Edited by: Hauke R. Heekeren, Max Planck Institute for Human Development, Germany
Reviewed by: Oliver C. Schultheiss, Friedrich Alexander University, Germany; Shozo Tobimatsu, Kyushu University, Japan
*Correspondence: Guido Gainotti, Center for Neuropsychological Research, Department of Neurosciences, Policlinico Gemelli, Catholic University of Rome, Largo A. Gemelli, 8, 00168 Roma, Italy. e-mail:
This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.
In the study of prosopagnosia, several issues (such as the specific or non-specific manifestations of prosopagnosia, the unitary or non-unitary nature of this syndrome and the mechanisms underlying face recognition disorders) are still controversial. Two main sources of variance partially accounting for these controversies could be the qualitative differences between the face recognition disorders observed in patients with prevalent lesions of the right or left hemisphere and in those with lesions encroaching upon the temporo-occipital (TO) or the (right) anterior temporal cortex. Results of our review seem to confirm these suggestions. Indeed, they show that (a) the most specific forms of prosopagnosia are due to lesions of a right posterior network including the occipital face area and the fusiform face area, whereas (b) the face identification defects observed in patients with left TO lesions seem due to a semantic defect impeding access to person-specific semantic information from the visual modality. Furthermore, face recognition defects resulting from right anterior temporal lesions can usually be considered as part of a multimodal people recognition disorder. The implications of our review are, therefore, the following: (1) to consider the components of visual agnosia often observed in prosopagnosic patients with bilateral TO lesions as part of a semantic defect, resulting from left-sided lesions (and not from prosopagnosia proper); (2) to systematically investigate voice recognition disorders in patients with right anterior temporal lesions to determine whether the face recognition defect should be considered a form of “associative prosopagnosia” or a form of the “multimodal people recognition disorder.”
Selective analysis of faces is certainly the most powerful channel we have for recognizing familiar people and deriving important information about known or unknown persons, such as their emotional state, age, race, and gender. This is why the term “prosopagnosia,” which was considered a form of visual agnosia specifically affecting face recognition, has played such a dominant role in the study of defective recognition and identification of familiar people since Bodamer's (
Regarding the first point, some authors (e.g., Lhermitte et al.,
Regarding the second point, the debate revolves around De Renzi et al.’s (
Regarding the problem of the mechanisms underlying face recognition disorders, most authors agree that prosopagnosia is due to a defect in the holistic/configurational processing of faces (Yin,
The difficulty of answering all of these questions is increased because prosopagnosia can be provoked by lesions in various parts of a bilateral network of cortical areas spanning from the inferior occipital areas [occipital face area (OFA) of Gauthier et al.,
We believe that two main sources of variance at least partially account for these controversies. The first concerns the hemispheric side of the lesion in patients with posterior temporo-occipital (TO) injuries. In patients with left TO lesions, face recognition disorders can be part of a general visual recognition defect (or “visual object agnosia”) in which the ability to access conceptual and person-specific semantic information from the visual modality is impaired; instead, in patients with right TO lesions the visual recognition disorder selectively concerns faces and seems due to a defect of a specific (configurational) form of visual processing.
Because both forms of visual agnosia can coexist in patients with bilateral lesions, there is the risk of attributing visual recognition disorders due to the concomitant left TO lesion to the mechanism responsible for prosopagnosia.
