n people. At the clinical interview, he was courteous, well groomed, and talkative. Spontaneous speech appeared normal and he was orientated in time and place. Visuoconstructive skills and verbal and non-verbal working memory were within normal range, and non-verbal reasoning was at a superior level. He performed Weigl’s sorting test without trouble. In contrast, his performance on tasks involving thing concepts (e.g. picture naming, definitions, generating concrete nouns) was impaired. He showed a pronounced semantic anomia, notably for animals, vegetables, and famous faces. Associative agnosia was present (Pyramids and Palm Trees Test, three-picture version). Repetition was preserved. Syntactic comprehension was preserved in both Swedish and German (Bilingual Aphasia Test). Reading aloud showed a surface alexic error pattern. Spelling on dictation showed a lexical agraphic pattern. Repeated testing indicated further deterioration of conceptual knowledge and slowing in attention-demanding tasks, while spatial cognition was retained. When last seen at the clinic, his anomia was severe. He referred to every oblong inanimate object as a “tamp” (rope’s end; he had been a yachtsman), whereas animals and humans alike were referred to as “a young woman” or “a man”.

His EEG was normal. Alpha rhythm with peak frequency at 9 Hz. MRI scanning showed marked bilateral but asymmetric temporal lobe atrophy, more pronounced at the left side and anteriorly. SPECT revealed strongly reduced left temporal perfusion.

Case 2: SD with predominant right-hemisphere atrophy This 60-year-old right-handed man presented with increasing difficulties in understanding words and pictorial symbols. Family members reported a tendency towards behaving embarrassingly in larger social contexts. He still worked part-time in a technically demanding position, but withdrew from verbally taxing duties because of his inability to understand words. At the clinical interview he was well groomed, courteous, and humorous. He was cooperative and claimed to be eager to learn why he had become “crazy, or rather, defective”. Jocular and compulsive traits were shown at the ward. For instance, he supervised the dishwasher so that nobody put the dishes in another order than that preferred by him. He expressed the concern that he might be a nuisance to the staff. Neuropsychological testing showed preserved working memory, visuoconstructive praxis, and psychomotor speed, while verbal abilities and identification of visual symbols were strongly impaired. Memory for faces, both known and unknown, was also strongly impaired. At speech-language assessment, he showed a profound semantic anomia and inability to understand virtually any concrete noun. In contrast, his spoken output was phonologically and syntactically well formed. Surface alexia and lexical agraphia were presented, as was associative agnosia.

Case 3: SD with predominant left-hemisphere atrophy This 62-year-old right handed woman presented with increasing difficulties in finding nouns even for very common objects. Her language problems had started 6 years before testing. She took up painting and participated in semi pro shows with her art and managed to go abroad doing this in spite of her severe language problems. Everyday activities like shopping did not trouble her, as she found out that she could make small drawings of items to be bought at the grocery. However, she was unable to make a drawing from memory, and was dependent on having an item in front of her when producing these small drawings. At the clinical interview she was anxious to find an explanation for her impairment, and she offered several hypotheses for her impaired speech. At testing she was cooperative and responded quickly to questions. Her personality was rather impulsive. Judging from her scores on AMQ, a self-report questionnaire [10], subjective memory for places as well as some aspects of face memory were preserved. Neuropsychological testing showed preserved logical and visuospatial skills and impaired verbal learning. Speechlanguage assessment showed profound anomia on picture naming and severely impaired letter and category fluency.

Case 4: SD with left hemisphere atrophy This 60 year-old right handed woman presented with increasing speech difficulties. Neuropsychological testing showed severely impaired semantic memory, impaired verbal learning and verbal episodic memory. Personal episodic memory and working memory for digits were intact as well as logical and visuoconstructive ability. Speech-language assessment revealed severe semantic anomia, orthographic agraphia and surface alexia. Associative agnosia for faces and objects was presented.

Case 5: SD with right hemisphere atrophy This 65-year-old man presented with increasing personality changes including impaired judgement. Neuropsychological testing showed impaired semantic memory and verbal learning as well as subnormal verbal episodic memory, although his verbal recognition score was preserved. His visuoconstructive ability was good as well as his Mini mental state.

For details regarding regular test scores for the SDparticipants, see Table 1.

3. RESULTS

3.1. Control Samples

In order to collect data on the performance of healthy subjects in different age groups in the Male Faces test, four groups were tested: senior high school students and college students in a medium sized town in the western part of Sweden, police officers from a big city in western Sweden, and a random sample of middle aged and elderly from a northern Swedish town. Mean scores in the Male Faces and Euro Flags tests are shown in Table 2. Because there were no significant differences between men and women in either test, separate mean scores for the two genders are not reported.

