Brain, Vol. 126, No. 4, 792-803,
April 2003
© 2003 Guarantors of Brain
doi: 10.1093/brain/awg092
Slowly progressive defect in recognition of familiar people in a patient with right anterior temporal atrophy
Neuropsychology Unit, Policlinico Gemelli, Catholic University of Rome, Rome, Italy
Correspondence to: Professor Guido Gainotti, Servizio di Neuropsicologia, Policlinico Gemelli, Largo A. Gemelli, 8, 00168 Roma, Italy E-mail: gainotti{at}rm.unicatt.it
Received August 29, 2002. Revised November 12, 2002. Accepted November 14, 2002.
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We report the case of a patient (C.O.) who showed a selective defect in the recognition of familiar people, with very mild disease progression during a period of 30 months resulting from focal atrophy of the right temporal lobe. On formal neuropsychological testing, C.O. obtained high scores on tests of general intelligence, episodic memory, language, executive functions, selective attention, visual recognition and visual–spatial abilities. On more specific tasks of familiar and unfamiliar face recognition, C.O. scored above the controls’ means on perceptual tests, but obtained highly pathological results on mnesic–associative tests. His disorder of recognition of familiar people was not due to loss of person-specific information, since he obtained highly abnormal naming scores when presented with photographs of famous people but borderline or mildly abnormal scores in a tasks in which he had to name celebrities from verbal definitions. On the other hand, C.O.’s recognition disorder could not be considered to be a form of ‘associative prosopagnosia’ since a similar defect was observed when he was requested to access information about famous persons through their voice rather than their face. Two alternative interpretations are advanced to explain C.O.’s inability to access his relatively spared person-specific knowledge not only through the person’s face but also through the person’s voice. The first hypothesis is that, before accessing the person-specific information, unimodal recognition channels must converge into a multimodal, non-verbal person-recognition system and that the right anterior temporal cortices play a crucial role in this integrative activity. The second hypothesis is that the face-recognition units have privileged access to person-specific semantic knowledge and that other recognition subsystems require coactivation of the face-recognition units in order to access person-specific semantic information.
Keywords: face recognition; recognition of familiar people; frontotemporal dementia; prosopagnosia; right anterior temporal atrophy
Abbreviations: FRU = face recognition unit; IAC = interactive activation and competition network; MMSE = Mini-Mental State Examination; PIN = person identity node; RAVLT = Rey’s Auditory Verbal Learning Test; VOSP = Visual Object and Space Perception Battery
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Introduction |
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Since Mesulam’s (1982
) first description of patients showing primary progressive aphasia as the result of focal atrophy of the left perisylvian cortices, several authors have described other selective cognitive disorders, due to equally selective atrophies of well circumscribed neocortical areas. Thus, De Renzi (1986), Benson et al. (1988) and Freedman et al. (1991) have reported patients with a slowly progressive visual agnosia associated with posterior (occipital) cortical atrophy; Hof et al. (1989), Berthier et al. (1991) and Victoroff et al. (1994) have described instances of progressive spatial disorders (with symptoms of Balint’s syndrome) in patients with bilateral parietal atrophy, and De Renzi (1986), Dick et al. (1989) and Gibb et al. (1989) have described cases of slowly progressive apraxia (with or without signs of corticobasal degeneration) in patients with asymmetrical parietal atrophy. Furthermore, Snowden et al. (1989) and Hodges et al. (1992) have described, under the name of ‘semantic dementia’, a degenerative syndrome consisting of severe anomia and progressive loss of semantic memory resulting from selective atrophy of the anterior and inferolateral parts of the left temporal lobe. This degenerative syndrome is particularly interesting from the viewpoint of the present report, since some anatomoclinical observations seem to show that, when the same temporal lobe structures are affected on the right side of the brain, a very different cognitive defect, namely a progressive impairment in the recognition of familiar faces (more generally, of familial people), can be identified. Tyrrell et al. (1990), Barbarotto et al. (1995), Evans et al. (1995) and Gentileschi et al. (1999, 2001) have described patients showing from the clinical standpoint a progressive defect in the recognition of familiar faces (or, in some cases, a cross-modal defect in the recognition of familial people) and from the anatomical point of view a prevalent or selective atrophy of the anterior temporal areas of the right hemisphere. These observations are consistent with (i) the anatomical correlates of the so-called associative forms of prosopagnosia and (ii) the results of some activation studies devised to clarify the functional neuroanatomy of the processing of face recognition. In support of the first point, De Renzi et al. (1991, 1994) and Tranel et al. (1997) have shown that defective recognition of familiar faces, in the absence of widespread disorders of visual perception and of defects in the perceptual analysis of unfamiliar faces, is usually observed in patients with anterior lesions of the right temporal lobe. With regard to the second point, PET and functional MRI studies of face recognition in healthy people have suggested that the anterior temporal regions of the right hemisphere play a critical role in face recognition (Sergent et al., 1992; Sergent and Signoret, 1992; Gauthier et al., 2000).