The second source of variance concerns the intrahemispheric locus of lesion and the nature of the people recognition defect in patients with right hemisphere damage. In fact, if disorders are circumscribed to the visual modality in patients with lesions encroaching upon the TO areas of this hemisphere, in those with lesions involving the right anterior temporal structures, people recognition disorders are multimodal, because they consistently affect familiar faces, voices, and names (see Gainotti,
There are several important differences between “prosopagnosia” proper, resulting from right TO lesions, and the face recognition disorders that are sometimes observed in a context of “visual object agnosia” in patients with left TO damage. On one hand, these differences concern the impact of associative or semantic disturbances on the pathophysiology of visual recognition disorders resulting from left and right TO lesions and, on the other hand, the mode of stimulus processing disrupted in patients with left and right TO lesions. Regarding the first point, several authors (e.g., McCarthy and Warrington,
A final difference between the recognition disorders observed in patients with left and right TO lesions is that, due to the social relevance of distinguishing well known from unfamiliar people, an early step in the recognition of a known person concerns the emergence of familiarity feelings. These feelings are usually absent or very mild in the process of object recognition (with the possible exception of personal owning), but contribute in the process of person recognition by focusing attention on known faces and gathering additional, confirmatory information about them (Atkinson and Juola,
Several pioneering authors (e.g., Albert et al.,
Patient | Anatomical lesion | Symptomatology |
---|---|---|
Vid. (Pillon et al., |
Hemorrhagic infarct in the territory of the left PCA | Right homonimous hemianopia, pure alexia, normal matching of objects and pictures but inability to categorize and show the use of visually presented objects. |
CARJ (Ferro and Santos, |
Infarct in the territory of the left PCA, involving the lower temporo-occipital areas | Right homonimous hemianopia, severe alexia, normal drawing by copy. Inability to categorize pictures of objects and to mime their use. |
Patient of Feinberg et al. ( |
Infarct of the left PCA, involving the left occipital lobe, the inferior posterior mesial temporal lobe, and the splenium | Right homonimous hemianopia, alexia, and combined visual and tactile agnosia. Could not name, describe, or show the use of objects presented visually or tactually, but could perfectly copy figures. |
FRA (McCarthy and Warrington, |
Infarct in the territory of the left PCA, involving the lower part of the occipital lobe | Right homonimous hemianopia, alexia, spared high level visual abilities but impaired categorization and visual matching of objects and pictures taken from a different view. |
Patient of Gallois et al. ( |
Infarct of the left PCA, involving the mesial part of the occipital and temporal lobes, and the splenium | Right homonimous hemianopia, alexia, and sparing of high level visual abilities but impaired categorization and visual matching of pictures of objects taken from different views. |
Patient 1 (Feinberg et al., |
Infarct of the left PCA, involving the mesial part of the occipital and temporal lobes | Right homonimous hemianopia, alexia, and impairment of visual object recognition (naming and demonstrating their use) in spite of spared high level visual abilities. |
Patient 2 (Feinberg et al., |
Infarct of the left PCA, involving the mesial part of the occipital and temporal lobes, and the splenium | Right homonimous hemianopia, alexia, and impairment of visual object recognition with inability to name and pantomime. Sparing of high level visual abilities. |
Patient 3 (Feinberg et al., |
Infarct of the left PCA, involving the mesial part of the occipital and temporal lobes | Right homonimous hemianopia, alexia, and impairment of visual object recognition with inability to name and pantomime objects. Sparing of high level visual abilities. |
The data reported in Table
From a neuropathological point of view, all of these patients had suffered an infarct in the territory of the left posterior cerebral artery (PCA), which involved the inferior and mesial parts of the occipital and temporal lobes and, in some cases, the splenium of the corpus callosum.
