution of errors for the three kinds of stimuli were significant (chi-square = 21.8, d.f. = 2, p = .0001). Moreover, D.G.’s score was significantly lower than that of the control subjects (mean = 29, S.D. = 0.9; t = −7.100, one-tail p = 0.004). The patient’s failure in “different” trials where the left side of the chimeric face differed from the target suggested that D.G.’s perceptual processing of faces was not spared, and that a specif-
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Fig. 5. Examples of “different” pairs used in the Experiment 3 (matching of chimeric objects). The target car is in the upper row and the chimeric car (the difference is in the left or the right side) in the lower row.
ically devised task in which either half of a face had to be processed could reveal her selective cognitive impairment. However, it could be hypothesised that the patient was affected by a subtle perceptual defect in visual processing, interfering with integration of complex stimuli. As standard face processing tasks could not reveal the patient’s basic impairment in processing face stimuli, so standard object perceptual tasks might be ineffective in detecting a subtle “hemi-impairment” in visual processing. To verify this possibility we devised a task requiring matching of chimeric complex objects.
form a follow-up study. At that time, D.G. still referred distorted face perception. Neuropsychological assessment based on the same three experiments of the first examination revealed an unchanged pattern of performance (matching of half-faces: correct responses 39/40; matching of chimeric faces: 21/30, errors were in “different” trials where the left side of the chimeric face differed from the target; matching of chimeric objects: 30/30). These results replicated previous data, thus further strengthening the observation that unilateral PMO for the left side of face was based on a specific cognitive impairment in our patient.
2.3. Experiment 3: matching of chimeric objects To verify whether our patient’s impairment was specific for facial stimuli we devised a further experiment in which the patient had to recognize non-facial chimeric stimuli; for this purpose we choose car-fronts, that have been shown to be affected by the same deformation as faces in the PMO patient described by Seron et al. (1995), and that have been considered as another kind of stimulus class, demanding within-category discrimination between visually similar items (Young et al., 1990). 2.3.1. Materials and methods Procedures and number of stimuli were the same as in the discrimination of chimeric faces, but in this experiment stimuli were composed by black and white line drawings depicting cars seen from the front (Fig. 5).
2.3.2. Results and comment The patient scored 29/30 correct. Her performance was errorless on “same” pairs. The only mistake was made on one “different” pair in which the target and the chimeric object differed for their right half. D.G.’s performance did not significantly differ from that of the control group (mean = 29.6, S.D. = 0.5; t = −1.095, one-tail p = 0.67). Consistent with data from the assessment of face and object processing and with the patient’s subjective reports, these results demonstrated that PMO was specifically related to a defect in perceptual processing of faces. 2.4. Follow-up About 2 weeks after the experimental investigation, the patient was discharged. One year after the first evaluation, we could per-
3. Discussion In the present paper we described a patient with subjective complaints of PMO for the left half of faces. At variance with previous left brain-damaged patients, D.G. did not report subjective distortions in perceiving stimuli other than faces, and showed a substantially unchanged pattern over 1 year, thus demonstrating that unilateral metamorphopsia can affect face perception specifically and chronically after a left hemisphere lesion. D.G. performed well on standard clinical tests tapping shape and size discrimination, and object and face perception (see Nijboer et al., 2008 for a careful description of a different pattern), whereas experimental testing procedures demonstrated a specific impairment only in one face processing task. Actually, the present patient performed as well as normal controls on tasks involving half-faces and chimeric objects, whereas she showed a significant impairment only in the chimeric face task. To explain these findings it could be hypothesized that the chimeric face task was more difficult than the chimeric object task, so that evidence from the third experimental task could not allow strong inferences about the specificity of our patient’s defect for face processing. However, several considerations suggest that task difficulty was not a viable explanation for our patient’s selective defect on the chimeric face task. First, we choose car-fronts for the chimeric object task on the basis of previous studies suggesting that such stimuli are the best control for face processing tasks (Young et al., 1990). Second, on a post hoc basis, we observed that normal controls’ performances did not significantly differ on the chimeric face and object tasks (paired t-test: t = −1.500, p = .208). Third, and more relevant here, the patient did not fail on
