Elsevier

Neuropsychologia

Volume 45, Issue 8, 2007, Pages 1591-1607
Neuropsychologia

Reviews and perspectives
Different patterns of famous people recognition disorders in patients with right and left anterior temporal lesions: A systematic review

https://doi.org/10.1016/j.neuropsychologia.2006.12.013Get rights and content

Abstract

Selective disorders in recognition of familiar people have been described in patients with right and left anterior temporal lesions, but the exact nature of these cognitive impairments remains controversial. A clarification of this issue could have theoretical implications, because, according to Snowden et al. [Snowden, J. S., Thompson, J. C., & Neary, D. (2004). Knowledge of famous faces and names in semantic dementia. Brain, 127, 860–872], the pattern of impairment shown by patients with right and left anterior temporal atrophy is inconsistent with unitary, abstract, amodal models of semantic memory. This pattern could, on the contrary suggest a multimodal network, in which the right and left temporal lobes would mainly process and store visual and, respectively, verbal information.

I tried to clarify this issue by systematically reviewing: (a) all published individual cases of patients showing a prevalent damage of the anterior parts of the right or left temporal lobes and a selective disorder of famous people recognition; (b) all group studies of patients with right or left temporal lobe epilepsy, which had investigated aspects of famous people recognition impairment.

Results of these reviews consistently showed that different patterns of impaired recognition of familiar people can be observed in patients with right and left anterior temporal pathology. These patterns consist of a loss of familiarity feelings and of person specific information retrieval from face stimuli, when the right temporal lobe is damaged and of a prevalent impairment in finding their names when the anterior parts of the left temporal lobe are selectively damaged.

Introduction

Since the early papers of Snowden, Goulding, and Neary (1989) and Hodges, Patterson, Oxbury, and Funnell (1992) it is commonly recognized that in patients with a temporal variant of fronto-temporal degeneration the symptomatology can be very different as a function of the prevalent side of atrophy. These authors have, indeed, described under the name of “semantic dementia” a degenerative syndrome, consisting of severe anomia and progressive loss of semantic memory, concomitant with a selective atrophy of the anterior and infero-lateral parts of the left temporal lobe. These authors have also noticed that when the same temporal lobe structures are affected on the right side of the brain, a progressive impairment in the recognition of familial faces (and more in general of familial people) can be observed.

At a more fine-grained level of analysis, however, the exact nature of these cognitive disorders remains poorly defined. Thus, drawing on recent developments of the early influential papers of Benton (1980) and Warrington and James (1967) some authors (e.g. Tyrrel, Warrington, Frackowiak, & Rossor, 1990; Evans, Heggs, Antoun, & Hodges, 1995; Mendez & Ghajarnia, 2001; Joubert et al., 2003) considered the reported defects in recognition of familiar people as a form of ‘associative prosopagnosia’. However, at least in some patients (e.g. Barbarotto, Capitani, Spinnler, & Trivelli, 1995; Evans et al., 1995; Gentileschi et al., 1999, Gentileschi et al., 2001; Thompson et al., 2004), these disturbances point more to a semantic (cross-modal) defect, selectively affecting familiar people recognition, than to an associative prosopagnosia. Furthermore, a cross-modal disorder of familiar people recognition, affecting various aspects of person-specific knowledge can also be observed in patients with lesions encroaching upon the anterior parts of the left temporal lobe. Patients belonging to this group have often been described as suffering from a proper name anomia (Damasio, Grabowski, Tranel, Hichwa, & Damasio, 1996; Fukatsu, Fujii, Tsikiura, Yamadori, & Otsuki, 1999), but in some patients (e.g., Graham, Pratt, & Hodges, 1998; Miceli et al., 2000; Papagno & Capitani, 2001; Sullivan Giovanello, Alexander, & Verfaille, 2003) a loss of person-specific knowledge better accounts for the patient's symptomatology. Uncertainties concerning the patterns of famous people identification impairment observed in patients with right and left anterior temporal lesions are relevant not only from the clinical, but also from the theoretical point of view. Snowden, Thompson, and Neary (2004) have, indeed, argued that a fine-grained investigation of the person-specific semantic impairment obtainable from visual (face) and verbal (name) stimuli in patients with degenerative lesions of the right and left temporal lobes could contribute to clarify the debate concerning the “unitary” (abstract-amodal) versus “nonunitary” (concrete-multimodal) format of semantic representations. One of the cornerstones of this debate turns, in fact, around the hypothesis that dissociations in access to the semantic representation through the visual and the verbal modalities might be due to the “perceptual affordances” of objects, allowing “priviledged accessibility” from vision to part of the semantic representation (Caramazza, Hillis, Rapp, & Romani, 1990). Snowden et al. (2004) reasoned that, since people's faces and names are arbitrary, the study of person-specific semantic information obtainable from visual (face) and verbal (name) stimuli in patients with degenerative lesions of the right and left temporal lobes could represent a potentially valuable means of addressing the unitary versus nonunitary semantic systems controversy, ruling out the possible influence of the perceptual affordances of objects. Results of their study showed that semantic information accessed through face and name are different according to the prevalent side of atrophy. Semantic dementia patients with predominantly left temporal lobe atrophy identified faces better than names and performed better on the picture than on the word version of the semantic memory “Pyramids and Palm Trees” test (Howard & Patterson, 1992), whereas patients with right temporal lobe atrophy showed the opposite pattern of performance. These data were considered as incompatible with a unitary abstract model of semantic memory. A problem with this study consisted of the fact that, due to the rarity of this disease, the number of patients reported by Snowden et al. (2004) was relatively small (nine patients with a prevalent atrophy of the left temporal lobe and three with greater right temporal atrophy). Paired comparisons between patients with right and left temporal lobe atrophy did, therefore, seldom reach significance because of the very small sample size. Since studies of semantic dementia patients typically involve single case studies, we thought that a strategy allowing to further check the Snowden et al.'s (2004) hypothesis could consist in systematically reviewing all the published individual cases of patients with a prevalent damage to the anterior parts of the right or left temporal lobes, in whom disorders of person recognition were on the foreground. At the same time, since aspects of impaired recognition of famous persons (or of famous faces) have also been investigated in groups of patients with unilateral temporal lobe epilepsy (TLE), before or after anterior temporal lobectomy (Barr, Goldberg, Wasserstein, & Novelly, 1990; Ellis, Hillam, Cardno, & Kay, 1991; Glosser, Salvucci, & Chiaravalloti, 2003; Lah, Grayson, Lee, & Miller, 2004; Seidenberg et al., 2002; Viskontas, McAndrews, & Moscovitch, 2002), a survey of these studies could corroborate (or infirm) results obtained in our review of single-case studies.