These findings were also confirmed by results of systematic investigations (e.g., De Renzi et al.,
Patient | Anatomical lesion | Symptomatology | Face processing | Familiarity feelings |
---|---|---|---|---|
AC (Tzavaras et al., |
Fluent aphasia, severe memory disorders. Associative prosopagnosia | Not studied | Spared | |
DN (Mattson et al., |
Visual acuity 20/70. Integrative prosopagnosia. Moderate visual disorders. Correct but slow unfamiliar faces matching | Feature-by-feature analysis? | Impaired | |
Subject 015 (Barton, |
Impairment in recognizing line drawings of objects. Prosopagnosia with severe defect on the Benton FRT. Poor familiarity and recall of person-specific semantic information from names | Global processing less impaired than feature processing | Mildly impaired (as with names) | |
Two patients (Damasio et al., |
Left occipital lesions | “Deep prosopagnosia,” “Semantic errors” in face recognition (subjects with semantic features in common with the targets) | Not studied | Spared |
RC (Carlesimo et al., |
Left occipital (+lower half splenium) | Associative visual agnosia. Associative prosopagnosia with impaired identification (3/20 = 15%) from faces | Not studied | Relatively spared (15/20 = 75%) |
EY (Verstichel and Chia, |
Left occipital infarct | Right superior hemianopia. Alexia without visual agnosia. Impaired people identification from face (11/38 = 30%) | Not studied | Spared (20/20 = 100%) |
DBO (Anaki et al., |
Left occipital infarct | Associative visual agnosia. Associative prosopagnosia with inability (9/24 = 37%) to access semantic information about known faces | Configural processing unimpaired | Spared (19/24 = 80%) |
Three main observations can be made from the data presented in Table
On the other hand, since the advent of neuroimaging, several studies have shown that when prosopagnosia is due to unilateral lesions these lesions usually encroach upon the right TO areas. Therefore, in Table
Patient | Anatomical lesion | Symptomatology | Face processing | Familiarity feelings |
---|---|---|---|---|
Michel et al. ( |
Right occipital hematoma | Left hemianopia. Moderate prosopagnosia. No visual agnosia | Not studied | Clinically impaired (stranger) |
Patient 1 (Charnallet et al., |
Large right occipital hemorrhagic infarct | Left hemianopia. Moderate prosopagnosia without visual agnosia | Not studied | Moderately impaired |
Patient 1 (De Renzi, |
Right PCA infarct | Left hemianopia. Severe prosopagnosia. No visual agnosia | Not studied | Impaired |
Patient 2 (De Renzi, |
Right PCA infarct | Left hemianopia. Severe prosopagnosia with visual agnosia | Not studied | Impaired |
BM (Sergent and Villemure, |
Right hemispherectomy | Severe prosopagnosia. No visual agnosia | Defective configural processing | Impaired |
LH (Levine and Calvanio, |
Right temporal lobectomy with subcortical lesions in the parieto-occipital white matter | Severe prosopagnosia. Relatively spared visual perception, but impaired recognition of living beings. Person recognition spared through other modalities | Defective configural processing | Very impaired |
PC (Sergent and Signoret, |
Right occipito-temporal hemorrhage | Associative prosopagnosia with relatively spared visual perception | Unimpaired configural processing | Impaired |
PM (Lhermitte and Pillon, |
Right occipital resection for AVM | Severe prosopagnosia. No signs of visual agnosia | Defective configural processing | Impaired |
RM (Sergent and Signoret, |
Ruptured temporo-occipital aneurysm | Severe prosopagnosia with very impaired visual perception | Defective configural processing | Impaired |
PA (De Renzi et al., |
Right PCA infarct | Left upper quadrantanopsia. Severe apperceptive prosopagnosia (7/32 = 22%) | Not studied | Impaired (13/36 = 36%) |
OR (De Renzi et al., |
Right temporo-parieto-occipital infarct | Left visual field defects. Severe prosopagnosia (12/32 = 37%) without visual object agnosia | Not studied | Impaired (17/36 = 47%) |
LM (De Renzi et al., |
Right PCA infarct | Left upper quadrantanopsia. Moderate prosopagnosia (8/20 = 40%) | Not studied | Impaired (9/20 = 45%) |
Patient 3 (Takahashi et al., |
Right temporo-occipital infarct | Lack of identification and memory from faces. Good recognition from voice. No visual perceptual defects | Not studied | Impaired |
CR (Gauthier et al., |
Micro-abscesses of the right temporal and occipital lobes | Prosopagnosia with impaired recognition of living beings. Prevalent left fusiform activation while viewing faces | Local over global processing advantage | Not tested |
Patient 5 (Barton et al., |
Right medial occipital stroke | Left hemianopia. Moderate perceptual face defects. Moderate prosopagnosia. Impaired imagery for facial shape | Moderate configural processing defect | Impaired (many false alarms) |
Patient 6 (Barton et al., |
Right occipital lobectomy for tumor resection | Left hemianopia. Severe perceptual face defects. Moderate prosopagnosia. Impaired imagery for facial shape | Severe defect of configural processing | Impaired (many false alarms) |
DE (Verstichel, |
Right occipital hematoma | Visual agnosia + severe prosopagnosia (8/28 = 29%) | Not studied | Impaired (5/11 = 45%) |