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the chimeric face task because of a general impairment with this class of stimuli, but for a significant asymmetry in processing the two halves of faces, a finding highly congruent with her subjective complaint. More sensitive assessment procedures (e.g., Gauthier, Behrmann, & Tarr, 1999) could have revealed subtle, not clinically relevant, visual defects in our patient, but the finding of higher error rate on the left side of chimeric face stimuli in free-viewing condition could be consistent with a face-specific spatial neglect in our patient. While typical neglect patients have been shown to fail in processing both face and non-face chimeric stimuli (Sarri, Kalra, Greenwood, & Driver, 2006; Young, Hellawell, & Welch, 1992), patient K.L. reported by Young et al. (1990) demonstrated a selective neglect in face processing. K.L. was affected by prosopagnosia and complained of unilateral right PMO (he referred that faces looked “different” or “deformed” and eyes were somehow misplaced). K.L. was impaired in processing the right-half of faces on different tasks, involving whole faces, chimeric faces, and half-faces presented in isolation; at variance, the patient was faultless in processing objects other than faces (e.g., car-fronts). K.L.’s impaired performance for the right side of facial stimuli was evident also when they were presented in the intact visual hemifield. On this basis, Young et al. (1990) suggested that K.L.’s clinical picture could be explained by a defect in lateralised face-specific attentional mechanisms, independent from visual field. The existence of such mechanisms has been also demonstrated by studies on chimeric face processing in normal subjects, who show a superiority in processing the right half of faces in free-viewing conditions but not in tachistoscopic presentation (Grega, Sackeim, Sanchez, Cohen, & Hough, 1988; Levy et al., 1983). According to Young et al. (1990), the attentional disorder in their patient would lead to a defect of “the mental representation” of one side of the faces (p. 412). Our patient’s subjective asymmetry in perceiving face stimuli was concomitant with a lateralized impairment in processing the left side of chimeric faces in free-viewing condition, as in patient K.L. assessed by Young et al. (1990) with the same procedure. However, the present patient D.G. showed defective performance on the opposite half of faces with respect to K.L. and, differently from K.L., she was not prosopagnosic and did not fail on the half-face task. Therefore, the hypothesis of a domain-specific form of unilateral neglect would require some specification to entirely account for the present clinical picture. If we posit that an analogous attentional system devoted to processing the contralateral side of faces is also present in the left hemisphere, our patient’s cognitive defect could be related to an impairment of such a system, that would render less effective the internal representation of the left side of faces (as suggested by Young et al., 1990; see also Levy, Trevarthen, & Sperry, 1972). However, functional consequences of this defect would be less severe than those observed after a right hemisphere lesion because of the lower specialization of the left hemisphere in face processing. In some sense, this defect would reveal itself only when integration of left- and right-sided information is required (and not with half-faces), as in a sort of extinction of left-sided face representation by right-sided ones. At variance, the analogous defect after a right hemispheric lesion would determine the more severe picture of facial neglect described by Young et al. (1990), likely associated to prosopagnosic disturbances. This interpretative hypothesis is admittedly based on several post hoc assumptions, and requires further independent evidence to be verified, but it would be consistent with available theoretical models of face processing. In terms of classical face recognition models, such that put forward by Bruce and Young (1986), the present putative defect of the attentional system would affect early stages of face processing, involved in extracting structural aspects of facial stimuli. The unilateral nature of the defect would suggest
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that early face processing stages are based on parallel mechanisms in the two hemispheres, although with different degrees of efficiency. Only after these early stages, specialized right hemispheric functions would take place. According to our hypothesis, a left occipital damage might only generate a contralesional defect in early stages of face processing, while a right occipital damage could give rise to either unilateral PMO for the right side of the face, or PMO disorders affecting the whole face, besides the classical impairments of face recognition. This interpretation follows the logic of the late convergence hypothesis for face-selective visual information; computational modelling of face processing would suggest that only at a late stage contralateral visual information gathered by the two hemispheres