Among the group of middle aged and elderly, range 38 - 94, there was a significant correlation between Male Faces recognition scores and age (r = 0.58, P < 0.01). Because the relationship was rather curvilinear, an exponential regression was better fit to the data. The nonlinear correlation was (r = 0.60). There was also a signifycant correlation between Euro Flags and Male Faces in this sample (r = 0.46, P < 0.01), indicating a shared variance of about 21% between the two tests in this sample.

3.2. SD Patients

As can be seen from Table 3 all five SD patients perform at a random level in Male Faces with a median of 55 percent correct, while four of them performed within the normal range in Euro Flags and Political Faces. The reversed distribution of SD cases who passed or failed the Political Faces and the Male Faces tests was signifi cant (Fisher’s exact P > 0.01).

3.3. Test Behavior

Three of the SD patients were predominantly impulsive indicated by short reaction times in the computerized tests. One of these three patients at two occasions enacted his ideas: for instance, to make it clear he was

Table 2. Means and standard deviations in male faces, Euro flags and political faces among healthy control samples.

Table 3. Recognition scores in non-verbal computerized memory tests among five SD participants. Subnormal scores are in boldface.

not “like the rest of you” he turned around as he remarked “Just so that you know I am a little whimsy!” (sv. snurrig)

After the testing session, one of these SD patients asked the examiner how the photos in the tests had been edited. After an explanation, and to give the patient a clue about the editing process, she was allowed to play with the Photoshop program which had been used at the design phase. After a brief introduction and with no prior experience in computer-aided painting, she quickly mastered the software and completed an expressive picture in a few minutes. This was in sharp contrast to her inability in drawing, because while her copying was preserved, her drawing from memory was severely impaired. She was unable to draw a bicycle from memory, though she was an eminent semi-pro expressive painter.

4. DISCUSSION

In this study, five patients with SD underwent two tests of face recognition, Male Faces and the Political Faces. The former test is an episodic face recognition test measuring recent face recognition, and the latter is conceived as a semantic face recognition test. The Male Faces test was administered to different groups showing about the same level of performance for participants below 70 years of age, which made it an appropriate instrument for the group of relatively young SD patients, who by the time of testing had a median age of 62. During the retention period of Male Faces all participants including the SD cases also took the Euro Flags test, a non-facial semantic recognition test.

SD subjects performed within normal range on the non-verbal semantic tests (Political Faces and Euro Flags) whereas episodic face recognition (Male Faces) was severely impaired. This is a surprising finding inasmuch as SD is generally characterized by severe semantic loss and clinically preserved episodic memory. This counterintuitive finding indicates that item knowledge of current politicians based on incidental encoding may in fact be preserved in SD. Performance on a semantic memory test may thus paradoxically be normal in SD. This in turn sheds doubt on the common notion of semantic memory as an atemporal form of memory, because the temporal range of “current nationwide politicians” may be 5 - 10 years, depending on the number of exposures. This may be compared to schematically organised knowledge acquired one week or a month earlier, such as knowledge about the immediate work environment and personal schedules and events tied to these. This latter kind of knowledge is, based on anecdotal clinical evidence, relatively preserved in SD, because the patients remember their appointments with examiners at the clinic and are able to run their own everyday life.

Four out of five of the SD patients also scored within normal range on the Euro Flags test, a test of non-facial semantic memory. Again, the notion of an atemporal semantic memory is called into question. Knowledge of the visual appearance of flags probably goes back far longer than knowledge of current political figures in these patients. Thus, the Euro Flags test may be regarded as a more specific semantic memory test than the Political Faces test. Moreover, because nation flags are conventional symbols of countries or nations, they carry more meaning and are thus more semantic in character than faces of politicians. The label semantic memory test therefore would be more appropriate for Euro Flags. Nevertheless, personal interest may play an important role in determining the number of incidental learning occasions regarding European flag knowledge. For example, flag learning may differ substantially between different groups. Irrespective of this, the artifactual schematic design of flags makes them quite different as visual objects compared to faces. The face is inherently a potential origin of a large amount of human signals or messages, whereas a nation flag does not really convey any message at all apart from signifying a nation. When analyzing what part of the world of meaning that our SD patients have lost, we may thus conclude that they may still master such non-verbal representations of central world knowledge as exemplified by flags.