The first aim of our review, therefore, consisted of trying to provide a consistent, fine-grained description of the patterns of impaired recognition of familiar people that can be observed in patients with right and left anterior temporal pathology. Furthermore, taking into account various aspects and models of person recognition disorders, our review could also contribute to clarify some aspects of this problem that are still controversial.

One of these issues concerns the functional architecture of current models of person identification, whereas a second issue concerns the specificity of person recognition disorders.

As for the first point, all the models of person recognition agree that several cognitive and subjective/behavioural stages are involved in the process of recognizing and accessing information about people, but disagree on more specific points. From the cognitive point of view, the stages identified by these models involve: (1) the formation of a structural description of a seen face, which is compared with all the known faces contained in the Face Recognition Units (FRUs). The same holds for voices and names, which are deemed to be stored in similar Voice Recognition Units (VRU) or Name Recognition Units (NRU); (2) the convergence of information stored in these modality-specific units into person-identity nodes (PINs), allowing recognition of a particular person and activation of the corresponding semantic information; (3) the retrieval of the corresponding biographical knowledge; (4) the production of the person's proper name.

From the subjective/behavioural viewpoint, the first stage consists of a feeling of familiarity of the perceived person, the second stage of retrieving information such as his/her occupation, nationality, and so on, and the third of retrieving and producing the person's name.

These models differ, however, in two important aspects, concerning the locus in which familiarity feelings are generated and in which person-specific information is stored. According to Bruce and Young (1986) face identification model, familiarity feelings arouse in the recognition units where, for instance, the structural description of a seen face is compared to the familiar faces stored in the FRUs. On the contrary, in Burton, Bruce, and Johnston (1990) and Burton, Bruce, and Hancock (1999), Brédart, Valentine, Caldor, and Gassi (1995) and Valentine, Brennen, and Bredart (1996) models, decisions about familiarity are taken at a supra-modal level, namely the PINs, where information from different modalities is combined in person-identity nodes. Furthermore, according to Bruce and Young's (1986) model, PINS store semantic information, whereas according to Burton et al., 1990, Burton et al., 1999, Brédart et al. (1995) and Valentine et al. (1996), PINs do not store semantic information, but provide a modality-free gateway to a single system, where semantic information about people is stored in an amodal format. A flow diagram stressing the main differences between the model of Bruce and Young (1986) and those of Burton et al., 1990, Burton et al., 1999, Brédart et al. (1995) and Valentine et al. (1996) is reported in Fig. 1.