are integrated together, after some information extraction has been applied separately in each hemisphere (Hsiao, Shieh, & Cottrell, 2008). In the same vein, electrophysiological studies on face and word recognition demonstrated that an early ERP component is modulated by contralateral features of the stimulus (Smith, Gosselin, & Schyns, 2004). Our proposal is consistent with both neuropsychological and neurofunctional data demonstrating a right hemispheric lateralization for face processing (Ishai, 2008), but highlight that contralateral visual information are first separately processed by the two hemispheres and then integrated in the right hemisphere. In the light of anatomofunctional data supporting a hierarchical organization of face processing areas (Fairhall & Ishai, 2007; Haxby, Hoffman, & Gobbini, 2000), unilateral PMO after a left hemisphere lesion would suggest that face-responsive regions in occipital areas of each hemisphere are involved in building up internal representation of the contralateral side of face. Output from this stage would then be directed towards the fusiform face area of the right hemisphere where the integration of information from two sides of face takes place. In synthesis, we described a patient with chronic and selective subjective complaints of PMO for the left half of faces after a left hemisphere lesion. To explain this very unusual clinical picture, we speculated that early stages of face perception proceed in parallel in the two hemispheres and only at late stages the right hemisphere integrates information gathered from both parts of the stimulus to build up an unitary face representation. Replication of such findings and neurofunctional investigations on patients with PMO are warranted to directly verify neural dynamics related to unilateral defects in face processing. References Angelini, R., & Grossi, D. (1993). La terapia razionale dei disordini costruttivi. Roma: Centro di Riabilitazione S. Lucia. Benton, A. L., De Hamsher, K., Varney, N. R., & Spreen, O. (1992). Test di riconoscimento di volti ignoti. Firenze: Organizzazioni Speciali. Bodamer, J. (1947). Die Prosop-agnosie. Archiv für Psychiatrie und Nervenkrankheiten, 179, 6–53. Butler, S., Gilchrist, I. D., Burt, D. M., Perrett, D. I., Jones, E., & Harvey, M. (2005). Are the perceptual biases found in chimeric face processing reflected in eye-movement patterns? Neuropsychologia, 43, 52–59. Bruce, V., & Young, A. (1986). Understanding face recognition. British Journal of Psychology, 77, 305–327. Brust, J. C. M., & Behrens, M. M. (1977). “Release Hallucinations” as the major symptom of posterior cerebral artery occlusion: A report of 2 cases. Annals of Neurology, 2, 432–436. Critchley, M. (1953). The parietal lobes. New York: Hafner. Crawford, J. R., & Garthwaite, P. H. (2002). Investigation of the single case in neuropsychology: Confidence limits on the abnormality of test scores and test score differences. Neuropsychologia, 40, 1196–1208. Della Sala, S., Laiacona, M., Trivelli, C., & Spinnler, H. (1995). Poppelreuter-Ghent’s Overlappping Figures Test: Its sensitivity to age, and its clinical use. Archives of Clinical Neuropsychology, 6, 511–534. Ebata, S., Ogawa, M., Tanaka, Y., Mizuno, Y., & Yoshida, M. (1991). Apparent reduction in the size of one side of the face associated with a small retrosplenial hemorrhage. Journal of Neurology, Neurosurgery and Psychiatry, 54, 68–70. Fairhall, S. L., & Ishai, A. (2007). Effective connectivity within the distributed cortical network for face perception. Cerebral Cortex, 17, 2400–2406.
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Neuropsychologia journal homepage: www.elsevier.com/locate/neuropsychologia
Note
Unilateral left prosopometamorphopsia: A neuropsychological case study Luigi Trojano a,b,∗ , Massimiliano Conson a , Sara Salzano a , Valentino Manzo c , Dario Grossi a a
Neuropsychology Laboratory, Dept. of Psychology, Second University of Naples, Via Vivaldi 43, 81100 Caserta, Italy Salvatore Maugeri Foundation, Scientific Institute of Telese Terme, IRCCS, Italy c Dept. of Neurology, A.O.R.N. Cardarelli, Via Cardarelli 45, Naples, Italy b
a r t i c l e
i n f o
Article history: Received 16 September 2008 Received in revised form 24 November 2008 Accepted 12 December 2008 Available online 24 December 2008 Keywords: Prosopometamorphopsia Face processing Occipital lobe
a b s t r a c t We describe a patient who suddenly developed prosopometamorphopsia after a childbirth; she claimed that the left half of well-known and unfamiliar faces looked distorted. Brain MR was normal, whereas SPECT showed hypoperfusion of the left infero-lateral occipital cortex. No visual recognition defects for objects or faces were present. In three matching tasks with half-faces (Experiment 1), chimeric faces (Experiment 2), or chimeric objects (Experiment 3), the patient was impaired only when she matched pairs of chimeric faces differing in their left half; the same results were obtained after 1 year. This is the first behavioural demonstration of selective chronic metamorphopsia for the left side of faces, and provides new insights for models of face processing. © 2009 Elsevier Ltd. All rights reserved.