Wada and Yamamoto ( |
Right occipital hematoma | Left hemianopia. Severe prosopagnosia. No visual agnosia. | Not studied | Impaired (stranger) |
Patient 2 (Uttner et al., |
Right PCA infarct | Left hemianopia. Severe apperceptive Prosopagnosia. No visual agnosia | Not studied | Impaired (stranger) |
FB (Riddoch et al., |
Embolization of a right temporo-occipital AVM | Severe prosopagnosia with a perceptual defect limited to face processing and intact subordinate object recognition | Partial defect of configural processing | Very impaired |
The data reported in Table
Some authors (e.g., Sergent and Signoret,
One of the most striking differences that emerged from this review (and from many previous studies) between the face identification disorders of patients with left TO lesions and of right prosopagnosic patients was the disruption of face processing based on a local, feature-by-feature analysis in patients with left TO lesions and of global, configurational encoding in those with right-sided lesions. This is consistent with the documented importance (e.g., Bradshaw and Nettleton,
One of the most striking results of our comparison between the characteristics of patients with face recognition or identification disorders resulting from right and left TO lesions concerns the study of face familiarity feelings. In fact, these feelings were relatively or completely spared in patients with left TO lesions and systematically impaired in right prosopagnosic patients. It is interesting that the loss of face familiarity feelings is not only considered a hallmark of prosopagnosia by authorities such as Ellis and Young (
In the last part of the Section
Patient | Anatomical lesion | Symptomatology | Person recognition through | Familiarity feelings | |
---|---|---|---|---|---|
voice | name | ||||
M.me V. (Boudouresques et al., |
HSE with massive damage of the anterior parts of the right temporal lobe | Selective defect of familiar people recognition. Unaware or poor voice recognition | Impaired | Not tested | Not tested |
LP: Patient 5 (De Renzi, |
HSE with lesion of the anterior and inferior parts of the |
Severe defect of familiar people recognition and semantic memory disorders (mainly for vegetables) | Impaired | Impaired | More impaired for faces than for names |
VA: Case 3 (De Renzi et al., |
HSE with lesion confined to the right temporal lobe | Moderate defect of familiar people recognition when seen out of context | Not tested | Not tested | Very impaired for faces |
MT (Schweinberger et al., |
Right temporo-parietal infarct | Severe defect of familiar people recognition from faces (1/18), without signs of visual agnosia. Poor memory for faces, but not for words | Not tested | Impaired (13/18) | Impaired |
VH (Evans et al., |
Diffuse atrophy of the right antero-inferior temporal lobe | Progressive defect recognizing familiar people with mild memory disorders | Initially clinically unimpaired | Normal retrieval of semantic information | Moderate impairment for faces |
Patient 8 (Barton et al., |
Bilateral anterior temporal lobe damage from CHI and right temporal lobe resection | Severe defect of familiar people recognition with impairment on the Benton FRT | Not tested | Not tested | Very impaired for faces |
FG (Joubert et al., |
Prevalent atrophy of the right fusiform gyrus; relative sparing of the anterior temporal cortex | Progressive defect recognizing familiar people with impaired configurational processing | Initially the voice of the person helped recognition | Normal retrieval of semantic information from name | Mildly impaired for faces |
BD (Williams et al., |
Right anterior temporal lobe atrophy | Progressive defect recognizing familiar people, with impaired configurational processing but spared semantic information | Not tested | Normal retrieval of semantic information from name | Moderately impaired for faces |
LR (Bukach et al., |
Traumatic lesion of the right antero-inferior temporal lobe; sparing the fusiform gyrus | Moderate defect of familiar people recognition when seen out of context | Not tested | Not tested | Impaired (many false alarms) |
MT (Nakachi and Muramatsu, |
Atrophy of the right anterior temporal lobe | Selective form of associative prosopagnosia | Spared | Spared | Impaired for faces |
Before discussing the appropriateness of the term “prosopagnosia” to classify the patients reported in Table
Regarding
Regarding the frequency with which
With respect to outcomes of the investigations concerning voice and name recognition,
Results obtained by analyzing
Regarding
Taken together, the data reported in Table
The main results of this review concern, on one hand, the qualitative differences between defects of visual recognition observed in patients with lesions involving the ventral TO structures of the right and left hemisphere and, on the other hand, the distinction between “prosopagnosia” and “multimodal people recognition disorders.” This second point of our review has led us to take into account aspects of familiar people recognition (such as the voice or the name) that clearly exceed the specific issue of prosopagnosia. This was made with two aims in mind: (a) to place the discussion of prosopagnosia in the more general context of familiar people recognition disorders; (b) to stress the need of investigating the other modalities of people recognition before considering a patients with face recognition disorders as an instance of prosopagnosia. In order to clarify the various parts of this discussion, we have reported in Figure