At first sight, the observation that focal atrophy of the antero-inferior parts of the temporal lobes leads to a progressive semantic disorder when the lesion is on the left side and to a progressive face recognition disorder when the atrophy affects the homologous structures of the right hemisphere may seem rather trivial. This distinction could, indeed, reflect other well-known aspects of brain lateralization, namely the dominance of the left hemisphere for language and the specialization of the right hemisphere for face processing. However, careful scrutiny of the available data suggests that the picture is more complex and interesting, for two main reasons. The first is that, at least in some patients, the recognition disorder resulting from atrophy (or from other kinds of lesion) of the anterior parts of the right temporal lobe seems to be due to a cross-modal disorder of the recognition of familiar people rather than to simple prosopagnosia. This claim holds in particular for patients V.H. (Evans et al., 1995), M.F. (Barbarotto et al., 1995), Maria (Gentileschi et al., 1999) and Emma (Gentileschi et al., 2001), who were affected by focal atrophy of the anterior parts of the right temporal lobe, for patient B.D. (Hanley et al., 1989), who suffered from selective damage to the anterior right temporal lobe resulting from herpes simplex encephalitis, and for patient K.S. (Ellis et al., 1989), who had sustained a right temporal lobectomy for intractable epilepsy. The second reason is that a similar cross-modal disorder of the recognition of familiar people, affecting various aspects of person-specific knowledge, has also been observed in patients with lesions encroaching on the anterior parts of the left temporal lobe. Patients belonging to this group have often been described as suffering from anomia for proper names (Damasio, 1996; Fukatsu et al., 1999); however, even though some patients have an excellent knowledge of people they cannot name (Harris and Kay, 1995), in other patients a careful scrutiny of performances obtained across various modalities rather suggests a loss of person-specific knowledge (Miceli et al., 2000).
Taken together, these data suggest that there is a more complex articulation between language processing, face processing and various aspects of semantics (related either to general categorical knowledge or to person-specific knowledge). The study of new patients showing defective recognition of familiar people as a consequence of right anterior temporal atrophy could help to clarify this issue. In this paper we describe a new patient with focal atrophy of the right anterior temporal lobe, who presented with a progressive impairment in his ability to recognize familiar people, in the absence of other memory, cognitive or perceptual disorders. During a period of 30 months (from June 1999 to January 2002), this patient showed a rather stable condition characterized by a severe form of associative prosopagnosia, by a similar inability to identify familiar persons through their voice and by much milder difficulty in accessing person-specific information through the person’s name.
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In June 1999, C.O., a 49-year-old right-handed man with 13 years of formal education, was referred to our service because of increasing difficulty recognizing familiar people and a questionable, mild personality change. The patient lived with his wife in a small town in central Italy, worked in an Italian bank and had two sons who lived with him. There was no history of dementia or neurological disease in the family and the wife mentioned no previous head trauma, psychiatric disorders or alcohol abuse.
About 1 year before coming to our attention, C.O. had noticed that he did not easily recognize the friends of his sons or their parents. Furthermore, he had also acknowledged some difficulty recognizing persons known as long-time customers of the bank. However, his daily life was not affected by these difficulties since he was still able to recognize lifelong friends and relatives.