The same SD patients, however, scored in the subnormal range, actually within the random range, on the Male Faces test. This is an episodic recent memory test, which, regarding the performance of the SD patients, indicates poor encoding of static person information of a non-verbal kind. Judging from the results of the study, a single presentation for 5 seconds is not enough to form even a slight recent episodic memory in these patients, even if the medial temporal lobe and more posterior cortical structures might support learning when presentation time is long and repeated. However, when the latter conditions are met, as is the case with well-known political figures who often appear as dynamic information on television, patients with SD seem to be able to form and retain robust face recognition. We may also note that 3/5 of SD patients in this study had left hemispheric atrophy, not the right temporal lobe atrophy typical of semantic dementia presenting with progressive prosopagnosia.

Because of their specific problems our SD patients did not recognize celebrities of the 1960s, which is a typical finding [10]. For example, one of our patients, who was a classmate of a very famous Swede, did not recognize this national celebrity from a photo at testing. In spite of this, he incidentally mentioned that he had seen the former classmate at the airport recently, but was too shy to approach him. This is in accordance with our theory that movement properties of persons, or in other words object properties of activities involving people as objects, may aid face recognition in SD Arguably, these properties should not be viewed as part of core conceptual structures or semantic memory per se, but rather as parts of spatial structures connected to word meaning [11]. In contrast to AD, the brain systems critical for this aspect of spatial cognition are known to be largely preserved in SD. While there is a moderate generalized brain atrophy in SD, the region with accentuated atrophy does not involve the posterior superior temporal region or inferior parietal lobule. This characteristic pattern of atrophy was figured already by Onary & Spatz [12].

According to James & Gauthier [13] the posterior superior temporal sulcus, which is known to respond to motion, was “preferentially activated by objects associated with ‘action’ features (e.g., hops)”. This finding supports the hypothesis of preserved action cues or motion affordances in SD. Tyler et al. [14] reported activation of the left fusiform gyrus and the superior and middle temporal cortex during retrieval of object names and their associated actions. This was claimed to be consistent with the notion that tool words and animal concepts “implicitly activate the actions associated with them”. However, it may also be the other way around: Because objects are often significant or required parts of actions and the conceptualization of actions and activities as such, it would not be surprising that thinking about objects and actions activates approximately the same set of brain regions.

A recent activation study by Kable et al. is very much in line with this reasoning [15]. They reported activation of areas close to MT/MST on the left “within the aspect of the middle and superior temporal gyri” when subjects were accessing knowledge of actions through words. They proposed that “the lateral occipital-temporal cortex contains a mosaic of neural regions that processes different kinds of motion, ranging from the perception of objects moving in the world to the conception of movement implied in action verbs”. According to Kable et al. the “lateral occipital-temporal cortex mediates the perceptual and conceptual features of action events”. However, “knowledge of actions” implies an idea of activity as such, that is, in Aristotelian terms, the potentiality for action of a person or animal. Activity may thus be mediated by relatively posterior regions, while its counterpart, action, as the actualization of activity, may be more dependent on frontal structures, which are important for initiating, maintaining, modifying, inhibiting or other properties related to action.

A methodological issue when assessing prosopagnosia is how to measure it in a clinical setting because of technical problems without making too much violence on ecological validity. Spoken words and written text are by definition much easier to expose to the patient, because they occur as such in the stimulus material. People and faces in experimental studies usually appear as pictorial representations, implying that investigators are most often confined to static images like photographs or drawings. When we design tests for the measurement of face recognition we also, in the name of perfect experimentation technique, try to refine the stimulus material in such a way as to clean them from emotional attributes. This was also the case in this study, for pure psychometric reasons, in order to arrive at a reliable and valid test. Photographs used in the Male Faces test were carefully chosen in order to eliminate confounding effects due to imbalance between targets and distractors. However, because people in the real world do not appear as static photographs without any emotional expressions or other motion attributes, we would rather characterize the Male Faces test, like all other alleged face memory tests, as a static non-emotional face recognition test. This point must be made in this context because we might have arrived at another pattern of result if we had used films or clips of films instead of photographs as stimuli. And then prosopagnosia paradox, that is, a preserved semantic memory for faces and a severely impaired episodic memory for faces in SD, would possibly not turn out to be paradoxical at all.

Methodological Issue

The five SD cases reported in this study were a few years older than the sample of controls who took the Political Faces test. The older control sample did not take this test, and this would have improved the study. However, this relatively younger sample with a mean age of 55 scored at about the same level as the SD cases.