Metamorphopsia encompasses a wide spectrum of visual perceptual distortions (Critchley, 1953), such as alteration of perceived object size (micropsia and macropsia) or, rarely, altered perception of faces (prosopometamorphopsia; ffytche & Howard, 1999). Prosopometamorphopsia (PMO) can involve the whole face, as in the classical description by Bodamer (1947), but also only one side of face, usually after a right hemisphere damage (Brust & Behrens, 1977; Ebata, Ogawa, Tanaka, Mizuno, & Yoshida, 1991; Young, de Haan, Newcombe, & Hay, 1990; for a review see, Miwa & Kondo, 2007). For instance, Brust and Behrens (1977) observed a patient with a right posterior temporal damage who had episodes of visual illusions during which the right half of faces seemed to melt, “like clocks in a Dalì painting”. An example of stable unilateral face distortion (the right side of a face appearing smaller than the left) has been reported by Ebata et al. (1991) in a patient with a small haematoma in the right retrosplenial region. In such cases, visual distortion did not involve perception of objects other than faces, and tasks assessing apperceptive or associative face processing did not show relevant impairments. Unilateral PMO after a left hemisphere lesion has been described only in four patients who however also showed metamorphopsia for objects or body parts (Imai, Nohira, Miyata, Okabe, & Hamaguchi, 1995; patient M.Z., Nijboer, Ruis, van der Worp, & De Haan, 2008; Satoh, Suzuki, Miyamura, Katoh, & Kuzuhara, 1997; Shiga, Makino, Ueda, & Nakajima, 1996). For instance, patient M.Z. described by Nijboer et al. (2008) had a left
∗ Corresponding author at: Dept. of Psychology, Second University of Naples, Via Vivaldi 43, 81100 Caserta, Italy. Tel.: +39 0823 274774; fax: +39 0823 274774. E-mail address: [email protected] (L. Trojano). 0028-3932/$ – see front matter © 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2008.12.015
temporo-occipital lesion and unilateral contralesional metamorphopsia; however, in an object confrontation task, she reported that objects presented on her right side appeared distorted as well. From the above overview, it should appear that only right hemisphere lesions can determine selective unilateral PMO, consistent with the idea of a right specialization for face processing. However, the analysis of selective PMO has always been based upon patients’ subjective complaints, thus preventing any attempt to comprehend its mechanisms. Here we describe a neuropsychological study on a patient with selective unilateral PMO. Our aim was to explore the cognitive basis of this rare disorder and its implications for cognitive models of face processing.
1. Case report D.G., a 24-year-old right-handed (no familiar history of lefthandedness; score on Edinburgh Handedness Inventory = 90; Oldfield, 1971) housewife with 8 years of formal education, suddenly developed severe migraine, confusional state, and blurred vision, mainly in her right visual hemifield, after child delivery. Consciousness returned normal and migraine subsided in a few hours, but the visual disturbances persisted longer. Repeated EEG recordings showed theta-wave slowing over posterior regions of the left hemisphere. Pattern reversal and flash VEPs were within normal limits 6 months after the stoke. Repeated MR did not disclose pathological areas. Brain SPECT (performed 30 min after the injection of 740 MBq of Tc-99m HMPAO) showed reduced blood flow in the inferior and lateral cortex of the left occipital lobe (Fig. 1).
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Fig. 1. Axial (on the left) and left paramedian sagittal (on the right) brain SPECT scans showing reduced blood flow in the inferior and lateral cortex of the left occipital lobe (regional blood flow reduced by 25.8% with respect to contralateral cortex).
The patient came to our observation 6 months after the stroke. At that time she was alert and cooperative, had recovered most of her visuo-perceptual abilities and was autonomous in her daily activities. The patient did not show visual field defects on Goldmann perimetry, but she complained that the left half of people’s faces (the part on her right side) appeared “out of shape”. D.G. claimed that “the left eye looks elongated towards left ear, the nose appears to be bended towards left cheek and the mouth towards the chin” (Fig. 2), irrespectively of whether she looked at familiar or unknown people, or even at herself in a mirror. Nonetheless, she reported to be able to recognize relatives and famous people by face, and also to visualise familiar faces in her mind without distortions. A general neuropsychological assessment did not reveal intellectual or language disturbances; the patient could correctly describe a complex scene, draw figures, read and write (words and nonwords). A specific battery for visuospatial abilities (BVA, known in Italy as TERADIC; Angelini & Grossi, 1993) did not disclose impairments in visuospatial perceptual skills; in particular, patient’s performances on tasks tapping discrimination of line length, line orientation and angle size were within the normal range.