Towards the end of 1998, two episodes forced him to acknowledge that the problem was more serious than he had previously realized. The first was a change of office. When he returned to his old office after having worked for a couple of years in another one, all his old colleagues obviously recognized him, whereas he was unable to recognize them. The second was a visit by the mayor of the town, whom he was unable to recognize in spite of having been introduced to him some days earlier. Probably as a consequence of these episodes, his wife noticed a mood change, with a tendency to become more depressed, anxious and irritable.
C.O. underwent a detailed neuropsychological assessment on five occasions during a period of 30 months (from June 1999 to January 2002). In each test session, the patient underwent a general neuropsychological assessment and received standard or experimental tests to explore specific aspects of his difficulty recognizing familiar people. Because the clinical picture did not show important changes in the cognitive tests that were administered repeatedly during the follow-up period, in the present paper we report in the same tables results obtained on general and specific tests both at the baseline and during the follow-up period.
Clinical notes
At the first examination, C.O. did not show any difficulty describing his deficits. He had no problem remembering dates, addresses and events of his life in recent months and was able to report details (e.g. places, dates and persons) about the most important episodes during which he had failed to recognize familiar persons. He said that his defect consisted selectively of inability to recognize a familiar face, whereas he was still able to recognize familiar persons using contextual information (such as hair, spectacles or dress). He also reported that, although unable to recognize a familiar face, he had initially been able to perceive the face as familiar, but even this ability was progressively vanishing; the deficit involved not only job-related persons, but also more distantly related members of his family, such as cousins. C.O. said that he had no difficulty recognizing facial emotional expressions or recognizing a person from his or her voice. His wife, however, questioned this last statement, noting that he had some difficulty recognizing the voice of persons in telephone calls, in particular when the person was not very familiar to him.
Being very concerned about these difficulties and worried about the possibility of losing acquired knowledge, C.O. began to develop compensatory strategies, such as reading encyclopaedias. In particular, as he had always been very involved in trade union activities and interested in political events, he began to collect pictures of famous persons in these fields in a photograph album.
Neurological examination
Neurological assessments performed on several occasions during the 30-month follow-up period were unremarkable. In particular, no pyramidal, extrapyramidal or cerebellar signs, no oculomotor abnormalities and no myoclonic jerks were observed. Somatosensory functions and visual fields were normal and no vestibular or hearing defects were detected.
Psychopathological assessment
Since the onset of the symptoms, C.O.’s wife had noted that he had a tendency to become more anxious, depressed and irritable, and she considered these to be accentuations of previous personality traits.
In the following months she also noticed (i) a progressive deterioration in his social activities, with increased egocentrism and mental rigidity and a reduction in the number and quality of social contacts; (ii) alternation of apathetic attitude with motor restlessness and verbal disinhibition (childish puns and jokes); (iii) and some changes in eating behaviour, with a tendency to overeat (in particular sweet foods).
Neuroradiological findings
An MRI obtained in May 1999 (Fig. 1) showed clear atrophy of the antero-inferior parts of the temporal lobes, greater on the right side, and questionable atrophy of the frontal lobes. These MRI findings were confirmed by a SPECT (single photon emission computed tomography) scan in June 1999 (Fig. 2), which showed severe hypoperfusion restricted to the anterior parts of the right temporal lobe
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General neuropsychological assessments
Formal neuropsychological tests, namely the Mini-Mental State Examination (MMSE) (Folstein et al., 1975
) and a standard neuropsychological battery devised to explore memory, language, praxis, executive functions, attention, visual and space perception and spatial reasoning, were administered five times between June 1999 and January 2002. Results of these serial assessments are reported in Table 1. These results indicate that (i) C.O. showed no signs of general mental impairment (MMSE) or of selective disorders of episodic memory [delayed recall of Rey’s Auditory Verbal Learning Test (RAVLT; Rey, 1958) and delayed reproduction of Rey’s complex figure (Rey, 1958)], language (phonological and semantic word fluency tasks), selective attention [Multiple Features Targets Cancellation (MFTC) (Gainotti et al., 2001)], executive functions [Luria tasks and Stroop interference test], high-level visual–spatial abilities [Raven’s Coloured Progressive Matrices (Raven, 1949)] or lower-level visual perception [Visual Object and Space Perception Battery (VOSP; Warrington and James, 1991)]; (ii) C.O. showed no evidence of visual naming disorders in the Snodgrass test, in which he obtained comparable results with both living and non-living items; (iii) this situation is relatively stable as it has shown only mild fluctuations and no consistent worsening during the 30 month period.