These two different models could make different predictions as for the dissociation or co-occurrence of familiarity feelings, generated by face and name of the same person. A frequent independence could be predicted by a modality-specific locus of familiarity judgment, whereas a co-occurrence could be predicted by a supra-modal locus of familiarity decision. A second aim of our review, therefore consisted in evaluating: (a) if in patients with a prevalent damage to the anterior parts of the right and left temporal lobes familiarity judgments in response to face and name cues usually co-occur or dissociate; (b) if in right and left temporal lobe patients with a relatively intact familiarity judgment, a similar amount of semantic information can be retrieved in response to face and name cues, as predicted by models assuming that PINs provide a modality-free gateway to a single amodal person-specific semantic system (Haslam, Cook, & Coltheart, 2001).

The last aim of our investigation (which concerned only the survey of single-case studies) consisted in evaluating if familiar people recognition disorders selectively affect the famous people category or also concern other instances of “uniques entities”, such as towns or monuments. Damasio et al. (Damasio, 1989, Damasio, 1990; Damasio, Damasio, Tranel, & Brandt, 1991) have, indeed, repeatedly suggested that the rostral regions of the temporal lobes may act as “convergence zones” binding together the distributed representations of concepts and that this mechanism may mainly concerns “unique entities” (i.e., persons and landmarks). A development of this model, consistent with a nonunitary account of the semantic representations, has been more recently advanced by the same group (Damasio et al., 1996; Damasio, Tranel, Grabowski, Adolphs, & Damasio, 2004; Grabowski et al., 2001, Grabowski et al., 2003; Tranel, 2006; Tranel, Damasio, & Damasio, 1997). This hypothesis assumes that retrieval of words denoting “unique entities’ relies upon left temporal polar regions whereas retrieval of conceptual knowledge pertaining to the same entities depends upon right temporal polar regions. This second hypothesis could suggest that knowledge of persons and of monuments are often correlated, but only in the visual modality in right and in the verbal modality in left temporal lobe patients.

The set of predictions made in the present review can, therefore, be summarized as it follows:

  • 1.

    If semantic information is stored in a unitary abstract system, then person-specific semantic knowledge, accessed through face and name should be roughly comparable in patients with right and left anterior temporal lesions. If, on the contrary, the right hemisphere semantic knowledge is mainly based upon an integration between visual and other perceptual information, whereas the left hemisphere semantic knowledge is mainly coded in linguistic terms (Gainotti, 2006, Snowden et al., 2004), then the amount of retrievable person-specific semantic knowledge should be greater from name in right and from face in left temporal lobe patients.

  • 2.

    If familiarity decisions are taken at the PINs’ level, then there should be a good agreement between familiarity judgments obtained from famous faces and names, irrespective of the side of lesion. If, on the contrary, they are made at the level of the modality-specific recognition units, then familiarity judgments could be dissociated, being mainly lost for faces in right and for names in left temporal lobe patients.

  • 3.

    If the PINs are simply a modality-free gateway to a single person-specific semantic system, then in patients with a relatively intact familiarity judgments the same amount of semantic information should be obtained in response to face and name, irrespectively of the side of temporal lobe damage.

  • 4.

    If famous people recognition disorders are only an instance of a more general defect in identification of “unique entities”, then impaired recognition of famous people and of other “unique entities” should usually coexist and be modality-independent.

Section snippets

General methodology

The present review was conducted on all single-case studies and on all group studies, found in the neuropsychological literature in the last 20 years that had investigated various aspects of famous persons identification disorders in patients with a prevalent or selective lesion of the anterior parts of the right or left temporal lobes. The time period of the last 20 years was chosen because the report of patients submitted to a detailed study of familiar people recognition disorders, including

Familiarity decisions about famous faces and names

Table 2 analytically reports the familiarity judgments about famous faces and names expressed by individual patients with right and left temporal lobe lesions.

Familiarity data were not reported in two patients (4, 11) with right temporal lesions (RTL) and in seven (26, 27, 28, 34, 35, 37 and 38) with left temporal lesions (LTL). Within the 19 R and 10 L patients in whom familiarity judgments had been studied, this variable was more frequently impaired in R (16/19: 84 percent) than in L (4/10:

Discussion

The aim of the present review of impaired recognition of famous people and of other “unique entities” by patients with right and left anterior temporal lobe lesions was two-fold. The first, more clinical purpose consisted in trying to give a fine-grained description of the patterns of impaired recognition of familiar people shown by patients with lesions encroaching upon the anterior parts of the right and left temporal lobes. The second, more ambitious purpose aimed to clarify theoretical

References (84)

  • G. Gainotti

    A metanalysis of impaired and spared naming for different categories of knowledge in patients with a visuo-verbal disconnection

    Neuropsychologia

    (2004)
  • G. Gainotti

    Anatomical, functional and cognitive determinants of semantic memory disorders

    Neuroscience and Biobehavioural Reviews

    (2006)
  • M.L. Gorno-Tempini et al.