Assessment of face processing was performed by means of the Benton Face Recognition Task (Benton, De Hamsher, Varney, & Spreen, 1992) and by a face recognition task requiring the patient to identify black and white images of 56 famous faces. Five normal right-handed females, matched to D.G. for age (range 22–26) and education, were tested for obtaining reference values for recognition of famous faces; the patient’s performance was compared with that of the normal subjects according to Crawford and Garthwaite’s (2002) statistical method. Moreover, we assessed visual object recognition by a naming task (Laiacona, Barbarotto, Trivelli, & Capitani, 1993) and the Poppelreuter-Ghent’s Overlapping Figures Test (Della Sala, Laiacona, Trivelli, & Spinnler, 1995). D.G. achieved a normal score on the Benton Face Recognition Task (44/54; cut-off = 38) and did not differ from normal controls in recognizing famous faces (D.G. = 46, controls = 48, S.D. 2.6; t = −1.053, two-tailed p = 0.352). The patient performed within normal range on the object naming task (raw score = 78/80, cut-off score = 61) and on the Poppelreuter-Ghent’s Overlapping Figures Test (raw score = 71; normal range = 51.5–71). These data demonstrated that D.G. did not show overt prosopoagnosic defects or object recognition impairments. 2. Special neuropsychological assessment A special neuropsychological assessment was performed to investigate the patient’s abilities to process information from the two sides of faces and objects. To this scope, D.G. underwent three experiments, requiring to match pairs of half-faces (Experiment 1), of chimeric faces (Experiment 2), and of chimeric objects (Experiment 3). Five normal right-handed females, matched to D.G. for age (range 21–29) and education, were tested to obtain reference values for the experimental tests. Also in this case we compared the patient’s performance with that of the normal subjects according to Crawford and Garthwaite’s (2002) statistical method. 2.1. Experiment 1: matching of half-faces
Fig. 2. Patient’s drawing of a face to depict her own subjective complaint.
The first experiment was aimed at verifying whether the patient’s subjective defect in perceiving the left half of faces could be evidenced in a task where she had to identify left (or right) half-faces. To this purpose, we devised a half-face matching task, in which the patient was required to match a target face with half-faces (right or left) in free-viewing condition without time constraints. This procedure allowed to assess the patient independently
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Fig. 3. Examples of “different” pairs used in the Experiment 1 (matching of half-faces). The target face is in the upper row and the half-face (the left or the right side) in the lower row.
from visual perceptual hemifield, in an experimental paradigm as similar as possible to ecological setting (see also Young et al., 1990). 2.1.1. Materials and methods The patient was presented with 40 pairs of stimuli. The two stimuli in each pair, aligned one above the other on an A4 sheet, consisted in black and white pictures of faces portrayed in canonical perspective (Fig. 3). The target stimulus depicting a whole face was printed in the upper half of the sheet, while the half-face stimulus depicting a half-face (the left or the right-hand side) was printed in the lower half of the sheet. In 20 trials, half-faces were different from the target (“different” pairs; 10 left half-faces and 10 right half-faces), while in the remaining trials half-faces were identical to the target (“same” pairs). The 40 stimuli were presented one at a time in random order. The patient had to judge whether faces depicted in the two stimuli were the same or different.
2.1.2. Results and comment The patient scored 38/40 correct; her performance was errorless on “same” pairs, whereas the two errors in “different” trials were observed for one right half-face pair and one left half-face pair. D.G.’s performance did not significantly differ from that of the control group (mean = 39.4, S.D. = 0.8; t = −1,598, one-tail p = 0.37). These results demonstrated that in spite of the patient’s subjective complaint of distorted perception of the left side of face, her ability to process half-faces, either left or right halves, was spared. The lack of impairment on this task could suggest, consistent with
formal assessment of face processing, that basic perceptual processes were spared and that unilateral PMO cannot be considered as a symptom germane to prosopagnosia. Alternatively, one could hypothesise that processing an half-face did not put in motion the same specialized cognitive mechanisms as processing whole faces, and that the task can be solved by resorting to non-specific visual feature analysis. Such non-specific processes had been demonstrated to be spared in D.G. thanks to her flawless performance on object processing, as well as on naming, reading and drawing tasks. To disentangle these two possibilities we performed a matching task on chimeric faces, in which the left and the right halves of different faces were assembled. If the patient had completely spared face perceptual processes, she should perform correctly on this second task too. Alternatively, an impairment in this task would favour the hypothesis that our patient’s subjective defect in perceiving the left half of face was related to a specific cognitive impairment, that would reveal itself when information from the two halves of a face stimulus have to be integrated. 2.2. Experiment 2: matching of chimeric faces To verify whether the patient was impaired in integrating features from the two halves of face we adopted a chimeric face recognition paradigm (Butler et al., 2005; Levy, Heller, Banich, &
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Fig. 4. Examples of “different” pairs used in the Experiment 2 (matching of chimeric faces). The target face is in the upper row and the chimeric face (the difference is in the left or the right side) in the lower row.