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Recognition of famous and unknown faces
Since the defect that had motivated the patient’s investigation consisted of a specific defect in face recognition, the testing battery devised by De Renzi et al. (1991
) to evaluate the apperceptive and the associative forms and prosopagnosia was also administered five times to C.O. between June 1999 and January 2002. This battery consists of two tests of unfamiliar faces (referred to as ‘perceptual’ tests by De Renzi et al., 1991) and two tests of famous faces (referred to as ‘mnestic’ tests by De Renzi et al, 1991).
The first perceptual test is the short form, devised by Levin et al. (1975), of Benton and Van Allen’s (1968) Face Matching Test, in which the patient is shown a photograph of an unfamiliar face that is lit so as to reveal only the central region of the face, excluding the hair. The patient is requested to match this face with other views of the same face (photographed from different perspectives), presented among similarly lit views of different faces.
The second perceptual test is the Age Estimation Test of De Renzi et al. (1989), in which the patient is presented with 12 cards, each containing four photographs of faces of the same sex but of different ages, with the instruction to point from the youngest to the oldest face.
The first (mnestic) famous faces test is the Familiarity Check Test (De Renzi et al., 1991), in which the subject is presented with 36 cards, each containing four faces of people (one famous and three anonymous) of the same sex and approximately the same age, and requested to point to the face that is to some extent more familiar than the others. The second famous face test is the Famous Face Recognition Test (De Renzi et al., 1991), in which the subject is presented with 32 cards, each containing four famous faces of the same sex and category (e.g. four actors), and is asked to point to the face corresponding to the name provided by the examiner. Only one face or name per display was tested.
In addition to providing the standard error of scores for each of these tests, by studying 100 age-, education- and sex-scattered healthy Italian controls, Faglioni et al. (1991) standardized the difference between the sum of the scores achieved on the perceptual and mnestic pairs of tests.
The adjustments for age and education and scale standardization made it possible to obtain three separate values for all four face recognition tests: (i) raw scores, (ii) standardized scores; (iii) age- and education-adjusted standardized scores. Furthermore, the statistical work carried out by Faglioni et al. (1991), providing normative values for the difference between pairs of tests, also made it possible to classify with 0.95 confidence Italian prosopagnosic patients as being more likely to belong to the ‘apperceptive’ or ‘associative’ end of a continuum (De Renzi et al., 1991). These statistical dissociation criteria were employed to determine whether C.O.’s scores reflected a predominantly perceptual or mnestic–associative face-processing deficit.
Table 2 gives results for each of the five face recognition assessments performed between June 1999 and January 2002. The table shows raw scores, standardized scores, standardized scores corrected for age and education, and differential scores between perceptual and mnestic tests.
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The data in Table 2 show that C.O. systematically obtained normal scores on the perceptual tests (age estimation and face matching test) and pathological scores on the mnestic–associative tests (familiarity check and famous face recognition test). If we consider that negative standard scores correspond to above-mean values, we can say that on the perceptual tests C.O. obtained results in the high range of normal controls in the first four assessments and slightly worse than the controls’ mean only on the last assessment. A similar trend to show progressive worsening of performance with disease progression was also observed in the mnestic–associative tests. The differential score between perceptual and mnestic tests is systematically above the cut-off point (2.88), which identifies a mnestic–associative form of face-processing disorder. All these data consistently show that C.O. suffers from a severe selective disorder of the recognition of familiar people.