5. CONCLUSION

Based on this study and the unsolved methodological issue discussed above we thus propose a follow-up study of face recognition in SD, which would use films or short film clips in addition to photographs as stimuli. This would help to identify the main factor behind the prosopagnosia in SD: time for encoding or lack of action attributes in photos. The critical experiment would be straightforward and demand the following: 1) variation of exposure times of stimuli, and 2) addition of tests of face recognition based on film clips with or without voice. If SD patients perform within the normal range or approach average performance levels at longer exposure times, we may conclude that their atrophy slows down their face encoding. If SD patients perform in the normal range when faces are presented on film, we would be more certain in concluding that their atrophy leads to degraded static information of face processing but leaves activity processing of faces intact.

6. ACKNOWLEDGEMENTS

PÖ’s participation was supported by a grant from the Gun and Bertil Stohne Foundation.

REFERENCES

  1. Crook, T.H. and Larrabee, G.J. (1992) Changes in facial recognition memory across the adult life span. Journal of Gerontology, 47, 138-141. HHUdoi:10.1093/geronj/47.3.P138U
  2. Measso, G., Romani, L., Martini, E. and Zappala, G. (1990) Preliminary analysis of effects of “normal” aging on different memory processes and abilities. Perceptual & Motor Skills, 71, 395-401.
  3. Snowden, J.S., Goulding, P.J. and Neary, D. (1989) Semantic dementia: A form of circumscribed cerebral atrophy. Behavioural Neurology, 2, 167-182.
  4. Hodges, J.R., Patterson, K., Oxbury, S. and Funnell, E. (1992) Semantic dementia. Progressive fluent aphasia with temporal lobe atrophy. Brain, 115, 1783-1806. HHUdoi:10.1093/brain/115.6.1783U
  5. Snowden, J.S., Thompson, J.C. and Neary, D. (2004) Knowledge of famous faces and names in semantic dementia. Brain, 127, 860-872. HHUdoi:10.1093/brain/awh099U
  6. Simons, J.S., Graham, K.S., Galton, C.J., Patterson, K. and Hodges, J.R. (2001) Semantic knowledge and pisodic memory for faces in semantic dementia. Neuropsychology, 15, 101-114. HHUdoi:10.1037/0894-4105.15.1.101U
  7. Mondini, S. and Semenza, C. (2006) How Berlusconi keeps his face: A neuropsychological study in a case of semantic dementia. Cortex, 42, 332-335. HHUdoi:10.1016/S0010-9452(08)70359-9U
  8. Lewin, C. and Herlitz, A. (2002) Sex differences in face recognition—Women’s faces make the difference. Brain and Cognition, 50, 121-128. HHUdoi:10.1016/S0278-2626(02)00016-7U
  9. HHJulin, P., HHHHAlmqvist, O., HHHHBasun, H., HHHHLannfelt, L., HHSvensson, L., Winblad, B. and HHWahlundHH, L.O. (1998) Brain volumes and regional cerebral blood flow in carriers of the Swedish Alzheimer amyloid protein mutation. Alzheimer’s Disease and Associated Disorders, 12, 49-53. HHUdoi:10.1097/00002093-199803000-00008U
  10. Neary, D., Snowden, J.S., Gustafsson, L., Passant, U., Stuss, D., Black, S., Freedman, M., Kertesz, A., Robert, P.H., Albert, M., Boone, K., Miller, B.L., Cummings, J. and Benson, D.F. (1998) Frontotemporal lobar degeneration: A consensus on clinical diagnostic criteria. Neurology, 51, 1546-1554. HHUdoi:10.1212/WNL.51.6.1546UH
  11. Jackendoff, R. (1996) The architecture of the linguisticspatial interface. In: Bloom, P., Peterson, M., Nadel, L. and Garrett, M., Eds., Language and Space, MIT Press, Cambridge, 1-30.
  12. Onari, K. and Spatz, H. (1926) Anatomische beitrage zur lehre von der pickschen umschriebenen grosshirnrindenatrophie (“Picksche Krankheit”). (English version: Anatomical contributions to the theory of the circumscribed cortical atrophy of Pick’s disease.) Zeitschrift für die Gesamte Neurologie und Psychiatrie, 101, 470-511.
  13. James, T. and Gauthier, I. (2003) Auditory and action semantic feature types activate sensory-specific perceptual brain regions. Current Biology, 13, 1792-1796.
  14. Tyler, L.K., Stamatakis, E.A., Dick, E., Bright, P., Fletcher, P. and Moss, H. (2003) Objects and their actions: Evidence for a neurally distributed semantic system. Neuroimage, 18, 542-557. HHUdoi:10.1016/S1053-8119(02)00047-2U
  15. Kable, J.W., Lease-Spellmeyer, J. and Chatterjee, A. (2002) Neural substrates of action event knowledge. Journal of Cognitiuve Neuroscience, 14, 795-805. HUdoi:10.1162/08989290260138681U

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