Burton, 1983; Young et al., 1990). Such a paradigm has been used to verify whether normal subjects are biased towards one side of face when required to recognize it; in the present context, the paradigm tapped our patient’s ability to recognize faces taking into account either the right or the left side of faces. 2.2.1. Materials and methods The patient was presented with 30 pairs of stimuli. As in the previous experiment, the two stimuli in the pair, aligned one above the other on an A4 sheet, consisted in black and white face pictures portrayed in canonical perspective. The target face was printed in the upper half of the sheet, while the chimeric face was printed in the lower half of the sheet. Ten chimeric faces were obtained assembling a right half-face identical to the target presented in the upper half of the sheet, and a left half-face from a different picture, while in other 10 chimeric faces the left half was identical to the target and the right was different (Fig. 4). Therefore, these two sets of pairs were composed by a chimeric face different from the target (“different” pairs), but the difference was in left or in the right part of the chimeric stimulus, respectively. In the remaining 10 chimeric stimuli both halves were from the same picture as the target (“same” pairs).
The 30 stimuli were presented one at a time in random order. The patient was required to judge whether the two faces of each pair were the same face or different. As above, no time constraint was imposed and the patient was free of moving her head and eyes.
2.2.2. Results and comment The patient scored 22/30 correct. Her performance was errorless (10/10) on “same” pairs and on “different” pairs in which the chimeric face differed in the right side from the target face. On the contrary, the patient scored 2/10 in “different” trials where the left side of the chimeric face differed from the target. Differences in the distribution of errors for the three kinds of stimuli were significant (chi-square = 21.8, d.f. = 2, p = .0001). Moreover, D.G.’s score was significantly lower than that of the control subjects (mean = 29, S.D. = 0.9; t = −7.100, one-tail p = 0.004). The patient’s failure in “different” trials where the left side of the chimeric face differed from the target suggested that D.G.’s perceptual processing of faces was not spared, and that a specif-
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Fig. 5. Examples of “different” pairs used in the Experiment 3 (matching of chimeric objects). The target car is in the upper row and the chimeric car (the difference is in the left or the right side) in the lower row.
ically devised task in which either half of a face had to be processed could reveal her selective cognitive impairment. However, it could be hypothesised that the patient was affected by a subtle perceptual defect in visual processing, interfering with integration of complex stimuli. As standard face processing tasks could not reveal the patient’s basic impairment in processing face stimuli, so standard object perceptual tasks might be ineffective in detecting a subtle “hemi-impairment” in visual processing. To verify this possibility we devised a task requiring matching of chimeric complex objects.
form a follow-up study. At that time, D.G. still referred distorted face perception. Neuropsychological assessment based on the same three experiments of the first examination revealed an unchanged pattern of performance (matching of half-faces: correct responses 39/40; matching of chimeric faces: 21/30, errors were in “different” trials where the left side of the chimeric face differed from the target; matching of chimeric objects: 30/30). These results replicated previous data, thus further strengthening the observation that unilateral PMO for the left side of face was based on a specific cognitive impairment in our patient.
2.3. Experiment 3: matching of chimeric objects To verify whether our patient’s impairment was specific for facial stimuli we devised a further experiment in which the patient had to recognize non-facial chimeric stimuli; for this purpose we choose car-fronts, that have been shown to be affected by the same deformation as faces in the PMO patient described by Seron et al. (1995), and that have been considered as another kind of stimulus class, demanding within-category discrimination between visually similar items (Young et al., 1990). 2.3.1. Materials and methods Procedures and number of stimuli were the same as in the discrimination of chimeric faces, but in this experiment stimuli were composed by black and white line drawings depicting cars seen from the front (Fig. 5).