Producing the names of celebrities from photographs and verbal definitions
As mentioned in the Introduction, the defective recognition of familiar people that is observed in some patients with right temporal lobe atrophy is not limited to a face recognition disorder, but also involves other modalities of person recognition. We tried to evaluate whether this was also the case with patient C.O. by administering on three separate occasions (November 2000, May 2001 and January 2002) the Famous Person Identification Test (I. Benaglio, S. Cappa and C. Semenza, unpublished), which contrasts the capacity to name 45 celebrities under two conditions: (i) from presentation of a photograph, and (ii) from a short verbal definition. The same test also explores the capacity to name 18 famous towns from a short verbal definition, in order to check if the deficit of these patients concerns famous people specifically or more general concepts denoted by a proper name and characterized by a particular semantic structure (Semenza, 1997). To evaluate the results obtained by C.O. with photographs and verbal definitions of famous people and with short definitions of famous towns, we used normative data obtained by I. Benaglio, S. Cappa and C. Semenza (unpublished) on a group of 50 healthy adult Italian subjects, subtracting two standard deviations from the controls’ mean scores to obtain the cut-off points between normal and pathological performances. Table 3 reports the normative data and the number of celebrities named by C.O. from photographs and verbal definitions.
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Data reported in Table 3 show that the results obtained by C.O. were severely abnormal when he was requested to give the name of a celebrity from a photograph, whereas they were borderline or mildly abnormal when a verbal definition was given to elicit the celebrity’s name. On the contrary, C.O.’s scores were consistently above the mean of the controls’ scores in naming famous towns from definitions.
An additional finding that emerged clearly from scrutiny of C.O.’s results was the influence on naming of the premorbid familiarity of the patient with different subcategories of celebrities. Irrespective of the modality of presentation, C.O. obtained his best results with politicians and trade union persons (with whom he was well acquainted) and his worst results with singers and actors (in whom he was not very interested).
Identification of friends and family members from photographs
Since C.O.’s defect in person identification had been noticed in the framework of his daily social activity, we tried to quantify this defect using photographs of friends and family members, obtained from his wife. Also, in order to check the influence of familiarity, which emerged from the study of celebrities, close family members and lifelong friends were distinguished from those less close. Twenty-eight clear photographs of close (n = 14) or less close (n = 14) members of his social network, were shown to C.O. for naming or other kinds of identification in May 2001 and in January 2002.
C.O. scored 14 out of 28 in May 2001 and 12 out of 28 in January 2002. His correct identifications were always of close friends and family members.
Accessing information about celebrities through the person’s face, voice and name
Results obtained by studying C.O.’s capacity to name celebrities from photographs and from verbal definitions had shown that he found it much more difficult to identify a celebrity through his or her face than through a verbal definition. According to his wife, however, it was not clear whether C.O.’s defect in the identification of familiar people was confined to visual (face) recognition or whether it also involved other perceptual modalities, such as the person’s voice.
To study this question, we constructed a new test to evaluate C.O.’s capacity to access information about 20 celebrities from their face, voice and name. This test consisted of several sections, which were administered to C.O. and his wife on different days. In the first two sections, the face and voice of a famous person were presented individually to C.O. in pseudorandom order, and he was requested to name or to give as much information as possible about the target person. In the third section, the voice of a celebrity was presented to C.O. He was instructed to point to the corresponding face, choosing it from among photographs of four of celebrities of the same sex. In the fourth section, C.O. was given the name of a famous person and was instructed to provide as much information as possible about that person. Finally, in the fifth section the name of a celebrity was presented to C.O., and (as in the third section) he was requested to point to the corresponding face, choosing it from among photographs of four of celebrities of the same sex. Results obtained by C.O. in these tasks were matched with those obtained by his wife, who was of comparable age and educational level. The verbal definitions given by C.O. and by his wife in sections 1, 2 and 4 were pooled and given to an independent rater, who was requested to guess the name of the person or to decide if the information provided was correct. The test was given to C.O. and to his wife in May 2001 and in January 2002. Results obtained by C.O. and his wife in these two test sessions are reported in Table 4.
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The data in Table 4 clearly show that the results obtained by C.O. were considerably worse than his wife’s results when information about a famous person had to be accessed either through the visual/face or the auditory/voice channel. This was true both when C.O. was requested to name (or define) a target face or voice and when he was requested to point to the face corresponding to a given name or voice. In the latter case, however, his results were clearly better when the stimulus corresponded to the person’s name rather than to the person’s voice. The results obtained by C.O. were much better (though still impaired) when he was given the name of a famous person and requested to give as much information as possible about him. Between May 2001 and January 2002, C.O.’s results showed further slight deterioration, whereas those of his wife improved slightly because of a practice effect.