Although important qualitative differences and a different clinical context were observed in face recognition and identification disorders associated with right and left TO lesions, only those resulting from right-sided lesions fully satisfied the criteria of a modality-specific recognition disorder selectively affecting familiar faces (prosopagnosia). This claim is based on the following: (a) the
Patients with left TO lesions can also rarely show defects of familiar people identification, but these defects are usually included in a context of associative visual object agnosia or of more general semantic disorders, as shown by data reported in Tables
This interpretation might also explain why these patients, in whom faces are processed normally in a configurational manner by the right hemisphere, do not show the loss of face familiarity feelings, which is a hallmark of true prosopagnosia.
More generally, the fact that the two markers of prosopagnosia resulting from disruption of the TO structures of the right hemisphere consist of (a) a defect in face configurational processing and (b) a loss of face familiarity feelings, raises the issue about the relationships that might exist between these two right hemisphere processing mechanisms. One hypothesis that might be advanced on this subject could consist in assuming that a sort of functional integration may exist between the coarse holistic treatment of faces performed by the right hemisphere and the emergence of familiarity feelings, aiming to check that the person who has raised these feelings really corresponds to the tentatively identified people. The hypothesis of a link between defective face configurational processing and impaired face familiarity feelings could explain the strong correlation observed in patients with a lesion involving the ventral TO areas of the right hemisphere (reported in Table
This hypothesis could also explain why in patients with a lesion involving the territory of the left PCA (Table
The distinction between “prosopagnosia” and “multimodal people recognition disorders” is probably based on the different functions accomplished in the earliest and in the last stages of face processing by the posterior (TO) and the anterior parts of the right temporal lobe.
According to a classical feed-forward model (Haxby et al.,
In the anterior temporal structures, on the contrary, visual processing output is associated with the output of other sensory modalities and with the mechanisms of episodic and semantic memory.
Impairment of these structures should, therefore, rarely provoke a modality-specific face recognition defect, but rather a multimodal person recognition disorder in which defects of face recognition are sometimes prominent. According to some authors (e.g., Mohedano-Moriano et al.,
In the introductory part of this review, we listed some issues (such as the specific or non-specific manifestations of prosopagnosia, the unitary or non-unitary nature of this syndrome and the mechanisms underlying face recognition disorders) that are still controversial in the study of prosopagnosia. We also suggested that two main sources of variance might be the qualitative differences between the face recognition disorders observed in patients with a prevalent lesion of the right or left hemisphere and in those with a lesion encroaching upon the TO or the (right) anterior temporal cortical areas.
Results of our review confirm that different kinds of face recognition disorders can be observed as a function of the right vs left and of the TO vs (right) anterior temporal lesion location. In fact, they show that the most specific forms of prosopagnosia are due to lesions of a right posterior network, including the OFA and the FFA, whereas (a) the face identification defects observed in patients with left TO lesions seem due to a semantic defect impeding access to the person-specific semantic information from the visual modality and (b) the face recognition defects resulting from right anterior temporal lesions can usually be considered as part of a multimodal people recognition disorder.
From the operational point of view, our results suggest: (a) considering the components of visual agnosia often observed in prosopagnosic patients with bilateral TO lesions as part of a semantic defect resulting from the left-sided lesion (and not of prosopagnosia proper); (b) systematically investigating voice recognition disorders in patients with right anterior temporal lesions to determine whether the patient's face recognition defect should be considered a form of “associative prosopagnosia” or a form of “multimodal people recognition disorder.”
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.