2.3.2. Results and comment The patient scored 29/30 correct. Her performance was errorless on “same” pairs. The only mistake was made on one “different” pair in which the target and the chimeric object differed for their right half. D.G.’s performance did not significantly differ from that of the control group (mean = 29.6, S.D. = 0.5; t = −1.095, one-tail p = 0.67). Consistent with data from the assessment of face and object processing and with the patient’s subjective reports, these results demonstrated that PMO was specifically related to a defect in perceptual processing of faces. 2.4. Follow-up About 2 weeks after the experimental investigation, the patient was discharged. One year after the first evaluation, we could per-
3. Discussion In the present paper we described a patient with subjective complaints of PMO for the left half of faces. At variance with previous left brain-damaged patients, D.G. did not report subjective distortions in perceiving stimuli other than faces, and showed a substantially unchanged pattern over 1 year, thus demonstrating that unilateral metamorphopsia can affect face perception specifically and chronically after a left hemisphere lesion. D.G. performed well on standard clinical tests tapping shape and size discrimination, and object and face perception (see Nijboer et al., 2008 for a careful description of a different pattern), whereas experimental testing procedures demonstrated a specific impairment only in one face processing task. Actually, the present patient performed as well as normal controls on tasks involving half-faces and chimeric objects, whereas she showed a significant impairment only in the chimeric face task. To explain these findings it could be hypothesized that the chimeric face task was more difficult than the chimeric object task, so that evidence from the third experimental task could not allow strong inferences about the specificity of our patient’s defect for face processing. However, several considerations suggest that task difficulty was not a viable explanation for our patient’s selective defect on the chimeric face task. First, we choose car-fronts for the chimeric object task on the basis of previous studies suggesting that such stimuli are the best control for face processing tasks (Young et al., 1990). Second, on a post hoc basis, we observed that normal controls’ performances did not significantly differ on the chimeric face and object tasks (paired t-test: t = −1.500, p = .208). Third, and more relevant here, the patient did not fail on
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the chimeric face task because of a general impairment with this class of stimuli, but for a significant asymmetry in processing the two halves of faces, a finding highly congruent with her subjective complaint. More sensitive assessment procedures (e.g., Gauthier, Behrmann, & Tarr, 1999) could have revealed subtle, not clinically relevant, visual defects in our patient, but the finding of higher error rate on the left side of chimeric face stimuli in free-viewing condition could be consistent with a face-specific spatial neglect in our patient. While typical neglect patients have been shown to fail in processing both face and non-face chimeric stimuli (Sarri, Kalra, Greenwood, & Driver, 2006; Young, Hellawell, & Welch, 1992), patient K.L. reported by Young et al. (1990) demonstrated a selective neglect in face processing. K.L. was affected by prosopagnosia and complained of unilateral right PMO (he referred that faces looked “different” or “deformed” and eyes were somehow misplaced). K.L. was impaired in processing the right-half of faces on different tasks, involving whole faces, chimeric faces, and half-faces presented in isolation; at variance, the patient was faultless in processing objects other than faces (e.g., car-fronts). K.L.’s impaired performance for the right side of facial stimuli was evident also when they were presented in the intact visual hemifield. On this basis, Young et al. (1990) suggested that K.L.’s clinical picture could be explained by a defect in lateralised face-specific attentional mechanisms, independent from visual field. The existence of such mechanisms has been also demonstrated by studies on chimeric face processing in normal subjects, who show a superiority in processing the right half of faces in free-viewing conditions but not in tachistoscopic presentation (Grega, Sackeim, Sanchez, Cohen, & Hough, 1988; Levy et al., 1983). According to Young et al. (1990), the attentional disorder in their patient would lead to a defect of “the mental representation” of one side of the faces (p. 412). Our patient’s subjective asymmetry in perceiving face stimuli was concomitant with a lateralized impairment in processing the left side of chimeric faces in free-viewing condition, as in patient K.L. assessed by Young et al. (1990) with the same procedure. However, the present patient D.G. showed defective performance on the opposite half of faces with respect to K.L. and, differently from K.L., she was not prosopagnosic and did not fail on the half-face task. Therefore, the hypothesis of a domain-specific form of unilateral neglect would require some specification to entirely account for the present clinical picture. If we posit that an analogous attentional system devoted to processing the contralateral side of faces is also present in the left hemisphere, our patient’s cognitive defect could be related to an impairment of such a system, that would render less effective the internal representation of the left side of faces (as suggested by Young et al., 1990; see also Levy, Trevarthen, & Sperry, 