It was also of some interest to evaluate the relationship between results obtained in the visual/face modality and the auditory/voice modality. To do this, we studied the consistency of errors within modalities (from the first to the second presentation of the face-naming and voice-naming tests) and across modalities (between face and voice in May 2001 and January 2002). The consistency of errors was extremely high both within and across modalities (95% from the first to the second presentation both for the face-naming and for the voice-naming task; 80% in May 2001 and 83% in January 2002 between results obtained in the face-naming and voice-naming tasks). This last result suggests intercorrelation rather than independence between defective recognition observed in the visual and auditory modalities.
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Discussion |
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Our patient C.O. is affected by a slowly progressive, very selective defect in the recognition of familiar people, resulting from focal atrophy of the anterior parts of the right temporal lobe.
In formal neuropsychological tests to assess several cognitive domains, administered five times between June 1999 and January 2002, C.O. consistently performed above the mean level on tests of episodic memory, language, selective attention, lower-level visual perception and higher-level visual recognition and visual–spatial abilities. In the more specific tasks of familiar and unfamiliar face recognition, C.O. scored above the controls’ means on the perceptual tests, but obtained highly pathological results on the mnesic–associative tests, in which he showed slow worsening of performance as the disease progressed. A similar selective, progressive defect in the recognition of familiar people has been reported by other authors (Tyrrell et al., 1990; Barbarotto et al., 1995; Evans et al., 1995; Gentileschi et al., 1999, 2001) in patients with selective atrophy of the anterior temporal cortices similar to that recorded in patient C.O.
The main theoretical problem raised by these findings concerns the cognitive locus of the lesion underlying the defective recognition of familiar people, since different interpretations are suggested by anatomophysiological and by clinical considerations. If we take as our cognitive framework the face-processing model proposed some years ago by Bruce and Young (1986), we can say that anatomical considerations suggest that the defect in these subjects lies at the level of the face-recognition units (FRUs). However, some clinical data suggest rather that their defect lies at the level of the person identity nodes (PINs), which store person-based semantic knowledge.
The suggestion that the defect in the recognition of familiar people in these patients may be due to disruption of the FRUs stems from the fact that the infero-anterior parts of the temporal lobes constitute the most rostral portion of the ventral stream of visual processing, which plays a crucial role in visual recognition. According to Mishkin et al. (1984), these cortices (and in particular area TE) may contain the ‘central representations’ of visual objects, and, in agreement with this viewpoint, Gross and Sergent (1992) and Allison et al. (1994) have identified face-selective neurons in the middle portion of the human fusiform gyrus. It may, therefore, be logical to expect that infero-anterior temporal atrophy, disrupting these FRUs or disconnecting them from the corresponding PINs, causes a sort of ‘associative prosopagnosia’. This could hold in particular for right-sided lesions, owing to the dominance of the right hemisphere for face processing (De Renzi et al., 1991, 1994; Sergent et al., 1992).
On the other hand, clinical data have shown that, at least in some patients (Ellis et al., 1989; Hanley et al., 1989; Barbarotto et al., 1995; Evans et al., 1995; Gentileschi et al., 1999, 2001), the recognition disorder is not limited to the visual/face modality but can be observed across different modalities of access to person-specific semantic knowledge, pointing to a PINs defect.
This problem was tackled in C.O. by asking him to name some celebrities on presentation of a photograph and from a short verbal definition, and to access information about famous persons through their face, voice and name. Results of these experiments supported neither the hypothesis of associative prosopagnosia nor that of the loss of person-specific semantic knowledge.