    Cognitive and behavioural profile in a case of right anterior temporal lobe degeneration

    Cortex

    (2004)
  • T.J. Grabowski et al.

    Residual naming after damage to the left temporal pole: A PET activation study

    Neuroimage

    (2003)
  • C. Haslam et al.

    Biographical knowledge: Modality specific or modality-neutral?

    Cortex

    (2004)
  • M. Hittmair-Delazer et al.

    Anomia for people's names

    Neuropsychologia

    (1994)
  • J. Hodges et al.

    A reversal of the temporal gradient for famous person knowledge in semantic dementia: Implications for the neural organisation of long-term memory

    Neuropsychologia

    (1998)
  • R. Jackendoff

    On beyond zebra: The relation of linguistic and visual information.

    Cognition

    (1987)
  • S. Lah et al.

    Memory for the past after temporal lobectomy: Impact of epilepsy and cognitive variables

    Neuropsychologia

    (2004)
  • M.A. Lambon Ralph et al.

    Is a picture worth a thousand words? Evidence from concept definitions by patients with semantic dementia

    Brain and Language

    (1999)
  • R.A. McCarthy et al.

    Actors but not scripts: The dissociation of people and events in retrograde amnesia

    Neuropsychologia

    (1992)
  • C. Papagno et al.

    Proper name anomia: A case with sparing of the first-letter knowledge

    Neuropsychologia

    (1998)
  • C. Papagno et al.

    Slowly progressive aphasia: A four-year follow-up

    Neuropsychologia

    (2001)
  • M. Reinkemeier et al.

    Differential impairments in recalling people's names: A case study in search of neuroanatomical correlates

    Neuropsychologia

    (1997)
  • M.C. Saetti et al.

    The nature of the disorder underlying the inability to retrieve proper names

    Cortex

    (1999)
  • M. Seidenberg et al.

    Recognition and identification of famous faces in patients with unilateral temporal lobe epilepsy

    Neuropsychologia

    (2002)
  • S.A. Thompson et al.

    Dissociating person-specific from general semantic knowledge: The roles of the left and right temporal lobes

    Neuropsychologia

    (2004)
  • D. Tranel et al.

    A neural basis for the retrieval of conceptual knowledge

    Neuropsychologia

    (1997)
  • P. Verstichel

    Hyperfamiliarité stereotypée pour les visages au cours d’une démence fronto-temporale avec prosopagnosie

    Revue Neurologique (Paris)

    (2005)
  • E.K. Warrington et al.

    The fractionation of retrograde amnesia

    Brain and Cognition

    (1988)
  • E.K. Warrington et al.

    An experimental investigation of facial recognition in patients with unilateral cerebral lesions

    Cortex

    (1967)
  • M.S. Albert et al.

    Temporal gradients in the retrograde amnesia of patients with alcoholic Korsakoff's disease

    Archives of Neurology

    (1979)
  • D.A. Allport

    Distributed memory, modular systems and dysphasia

  • R. Barbarotto et al.

    Slowly progressive semantuc impairment with category specificity

    Neurocase

    (1995)
  • A.L. Benton

    The neuropsychology of face recognition

    American Psychologist

    (1980)
  • S. Brédart et al.

    An interactive activation model of face naming

    Quarterly Journal of Experimental Psychology

    (1995)
  • V. Bruce et al.

    Understanding face recognition

    British Journal of Psychology

    (1986)
  • A.M. Burton et al.

    Understanding face recognition with an interactive activation model

    British Journal of Psychology

    (1990)
  • A. Caramazza et al.

    The multiple semantic hypothesis: Multiple confusions?

    Cognitive Neuropsychology

    (1990)
  • H.B. Coslett et al.

    Preserved object recognition and reading comprehension in optic aphasia

    Brain

    (1989)
  • A.R. Damasio et al.

    Neural regionalization of knowledge access: Preliminary evidence

  • H. Damasio et al.

    A neural basis for lexical retrieval

    Nature

    (1996)
  • Cited by (0)

    View full text