1972). However, functional consequences of this defect would be less severe than those observed after a right hemisphere lesion because of the lower specialization of the left hemisphere in face processing. In some sense, this defect would reveal itself only when integration of left- and right-sided information is required (and not with half-faces), as in a sort of extinction of left-sided face representation by right-sided ones. At variance, the analogous defect after a right hemispheric lesion would determine the more severe picture of facial neglect described by Young et al. (1990), likely associated to prosopagnosic disturbances. This interpretative hypothesis is admittedly based on several post hoc assumptions, and requires further independent evidence to be verified, but it would be consistent with available theoretical models of face processing. In terms of classical face recognition models, such that put forward by Bruce and Young (1986), the present putative defect of the attentional system would affect early stages of face processing, involved in extracting structural aspects of facial stimuli. The unilateral nature of the defect would suggest
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that early face processing stages are based on parallel mechanisms in the two hemispheres, although with different degrees of efficiency. Only after these early stages, specialized right hemispheric functions would take place. According to our hypothesis, a left occipital damage might only generate a contralesional defect in early stages of face processing, while a right occipital damage could give rise to either unilateral PMO for the right side of the face, or PMO disorders affecting the whole face, besides the classical impairments of face recognition. This interpretation follows the logic of the late convergence hypothesis for face-selective visual information; computational modelling of face processing would suggest that only at a late stage contralateral visual information gathered by the two hemispheres are integrated together, after some information extraction has been applied separately in each hemisphere (Hsiao, Shieh, & Cottrell, 2008). In the same vein, electrophysiological studies on face and word recognition demonstrated that an early ERP component is modulated by contralateral features of the stimulus (Smith, Gosselin, & Schyns, 2004). Our proposal is consistent with both neuropsychological and neurofunctional data demonstrating a right hemispheric lateralization for face processing (Ishai, 2008), but highlight that contralateral visual information are first separately processed by the two hemispheres and then integrated in the right hemisphere. In the light of anatomofunctional data supporting a hierarchical organization of face processing areas (Fairhall & Ishai, 2007; Haxby, Hoffman, & Gobbini, 2000), unilateral PMO after a left hemisphere lesion would suggest that face-responsive regions in occipital areas of each hemisphere are involved in building up internal representation of the contralateral side of face. Output from this stage would then be directed towards the fusiform face area of the right hemisphere where the integration of information from two sides of face takes place. In synthesis, we described a patient with chronic and selective subjective complaints of PMO for the left half of faces after a left hemisphere lesion. To explain this very unusual clinical picture, we speculated that early stages of face perception proceed in parallel in the two hemispheres and only at late stages the right hemisphere integrates information gathered from both parts of the stimulus to build up an unitary face representation. Replication of such findings and neurofunctional investigations on patients with PMO are warranted to directly verify neural dynamics related to unilateral defects in face processing. References Angelini, R., & Grossi, D. (1993). La terapia razionale dei disordini costruttivi. Roma: Centro di Riabilitazione S. Lucia. Benton, A. L., De Hamsher, K., Varney, N. R., & Spreen, O. (1992). Test di riconoscimento di volti ignoti. Firenze: Organizzazioni Speciali. Bodamer, J. (1947). Die Prosop-agnosie. Archiv für Psychiatrie und Nervenkrankheiten, 179, 6–53. Butler, S., Gilchrist, I. D., Burt, D. M., Perrett, D. I., Jones, E., & Harvey, M. (2005). Are the perceptual biases found in chimeric face processing reflected in eye-movement patterns? Neuropsychologia, 43, 52–59. Bruce, V., & Young, A. (1986). Understanding face recognition. British Journal of Psychology, 77, 305–327. Brust, J. C. M., & Behrens, M. M. (1977). “Release Hallucinations” as the major symptom of posterior cerebral artery occlusion: A report of 2 cases. Annals of Neurology, 2, 432–436. Critchley, M. (1953). The parietal lobes. New York: Hafner. Crawford, J. R., & Garthwaite, P. H. (2002). Investigation of the single case in neuropsychology: Confidence limits on the abnormality of test scores and test score differences. Neuropsychologia, 40, 1196–1208. Della Sala, S., Laiacona, M., Trivelli, C., & Spinnler, H. (1995). Poppelreuter-Ghent’s Overlappping Figures Test: Its sensitivity to age, and its clinical use. Archives of Clinical Neuropsychology, 6, 511–534. Ebata, S., Ogawa, M., Tanaka, Y., Mizuno, Y., & Yoshida, M. (1991). Apparent reduction in the size of one side of the face associated with a small retrosplenial hemorrhage. Journal of Neurology, Neurosurgery and Psychiatry, 54, 68–70. Fairhall, S. L., & Ishai, A. (2007). Effective connectivity within the distributed cortical network for face perception. Cerebral Cortex, 17, 2400–2406.
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