Contrary to the associative prosopagnosia hypothesis, C.O. has shown severe inability to access person-specific information about famous persons not only through their face, but also through their voice. On the other hand, contrary to the hypothesis of loss of person-specific semantic information, C.O. has proven able to access much more information through the name or the verbal definition of a famous person than through his or her face or voice. It could be argued that a similar pattern of results can be observed in reaction time experiments comparing familiarity and semantic decision times for faces and printed names, since, in these cases too, name recognition is generally easier (or at least faster) than face recognition (Young et al., 1986a, b). However, the differences reported in Table 4 seem too sizeable to be considered as reflecting a difference in the difficulty of tasks requiring face, voice and name recognition. More complex interpretations must be advanced to explain this puzzling set of data.
The first interpretation is that the patient has three separate problems: (i) (mild) damage to the person-semantic system, which impairs person recognition in all modalities and accounts for the deficit in name definition reported in Table 4; (ii) impaired access to knowledge from the FRUs; (iii) impaired access to personal information from the voice recognition units. An objection to this interpretation is that the hypothesis of independent disruption of two unimodal (visual and auditory) recognition systems is not parsimonious. However, if we assume that the pathways that provide access to stored knowledge about people from voices and faces are located close together, then C.O. could easily have suffered damage to both.
The second and third interpretations acknowledge that C.O. may have mild damage to the person-semantic system, but give a more parsimonious account of his very impaired access to this knowledge, through both face and voice. The second interpretation is that, before accessing the personal semantic information, unimodal recognition subsystems must converge into a non-verbal multimodal person-recognition system and that the right anterior temporal lobe plays a crucial role in this integrative activity. This interpretation is consistent both with empirical data and with some theoretical neurobiological and cognitive models. From the empirical point of view, it is supported by a recent activation study (Nakamura et al., 2001) that has shown that the right temporal pole is part of a neural network involved in the recognition of familiar voices, and by clinical data (Ellis et al., 1989; Van Lanker et al., 1989) showing that familiar voice recognition is impaired by right but not by left brain damage. From the theoretical point of view, this interpretation is in keeping with: (i) Damasio’s neurobiological model, which assumes that the temporal poles may be considered as higher-order convergence zones that bind together the different components of a concept’s distributed representation (Damasio, 1989, 1990); (ii) the IAC (interactive activation and competition network) model (Burton et al., 1990; Burton and Young, 1998), which is a recent extension of the cognitive model of person recognition of Bruce and Young (1986). In this model, personal information is not stored in PINs but is simply accessed via the PINs, which are considered as nodes that allow access to semantic information about person identity. Viewing PINs as gateways to semantic information held in a functionally separate store may be consistent with our suggestion that there is a point of convergence between different modes of recognition before semantic access.
The last interpretation is that the FRUs have privileged access to the PINs and that the other recognition subsystems require coactivation of the FRUs to access person-specific semantic information. This interpretation is supported by two lines of experimental evidence: (i) data which have shown that, in normal subjects, voice recognition is a much slower and more error-prone process than face recognition (Ellis et al., 1997; Schweinberger et al., 1997); and (ii) data reported by Hanley et al. (1998, 2000) which show that, when compared with famous faces, famous voices elicit a much higher percentage of ‘familiar-only’ states, in which listeners experience a feeling of familiarity but are unable to retrieve any further information about the famous person.
These last two interpretations, which stress the correlations between results obtained in the visual/face modality and the auditory/voice modality, are both in keeping with results of our study assessing the C.O.’s consistency of errors across the face and voice modalities. Furthermore, both interpretations support the existence of an ordered sequential progression of the familiar people-recognition disorder in patients with selective atrophy of the right temporal lobe. The first stage of this progression, due to the specific visual recognition properties of the infero-anterior parts of the temporal lobes, should consist of progressive disruption of the FRUs, leading to a selective form of associative prosopagnosia. The second stage results from the increasing difficulty in coactivating partially functioning FRUs or in integrating them in a partly effective multimodal person recognition system. This stage should be characterized by inability to access the person-specific semantic knowledge not only through face recognition but also through the voice or the other non-verbal person recognition modalities. The final stage should consist of complete inability to access (or complete disruption of) the person-specific semantic knowledge.
It is not yet possible to check the validity of this model of disease progression against a sufficient body of clinical data. However, (i) a longitudinal study of disorders of familiar people recognition associated with a selective right temporal lobe atrophy has been attempted in a small number of patients, namely V.H. (Evans et al., 1995), Maria (Gentileschi et al., 1999), Emma (Gentileschi et al., 2001) and C.O. (this study); (ii) in patient V.H., access to person-specific semantic knowledge has been evaluated in objective tests through the person’s face and name, but not through his or her voice; (iii) in patients Maria and Emma the pattern of disease progression has been studied retrospectively but not by means of objective tests. In spite of all these caveats, data obtained in these longitudinal studies seem rather consistent with the model. Patient V.H. (Evans et al., 1995) was studied twice, with an interval of 6–9 months between the first and the second assessments. In the first assessment it was noted that she did not recognize familiar actors in films and had to rely on voice or other non-facial characteristics to aid recognition. On the objective tests, famous face identification was severely impaired, whereas identification from the name was only mildly impaired. In the second assessment, not only was her ability to identify famous faces worse, but also her capacity to provide detailed information about the person corresponding to a given name was severely impaired.
In the description of the patient Maria, Gentileschi et al. (1999) noted that in the first year after onset her recognition ability seemed to benefit from hearing the voice of the unrecognized person, but that by the end of the first year her impaired recognition no longer benefited from hearing the person’s voice or from other non-facial characteristics. Even at this stage, however, Maria had no difficulty retrieving the relevant biographical information when given the name of the unrecognized familiar person. Slightly different is the description of the disease progression in the patient Emma, since, according to the retrospective data gathered by Gentileschi et al. (2001), this patient’s recognition disorder never benefited from hearing the voice or inspecting other non-facial characteristics of the unrecognized person. This patient too, however, was helped in the first stages of her disease by being given the names of the unrecognized people, a benefit that vanished by the end of the first year after onset.
Taken together, these data seem to show that: (i) in the initial stages of the disease the recognition disorder affects mainly the facial channel and has the characteristics of associative prosopagnosia; (b) in the ensuing stage the ability to compensate for the face recognition disorder by the use of other sensory modalities vanishes, but the subject is still able to access person-specific information through the person’s name; (iii) in later stages even this capacity to access the person-specific semantic knowledge through the person’s name is lost.
This general interpretation, which points to the primacy of the visual/face (with respect to the semantic/PINs) aspects of the disorders of familiar person recognition, is supported by the very good scores obtained by C.O. when requested to provide the names of famous towns from their verbal definitions. The contrast between these results and the mildly abnormal scores obtained when verbal definitions were used to find the name of famous persons (Table 3) is not consistent with a semantic account of the disorder of familiar person recognition shown by C.O. Indeed, several authors (e.g. Cohen and Burke, 1993; Valentine et al., 1996; Semenza, 1997) have stressed the similarity between the semantic properties of persons and places (whose proper names refer to unique entities and have a one-to-one relationship with their referent), and other authors (e.g. McKenna and Warrington, 1980; Semenza and Zettin, 1989; Lucchelli and De Renzi, 1992) have stressed the frequent co-occurrence of anomia for persons and for geographical locations.
On the other hand, a similar dissociation between impaired capacity to name or recognize familiar persons and spared ability to name or recognize other instances of unique entities has been reported in other patients, such as V.H. (Evans et al., 1995) and Maria (Gentileschi et al., 1999), who have selective right temporal lobe atrophy.
Taken together with the observations of Miceli et al. (2000), which point to a loss of person-specific semantic information even in patients with lesions encroaching upon the anterior parts of the left temporal lobe, these data suggest a bilateral but asymmetrical distribution of person-specific semantic knowledge. In the anterior parts of the right temporal lobe, this semantic network should be linked mainly to the non-verbal (in particular to the facial) person-recognition units, whereas in the homologous regions of the left hemisphere it should be based on proper linguistic knowledge and subserve many instances of proper name anomia (Damasio, 1996; Fukatsu et al., 1999). Although the hypothesis of two separate person-semantic systems in both the right and the left hemisphere may seem unparsimonious, a similar claim has already been made in a small number of previously published papers (e.g. Eslinger et al., 1996) on the basis of patients who were better at recalling biographical information about people from their name than their face, and vice versa.
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